OCEANOGRAPHY and MARINE BIOLOGY: AN ANNUAL REVIEW (Volume 44) - Chapter 6 ppsx

277
Oceanography and Marine Biology: An Annual Review, 2006, 44, 277-322
© R. N. Gibson, R. J. A. Atkinson, and J. D. M. Gordon, Editors
Taylor & Francis
TAXONOMY, ECOLOGY AND BEHAVIOUR
OF THE CIRRATE OCTOPODS
MARTIN A. COLLINS
1
& ROGER VILLANUEVA
2
1
British Antarctic Survey, Natural Environmental Research Council,
High Cross, Madingley Road, Cambridge, CB3 0ET, U.K.
E-mail:
2
Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas (CSIC),
Passeig Marítim de la Barceloneta 37-49, E-08003 Barcelona, Spain
E-mail:
Abstract The cirrate octopods are deep-sea, cold-adapted cephalopod molluscs that are found
throughout the world’s oceans, usually at depths in excess of 300 m, but shallower in cold water
at high latitudes. The gelatinous bodies of the cirrates, which deform when preserved, coupled with
low capture rates have caused considerable confusion in the systematics of the group. The taxo-
nomically relevant morphological features are briefly reviewed and the taxonomy revised. On the
basis of morphological and molecular information the cirrates are divided into four families, the
Cirroteuthidae (including the genera Cirroteuthis, Cirrothauma and Stauroteuthis), Cirroctopodidae
(Cirroctopus), Grimpoteuthidae (Cryptoteuthis, Grimpoteuthis and Luteuthis) and Opisthoteuthidae
(Opisthoteuthis). A total of 45 species are recognised. The opisthoteuthids are primarily benthic
animals, the grimpoteuthids and cirroctopodids benthopelagic and the cirroteuthids essentially
pelagic, but generally close to the sea floor. With the exception of two common, shallow, Opistho-
teuthis species, the biology of the cirrates is poorly studied. The data on reproductive biology indicate
that spawning is extended, with growth continuing during a reproductive period that probably

occupies much of the life cycle, an unusual strategy in cephalopods. Diet studies suggest that benthic
cirrates feed on small-sized organisms with low swimming speeds and the main prey are amphipods
and polychaetes. Cirrate predators include sharks, teleost fishes, fur seals and sperm whales. Behav-
ioural observations, based on underwater photographs, submersible observations and aquarium
studies, show a range of postures, modes of locomotion and responses to disturbance that differ
between the families. Behavioural observations also help interpret the unusual morphology and
physiology of the cirrates, such as the use of cirri, fins, secondary web and bioluminescent emissions.
Introduction
The cirrate octopods are deep-sea cephalopod molluscs, possessing a semigelatinous body, paired
fins, well-developed web, a large internal shell and paired cirri between a single row of suckers.
The morphology of the cirrates indicates that the group are relatively primitive, with similarities
to ancestral octopods (Young et al. 1998). However, molecular studies of cephalopod evolution
have produced mixed results, with no clear monophyly in the Octopoda (incirrates and cirrates)
and the suggestion of polyphyly in the cirrates (Carlini et al. 2001, Lindgren et al. 2004).
The cirrates are known from all oceans, typically at depths of 300–7000 m, but are found
shallower in cold waters at high latitudes (Voss 1967, 1988a) and include some of the largest
© 2006 by Taylor & Francis Group, LLC
MARTIN A. COLLINS & ROGER VILLANUEVA
278
invertebrates in the deep sea. They are usually caught in small numbers, are extremely fragile and
easily damaged on capture, and often distort during preservation. Many of the early descriptions
of species, genera and families were based on small numbers (often one) of badly damaged and
poorly preserved specimens (e.g., Cirroteuthis muelleri (Eschricht 1836), Cirrothauma magna
(Hoyle 1885), Grimpoteuthis umbellata (Fischer 1883), Opisthoteuthis massyae (Grimpe 1920)).
These factors have led to considerable confusion in the taxonomy of the group, with debate about
which characters should be used to separate genera and families and consequently the classification
of the cirrates has been in an almost constant state of flux, with species being moved between
genera and genera between families (e.g., Robson 1930, Nesis 1987, Voss 1988a, Sweeney & Roper
1998). Studies of the morphology of the cirrates have, with a small number of exceptions (Meyer
1906, Ebersbach 1915, Robson 1932, Aldred et al. 1983), been limited to brief taxonomic descrip-

tions and some of the early detailed studies have been confounded by confusion over the definition
of structures and of the species being examined.
The development of new technology, allowing access to the deep sea (e.g Roper & Brundage
1972, Villanueva et al. 1997) and the extension of commercial fishing into deeper water (Boyle
et al. 1998), has stimulated renewed interest in this enigmatic group in the last 20 yr. Much of the
recent work has focused on taxonomy and distribution (e.g., O’Shea 1999, Collins et al. 2001a,
Villanueva et al. 2002, Collins 2003), ecology of the relatively shallow species (e.g., Villanueva &
Guerra 1991, Boyle & Daly 2000) and in situ behavioural observations from submersibles (Vec-
chione & Young 1997, Villanueva et al. 1997, Johnsen et al. 1999a,b). Correct identification is
important to all studies, but taxonomic work has been handicapped by the poor state of type
specimens, rather confused literature and problems with definitions of anatomical structures.
Ecological studies of the cirrates have, largely through lack of specimens, been limited to
shallow species of the Opisthoteuthis genus, which have been caught as by-catch of commercial
fisheries (Cupka 1970, Vecchione 1987, Villanueva & Guerra 1991, Villanueva 1992a, Boyle et al.
1998, Laptikhovsky 1999, Daly et al. 1998, Boyle & Daly 2000), but little or no ecological work
has been undertaken on the deeper species. The existing data indicate important differences in
reproduction between the cirrate and incirrate octopods, notably in lack of seasonality associated
with spawning and the continuous production of eggs and spermatophores in adult individuals of
the species studied to date.
During recent years in situ and aquaria observations of live cirrates have dramatically changed
our understanding of how these animals use their fins and web to swim and respond to external
disturbance (e.g., Boletzky et al. 1992, Vecchione & Young 1997, Villanueva et al. 1997, Villanueva
2000). These behavioural observations have been indispensable in interpreting the morphological
characteristics of the cirrates, such as the delicate secondary web and the bioluminescent capabilities
(Johnsen et al. 1999a,b), and suggest that future observations on live specimens will produce new
findings and help explain the function of other unusual morphological features such as the areolar
spots and mantle ‘windows’.
Here the taxonomy of the group is reviewed and updated and the limited data on ecology and
behaviour summarised. To underpin the taxonomic review, the first section briefly compares the
anatomy of the different genera and families.

Comparative anatomy
This section is intended to provide the reader with details of the comparative anatomy of the cirrates
to facilitate identification and taxonomic descriptions. For a detailed study of the anatomy of a
cirrate (Cirrothauma murrayi) the reader is referred to Aldred et al. (1983).
The cirrates are essentially deep-water forms, and exhibit a number of characteristics that are
considered modifications to deep-sea life (reduction or loss of radula and posterior salivary glands;
© 2006 by Taylor & Francis Group, LLC
CIRRATE OCTOPODS
279
loss of ink sac; reduction of gills; narrowing of funnel aperture; large eggs), which are shared by deep
incirrate species (Robson 1925, Voss 1988b). The gelatinous nature and few hard parts of the cirrates
mean that preservation can dramatically change the form of the animal, and this has been clearly
demonstrated with whole animals (e.g., Luteuthis shuishi (O’Shea & Lu 2002) and Cryptoteuthis
brevibracchiata (Collins 2004) where comparisons of fresh and preserved specimens are illustrated).
Different preservatives will cause different types of distortion, with considerable shrinkage of Cirro-
teuthis, Cirrothauma and Stauroteuthis in alcohol. Freezing may also cause distortion, notably to
the internal shell (Collins 2003) and possibly spermatophores (Villanueva et al. 2002). Guidelines for
dealing with captured specimens were produced at a workshop in 2000 (Vecchione & Collins 2002).
External
Externally the cirrates are characterised by the possession of lateral to terminal fins and paired
cirri, which are interspersed between a single row of suckers that are highly variable in form. The
body is semigelatinous and varies from an extended bell-shape with long arms (Cirroteuthidae)
through bell-shaped forms with moderate arms (Grimpoteuthidae) to the ovoid shaped Opistho-
teuthis (Figure 1 and Figure 2). Fin size varies from large in Cirroctopus, Cirroteuthis and
Cirrothauma through moderate (Grimpoteuthis, Luteuthis and Stauroteuthis) to small (Cryptoteuthis
and Opisthoteuthis). The fins are generally larger in juvenile cirrates than in adults (Figure 2G).
Figure 1 Ventral view of basic body form in the cirrate octopods. (A) Cirroteuthis muelleri, (B) Cirrothauma
murrayi, (C) Stauroteuthis syrtensis, (D) Grimpoteuthis discoveryi, (E) Opisthoteuthis massyae, (F) Cirroc-
topus glacialis. Sources (with permission where required): (A, B, F) Collins unpublished; (C) from Collins &
Henriques (2000); (D) from Collins (2003); (E) from Villanueva et al. (2002). Scale bars = 100 mm.

© 2006 by Taylor & Francis Group, LLC
MARTIN A. COLLINS & ROGER VILLANUEVA
280
The cirrates lack the innervated
chromatophores that are found in shallow-water cephalopods
(Aldred et al. 1983, Nesis 1987), and are therefore not capable of colour change. In most species
the skin is pigmented and is an orange/red/purple colour in fresh specimens of Opisthoteuthis,
Figure 2 (See also Colour Figure 2 in the insert following page 276.) Photographs of cirrate octopods. (A)
dorsal view of Opisthoteuthis massyae (fresh specimen), (B) ventral view of Cryptoteuthis brevibracchiata
(fresh specimen), (C) dorso-posterior view of Cirroctopus glacialis (fresh specimen), (D) ventral view of
Grimpoteuthis discoveryi (formalin-preserved specimen), (E) ventral view of Cirrothauma murrayi (fresh
specimen), (F) oral view of male Stauroteuthis syrtensis (formalin-preserved specimen), (G) Juvenile specimen
of Opisthoteuthis calypso, note the relatively large fins and funnel in comparison with the adult Opisthoteuthis
in (A). Sources (with permission where required): (A) Collins unpublished; (B) from Collins (2004); (C) Mike
Vecchione unpublished; (D) from Collins (2003); (E) from Aldred et al. (1983); (F) from Collins & Henriques
(2000); (G) L. Dantart. Scale bars: (A–F) = 100 mm; (G) = 10 mm.
© 2006 by Taylor & Francis Group, LLC
CIRRATE OCTOPODS
281
Grimpoteuthis, Luteuthis, Cryptoteuthis and Cirroctopus. In the Cirroteuthidae the oral surface of
the arms is usually deep purple in colour, with the rest of the body pale or unpigmented, although
in situ photographs do show cirroteuthids with purple, red and/or brown colour in both oral and
dorsal surfaces. Although much of the external tissue of Stauroteuthis is translucent, the internal
organs are surrounded by a pigmented membrane, which has a ‘window’ of unknown function in
the area of the accessory glands in males and oviducal glands in females (Collins & Henriques
2000). In Cirrothauma murrayi the pigmentation occurs in two layers: an outer layer that contains
many small granules and an inner layer containing spherical clusters of pigment granules (Aldred
et al. 1983). Pigment-free (areolar) spots are seen on some species of Opisthoteuthis and Cirroctopus
(Vecchione et al. 1998, Villanueva et al. 2002), and Vecchione et al. (1998) speculated that the
pigment-free spots in Cirroctopus glacialis gather and channel light.

The arms vary in length from short to moderate in Opisthoteuthis and Cryptoteuthis, moderate
in Grimpoteuthis, Luteuthis and Cirroctopus and long in Cirroteuthis, Stauroteuthis and Cirrothauma.
In many species the arms are of approximately the same length, and if there are differences, it is
usually the dorsal arms that are the longest. In at least two species of Opisthoteuthis (O. massyae
and O. hardyi) the dorsal arms of the mature males are considerably thicker than the other arms
(see Villanueva et al. 2002). The function of the thickened arms is not known. The cirrates do not
possess a hectocotylus (the modified arm of male incirrate octopods, used to transfer spermatophores
to the female).
In all cirrates the arms are connected by a deep web, which occurs in two forms. In Opistho-
teuthidae, Grimpoteuthidae and Cirroctopodidae the arms are directly connected to the web
(Figure 3B), whilst in Cirroteuthidae each arm is independent of the primary web and is connected
to it by a single, delicate vertical membrane (the intermediate or secondary web) that is attached
along the dorsum of the arm (Figure 3A; see Vecchione & Young 1997). The secondary web of
the Cirroteuthidae may allow greater flexing in the web, and therefore greater locomotory capacity
(see section on behaviour, p. 310). The web is particularly thin and delicate in the Cirroteuthidae,
but thicker and tougher in the other families. In Cirroteuthis muelleri and many Grimpoteuthis
species (Voss & Pearcy 1990, Collins 2003) the web is supported by a single fleshy nodule at the
Figure 3 Cross section of the arm and web of (A) Stauroteuthis syrtensis and (B) Cirroctopus glacialis
contrasting the complex web (secondary web) of S. syrtensis with the simple web form of C. glacialis. From
Vecchione & Young (1997). With permission.
© 2006 by Taylor & Francis Group, LLC
MARTIN A. COLLINS & ROGER VILLANUEVA
282
web margin on the ventral side of each arm (see Figure 4E). Opisthoteuthis species lack these
single fleshy nodules, but instead the web is supported, in some species at least, by multiple, thin,
web supports also placed at the web margin (Figure 4D). In Cirrothauma murrayi the web extends
right to the arm tips (Aldred et al. 1983).
The arms carry a single row of suckers of highly variable form (Figure 4), with distinct sexual
dimorphism in many species. In Opisthoteuthis the suckers are embedded in the arms, with two
distinct enlarged fields in mature males, the proximal enlarged field typically occupies suckers 3–8,

whilst the location, number and degree of enlargement of the distal field is generally species specific,
with gross enlargement in some species (e.g., O. calypso, see Villanueva et al. 2002). In females
the suckers increase gradually in size to a single maximum. In Grimpoteuthis and Cirroctopus the
suckers increase to reach a single maximum, somewhere between sucker 8 and the web margin.
In many Grimpoteuthis species the suckers also show sexual dimorphism, with suckers larger in
males than females but in G. tuftsi and G. challengeri there is no apparent sexual dimorphism. In
mature specimens of Grimpoteuthidae and Opisthoteuthidae total sucker counts vary between 50
and 120 suckers. Sucker form is either barrel-shaped or cylindrical in Grimpoteuthis and distinctly
barrel-shaped in Opisthoteuthis and Cirroctopus. The suckers of Opisthoteuthis have a distinct
peduncle, with the infundibulum composed of radially arranged cushions similar to incirrate
octopods (Villanueva & Guerra 1991) (Figure 5A,B) and the suckers of the other Opisthoteuthidae
and Grimpoteuthidae appear similar in basic structure.
The suckers of the Cirroteuthidae are highly modified. In Stauroteuthis syrtensis the suckers
are highly sexually dimorphic, with very small suckers in the females (maximum sucker diameter
(MSD) = 2.2 mm), but considerably larger in the males (MSD = 6.5 mm; Collins & Henriques
2000) (Figure 5E). In both sexes the first 5–6 (oral) suckers are close together, then 7–23 are spaced
out, with maximum intersucker distance between suckers 13 and 14, with the distal suckers small
and closely packed (Figure 4G–I). From behavioural, anatomical and ultrastructural examination,
Johnsen et al. (1999a,b) considered the suckers of S. syrtensis to be photophores, not true octopodan
suckers. These suckerlike photophores have the capability for bioluminescent emission, but it is
not clear if the suckers of both males and females produce light (Collins & Henriques 2000). These
findings suggest that careful observations of living material and ultrastructural examination may
be useful in other species of cirrates. The function of the light could be to attract either food or
mates. In S. gilchristi there is no dimorphism in sucker form, and the bioluminescent capability is
not known.
In Cirrothauma murrayi the first 5–6 (oral) suckers are small, rounded and closely packed, and
somewhat similar to the oral suckers of Stauroteuthis, but the remaining suckers are borne on long,
conspicuous, fleshy peduncles (see Figures 4J,K; 5D,E; Aldred et al. 1983). The oral suckers have
a small orifice in the infundibulum, but lack a suction chamber. There is no orifice in the distal
suckers, with the infundibulum resembling a small cap (Figure 5C,D). It has been suggested that

there is a possible light organ at the base of the fleshy peducle of the distal suckers (Chun 1913;
Aldred et al. 1982, 1983), but this has not been confirmed (Aldred et al. 1984). In Cirroteuthis
muelleri the oral suckers (1–8) are the largest and are tightly packed, cup-shaped and raised on
broad heavy pads (Voss & Pearcy 1990). The distal suckers appear nonfunctional (as adhesive
suckers) and are raised on fluid filled peduncles, similar in form to those of Cirrothauma murrayi,
but they stop at the web margin (Voss & Pearcy 1990). Three types of suckers are found on the
arms of Cirrothauma magna (Guerra et al. 1998): the oral suckers are small, closely packed and
cylindrical, mounted on a stout stalk; mid-arm suckers have a long stalk and an inflatable acetabulum
chamber; distal suckers are bowl-like with a rigid muscular base.
The cirri are thought to have a sensory function (Aldred et al. 1983) and vary in length,
arrangement and internal structure between genera. In the Cirroteuthidae the cirri are extremely
long, particularly on the midsection of the arms (approximately 50% of mantle length (ML) in
© 2006 by Taylor & Francis Group, LLC
283
CIRRATE OCTOPODS
Figure 4 Illustrations of the arms, suckers and cirri form in the cirrate octopods. Opisthoteuthis agassizii: (A) arm, (B) enlarged male suckers and cirri, (C) female
suckers and cirri, (D) web supports. Grimpoteuthis boylei: (E) arm, (F) suckers and cirri. Stauroteuthis syrtensis: (G) arm, (H, I) male suckers and cirri from
(H) oral and (I) mid-arm sections. Cirrothauma murrayi: (J) arm, (K) suckers and cirri. Cirroctopus glacialis: (L) arm. Cryptoteuthis brevibracchiata: (M) arm,
(N) suckers and cirri. Sources (with permission where required): (A–D) from Villanueva et al. 2002; (E–F) from Collins 2003; (G) from Collins & Henriques
2000; (H–L) Collins, unpublished; (M-N) from Collins 2004. Unmarked scale bars = 10 mm.
© 2006 by Taylor & Francis Group, LLC
MARTIN A. COLLINS & ROGER VILLANUEVA
284
Figure 5 Detail of suckers and cirri. (A, B) Scanning electron micrographs of suckers of Opisthoteuthis
calypso (sp, sucker peduncle; inf, sucker infundibulum), (C) Section of mid-arm sucker of male Stauroteuthis
syrtensis, (D) Scanning electron micrograph of Cirrothauma murrayi sucker, (E) Sagital section of stalked
sucker of Cirrothauma murrayi, (F) Scanning electron micrograph of cirrus of Opisthoteuthis calypso,
(G) longitudinal section of Cirrothauma murrayi cirrus (sep = septum). Sources (with permission where
required): (A, B, F) from Villanueva & Guerra (1991); (C) Collins unpublished; (E, D, G) from Aldred et al.
(1983). Scale bars: (A, B, C, E, F, G) = 0.5 mm; (D) = 2 mm.

© 2006 by Taylor & Francis Group, LLC
CIRRATE OCTOPODS
285
Stauroteuthis; Collins & Henriques 2000). In Stauroteuthis, Cirroteuthis and Cirrothauma magna
the cirri are absent from the distal parts of the arms, stopping at the web margin. In Cirrothauma
murrayi, both the web and cirri extend to the distal ends of the arms. In the other families the cirri
continue to the arm tips and are of moderate length in the Grimpoteuthidae but typically short and
stubby in Opisthoteuthidae and Cirroctopus. Cirri are usually absent between some of the oral
suckers, but the location of the first (oral) cirrus varies between species. In Cirrothauma murrayi
the long cirri are divided internally by transverse septa (Figure 5G; Aldred et al. 1983), but these
septa were not seen in the shorter cirri of Opisthoteuthis massyae (Villanueva & Guerra 1991). In
O. massyae, the cirri are composed of sensory tissue surrounded by muscle (Villanueva & Guerra
1991), similar in structure to O. depressa (Meyer 1906). Hochberg et al. (1992) reported that cirri
are absent in early juvenile forms of some Opisthoteuthis sp., however juvenile Opisthoteuthis
calypso have well-developed cirri, that are relatively longer (in relation to sucker diameter) than adults
(Villanueva unpublished). Early juveniles of Cirrothauma murrayi also possess well-developed cirri
(Aldred et al. 1983).
The funnel form is variable, being extremely long in Cirrothauma, but relatively short in the
other genera. The mantle aperture is reduced, probably associated with the reduction or lack of jet
propulsion. In Stauroteuthis it is extremely reduced, such that on preservation it appears as a small
pore in the mantle, with the funnel often contracted inside. The funnel organ, which is a useful
taxonomic character in the incirrate octopods, is rather indistinct in the cirrates, but in those species
for which it has been described, it is an inverted V-shape (e.g., Berry 1918, Voss & Pearcy 1990,
Collins 2003).
The eyes are large in all but Cirrothauma, which has greatly reduced eyes that lack an iris and
lens (see Aldred et al. 1983). Rounded, prominent olfactory organs are found within the mantle
aperture and either side of the funnel in all cirrate species. They are served by a complex nerve
net, but their supposed chemosensory function has not been established.
Internal
The arrangement of organs in the mantle cavity is similar in all cirrates (Figure 6), but the structure

of the gills and the digestive system is variable. The gills of the cirrates are of two basic forms,
the sepioid form is found in the Cirroteuthidae and the half-orange or modified half-orange form
in the other families (Figure 6). The gills are divided into a series of lamellae, which in the sepioid
form are arranged linearly, whist in the half-orange form they are grouped like segments of an
orange. Opisthoteuthidae, Grimpoteuthidae and Cirroctopus and have the half-orange form, but the
number and form of the lamellae varies between species. In Grimpoteuthis, G. challengeri and G.
tuftsi possess very fine lamellae and small gills, but the other species have broad lamellae and
larger gills. Associated with each gill is a branchial heart, which leads to the systemic heart. A
detailed description of the circulatory system of Stauroteuthis syrtensis and Grimpoteuthis is given
by Ebersbach (1915), and Aldred et al. (1983) describe interspecific differences in the structure of
the cirrate heart.
The internal shell is distinct in each of the genera (Figure 7; see Bizikov 2004 for detail of the
form and evolution of the shell). The vacuolated cartilage of the shell becomes distorted during
freezing, so caution should be exercised when examining frozen material. In Cirroteuthis muelleri
the shell is saddle-shaped, with large ‘wings’ associated with the large fin muscles. Cirrothauma
magna and C. murrayi possess a butterfly-shaped shell, a character that unites these species in
Cirrothauma (see O’Shea 1999). In Stauroteuthis the shell is a simple U-shape. The shell of
Cirroctopus is V-shaped, whilst those of Grimpoteuthis, Opisthoteuthis and Cryptoteuthis are
U-shaped. The shells of Opisthoteuthis and Cirroctopus have lateral walls that taper to fine points,
whilst those of Grimpoteuthis and Cryptoteuthis either end bluntly or in two lobes. Luteuthis has
© 2006 by Taylor & Francis Group, LLC
MARTIN A. COLLINS & ROGER VILLANUEVA
286
a distinctly W-shaped shell. The shell is tightly bound in the shell sac, to which the fins adhere.
The fins, which contain the most robust muscle in the cirrate octopods (Vecchione & Young 1997),
are divided into distinct proximal and distal regions (Figure 8). The proximal region has a central
cartilaginous core, which is covered by thick bundles of muscle fibres, parallel to the fin axis, that
insert on the shell sac or on the cartilaginous core. The distal region lacks the cartilaginous core
of the proximal region, consisting of two layers of thin muscles that are oriented transversely to
the fin plane.

The digestive system is similar in all the cirrates (Figure 9) consisting of buccal mass and
beaks, radula (in some species), anterior and posterior (reduced or absent) salivary glands, oesoph-
agus, stomach, caecum, digestive gland and intestine. The beak form varies between the genera
(Figure 10), with Stauroteuthis possessing a particularly distinct beak, although insufficient material
has been examined to distinguish interspecific variability. A radula is only found in some species
of Grimpoteuthis (Figure 11) and in Luteuthis, but in a highly reduced monodont form (Voss &
Pearcy 1990, O’Shea 1999, Collins 2003). Anterior salivary glands are present in all species, but
posterior salivary glands are only reported in two species of Grimpoteuthis, where they are small
(Collins 2003). Aldred et al. (1983) did report a single posterior salivary gland in Cirrothauma, but
the location of the single gland is different to Grimpoteuthis and incirrate octopods and is possibly
not an analagous structure. The oesophagus, stomach and intestine are a deeply pigmented purple
colour that may be associated with the consumption of bioluminescent prey (Vecchione & Young
1997). A swelling of the oesophagus (crop?) has been reported for some species, but is rather
indistinct. The stomach, which lies in a groove in the digestive gland, is lined with a thick cuticle
and leads, via a narrow duct, to the caecum, which typically has a single turn and is connected to
the digestive gland by two digestive ducts. The digestive gland consists of a single lobe in most
species but is bilobed (two discrete lobes) in some Opisthoteuthis species and in Luteuthis. The
intestine is straight (uncoiled) in Cirroteuthis, Stauroteuthis and Cirrothauma but slightly coiled
in the other genera.
The basic form of the nervous system is similar for all the cirrates and is described in detail
for Cirrothauma murrayi by Aldred et al. (1983). A major difference between the cirrates and
incirrates is the form of the central ganglia, which in cirrates consist of two rings surrounding the
Figure 6 Internal anatomy of (A) female Grimpoteuthis wuelkeri and (B) male Stauroteuthis syrtensis illus-
trating the gill form and location of internal organs. Sources (with permission where required): (A) from
Collins (2003); (B) Collins unpublished. Scale bars = 25 mm.
© 2006 by Taylor & Francis Group, LLC
CIRRATE OCTOPODS
287
oesophagus (Figure 12), somewhat similar to that of Nautilus (Aldred et al. 1983). The eyes are
directed laterally with long optic nerves passing through a large ‘white body’, which varies in

colour between species. The form of the optic nerve is an important taxonomic character: in the
Cirroteuthidae and Grimpoteuthidae the optic nerve passes through the white body as a single
bundle of fibres (Figure 13), whilst in Opisthoteuthidae there are two to four bundles of nerve fibres
and in Cirroctopodidae there are eight or nine bundles. The form of the stellate ganglion and
epistellar body has also been used as a taxonomic character (e.g Robson 1932, Voss & Pearcy
1990) and the epistellar body is particularly well developed in the cirrates (Aldred et al. 1983),
although its function is not known.
Figure 7 Shell form in the cirrate octopods. (A) Cirrothauma murrayi, (B) Cirroteuthis muelleri, (C) Stau-
roteuthis syrtensis, (D) Cirroctopus glacialis, (E) Grimpoteuthis discoveryi, (F) Opisthoteuthis agassizii,
(G) Cryptoteuthis brevibracchiata. Sources (with permission where required): (A, B, C, D) Collins, unpub-
lished; (E) from Collins 2003; (F) from Villanueva et al. 2002; (G) from Collins 2004. Scale bars = 10 mm.
© 2006 by Taylor & Francis Group, LLC
MARTIN A. COLLINS & ROGER VILLANUEVA
288
The female reproductive system is similar in all the cirrates consisting of ovary, thin-walled
proximal oviduct (left only), oviducal gland and a fleshy distal oviduct (Figures 14, 15; see Boyle &
Daly 2000, Villanueva 1992a). For all species studied the ovaries contain a wide range of egg sizes
and developmental stages (see section on reproduction, p. 302). The oviducal gland consists of two
sections, both striated, but differing distinctly in colour. The proximal section, which is usually
lighter in colour functions as a spermatheca (Aldred et al. 1983) and is the presumed location of
fertilisation, whilst the distal section is responsible for providing the tough egg case.
The male reproductive system is more variable, consisting of testes, seminal vesicle, accessory
gland(s) and terminal organ (or penis) (Figure 14). The testis is located posteriorly in the mantle
cavity, and leads via the vas deferens to the seminal vesicle, which passes through the accessory
gland(s) to the terminal organ. The number and size of the accessory glands vary between genera
and species. In the Cirroteuthidae there is a single accessory gland (Aldred et al. 1983, Voss &
Pearcy 1990, Collins & Henriques 2000), whilst in Opisthoteuthis, Cirroctopus and Grimpoteuthis
there are multiple accessory glands (Voss & Pearcy 1990, O’Shea 1999, Villanueva et al. 2002,
Collins 2003). In mature males the spermatophores (‘sperm packets’) are unlike those of incirrate
Figure 8 The structure of the shell, fin cartilage and fin muscles of (A, B) Cirroctopus glacialis and (C, D)

Stauroteuthis syrtenis. (B) and (D) are schematic sections through the long axis of the fins. Modified from
Vecchione & Young (1997). With permission.
Figure 9 Digestive system of (A) Opisthoteuthis massyae, (B) Grimpoteuthis wuelkeri (with detail of posterior
salivary glands) and (C) Stauroteuthis syrtensis. Sources (with permission where required): (A) from Villanueva
et al. (2002); (B) from Collins (2003); (C) from Collins & Henriques (2000). Scale bars = 10 mm.
© 2006 by Taylor & Francis Group, LLC
CIRRATE OCTOPODS
289
Figure 10 Lower and upper beaks of (A) Opisthoteuthis agassizii, (B) Grimpoteuthis wuelkeri, (C) Stauro-
teuthis syrtensis and (D) Cirrothauma magna. Sources (with permission where required): (A) from Villanueva
et al. (2002); (B) from Collins (2003); (C) from Collins & Henriques (2000); (D) Collins unpublished. Scale
bars = 5 mm.
Figure 11 Scanning electron micrographs of the radula of Grimpoteuthis wuelkeri. Modified from Collins
(2003). With permission. Scale bars = 1 mm.
© 2006 by Taylor & Francis Group, LLC
MARTIN A. COLLINS & ROGER VILLANUEVA
290
octopods, being ovoid in shape (approximately 2–3 × 1–1.5 mm) embedded in gelatinous material
(in preserved specimens) and located in the seminal vesicle and terminal organ. The spermatophores
of Opisthoteuthis hardyi appear disc-shaped (Villanueva et al. 2002), but this may be a consequence
of distortion due to freezing prior to fixation. Detailed examination of the spermatophores of
Figure 12 Eye, central nervous system and statocyst of Cirrothauma murrayi. Modified from Aldred et al.
(1983). With permission.
Figure 13 Optic nerve configuration in the cirrate octopods. (A) Opisthoteuthis, (B) Grimpoteuthis,
(C) Stauroteuthis, (D) Cirroctopus. Sources (with permission where required): (A) from Villanueva et al.
(2002); (B) from Collins (2003); (C) from Collins & Henriques (2000); (D) Collins unpublished. Scale bars =
10 mm.
© 2006 by Taylor & Francis Group, LLC
CIRRATE OCTOPODS
291

Figure 14 Reproductive system of cirrate octopods. (A) Female reproductive system of Grimpoteuthis boylei,
male reproductive system of (B) Grimpoteuthis boylei and (C) Stauroteuthis syrtensis. Sources (with permis-
sion): (A, B) from Collins (2003); (C) from Collins & Henriques (2000). Scale bars = 20 mm.
Figure 15 (A) Section of ovary of Opisthoteuthis massyae, showing maturing eggs and convoluted follicular
epithelium which secretes yolk into the lumen of the ovum, (B) dissected ovary of O. massyae showing
distribution and size range of maturing eggs, (C) section of mature ovarian egg showing formed chorion and
outer sheath layer, (D) general view of released eggs among remaining maturing eggs of various sizes. From
Boyle & Daly (2000). With permission. Scale bars: (A, C, D) = 500 μm; (B) = 20 mm.
© 2006 by Taylor & Francis Group, LLC
MARTIN A. COLLINS & ROGER VILLANUEVA
292
O. calypso (Figure 16A) shows them to possess pores at each end, which are covered with a hinged
opercular structure (Villanueva 1992a), although these have not been found in other species
(Figure 16B, Villanueva et al. 2002). The spermatophores function as a sperm reservoir, and sections
through the spermatophores show aggregations of spermatozoids, with the heads oriented toward
the walls and tails in the centre (Figure 16D,E; Aldred et al. 1983, Guerra et al. 1998, Collins &
Henriques 2000).
Healy (1993) compared mature spermatozoa from Opisthoteuthis persephone with those of
Octopus and Vampyromorpha and found them to be similar to those of Octopus species, consisting
of an elongate, solid acrosome; a straight, rodlike nucleus; a short midsection with a post mitochondrial
Figure 16 (A) Diagram of a spermatophore from Opisthoteuthis calypso, (B) scanning electron micrograph
of a spermatophore of O. massyae, (C) spermatozoa of O. calypso (left) and O. massyae, (D, E) scanning
electron micrographs of the inside wall of the spermatophores of (D) Stauroteuthis syrtensis and (E)
O. grimaldii showing the form of the spermatozoa. Sources (with permission where required): (A, C) from
Villanueva 1992a; (B, E) Collins unpublished; (D) from Collins & Henriques 2000. Scale bars: (A, B) =
1 mm; (C, D, E) = 3 μm.
© 2006 by Taylor & Francis Group, LLC
CIRRATE OCTOPODS
293
skirt and a long flagellum. The form of sperm in Opisthoteuthis massyae (Villanueva 1992a), O.

grimaldii and Stauroteuthis (Collins & Henriques 2000) is similar (Figure 16C,D,E), although
Opisthoteuthis calypso has a broader, more oval nuclear section (Figure 16C; Villanueva 1992a).
Systematics
In his review of the deep-sea octopods Voss (1988a) recognised 24 cirrate species in three families
(Opisthoteuthidae, Stauroteuthidae and Cirroteuthidae), with 21 species in the Opisthoteuthidae.
Recent work (Voss & Pearcy 1990, O’Shea 1999, Villanueva et al. 2002, Collins 2003) has increased
the number of species considerably, with 45 species now recognised. Based on studies of the New
Zealand fauna, O’Shea (1999) split the Opisthoteuthidae, adding the families Grimpoteuthidae and
Luteuthidae. Recently, in a molecular study using sequences of the 16s gene, Piertney et al. (2003)
suggested a division into four families, with Stauroteuthis, Cirroteuthis and Cirrothauma united in
the Cirroteuthidae; Opisthoteuthis in the Opisthoteuthidae; Grimpoteuthis, Luteuthis and Enigma-
titeuthis in the Grimpoteuthidae and a new family to include the genus Cirroctopus. The division
into four families proposed by Piertney et al. (2003) is in general agreement with the morphological
data and is followed here.
Class Cephalopoda Cuvier, 1797
Order Octopoda Leach, 1818
Suborder Cirrata Grimpe, 1916
Family Cirroteuthidae Keferstein, 1866
Diagnosis Small-to-large cirrates, with extended bell-shaped body. Web complex, with secondary
web linking arms to primary web. Digestive gland entire. Cirri long. Radula and posterior salivary
glands absent. Gill form sepioid.
Comments The family is represented by four genera (Table 1) and characterised by the possession
of a secondary web (Figure 2) and extremely long cirri. Previous taxonomic organisations included
Stauroteuthis in a separate family (Stauroteuthidae, Grimpe 1916), but a recent molecular study
supports inclusion in the Cirroteuthidae (Piertney et al. 2003).
Genus Cirroteuthis Eschricht, 1836
Diagnosis Small-to-medium sized cirroteuthids, with large fins, saddle-shaped shell and long
cirri. Cirri absent from distal section of arms. One recognised species. Type species Cirroteuthis
muelleri (Eschricht 1836).
Comments The genus previously included species that have since been moved to other genera or

are considered nomen dubium (Table 1). Cirroteuthis muelleri was the first described cirrate
(Eschricht 1836) and was redescribed by Voss & Pearcy (1990). It is benthopelagic and has a circum-
Arctic distribution extending into the northern basins of the Pacific and Atlantic Oceans (Voss &
Pearcy 1990, Nesis 2001, Collins et al. 2001a, Collins 2002). It occurs from near the surface in
the high Arctic to 4500 m in the ocean basins, with distribution probably limited by temperature
rather than depth. A specimen tentatively attributed to this species was caught off New Zealand
but may represent a new species (O’Shea 1999).
Cirroteuthis hoylei was described from a single specimen caught during the Challenger Expe-
dition (Station 298) and was originally identified as C. magna by Hoyle (1885a). The specimen is
small and badly damaged, but Robson (1932) considered that it represented a new species, which
© 2006 by Taylor & Francis Group, LLC
MARTIN A. COLLINS & ROGER VILLANUEVA
294
he called Cirroteuthis (?) hoylei. The presence of a saddle-shaped shell indicates that it is a
Cirroteuthis (Guerra et al. 1998), but it should be considered as Cirroteuthis sp. Cirroteuthis hoylei
is thus nomen dubium.
Genus Cirrothauma Chun, 1911
Diagnosis Large-sized cirroteuthids with butterfly-shaped shell, large fins, extremely long cirri, distal
suckers stalked and highly modified. Two species. Type species: Cirrothauma murrayi (Chun 1911).
Comments The genus includes two recognised species, C. murrayi and C. magna (see Table 1).
C. murrayi, which lacks lens and iris and has been called the ‘blind octopus’, appears to have a
worldwide distribution, with specimens reported from the North Atlantic (Chun 1911, 1913, Aldred
et al. 1983, Collins et al. 2001a), south Atlantic (Roper & Brundage 1972) and Pacific Oceans (see
Aldred et al. 1983). However, geographic variability in these specimens has not been critically
reviewed. Recent captures in the northeast Atlantic have been taken in bottom trawls at depths from
3900–4800 m (Aldred et al. 1983, Collins et al. 2001a), but other specimens (including the type)
have been captured in midwater, usually over deep water. A specimen has also been captured with
a dip net in the Arctic (Voss 1967).
There are only four records of C. magna, from the Atlantic and Indian Oceans (Hoyle 1885a,b,
Guerra et al. 1998, Collins et al. 2001b). This species grows to a large size and is probably the

largest of the cirrates (Collins et al. 2001b). It was previously included in the genus Cirroteuthis,
but the form of the shell, long arms and extremely large fins indicate it should be included in
Cirrothauma (see O’Shea 1999).
Table 1
Family Cirroteuthidae: distribution of recognised species
Species Distribution Comments References
Cirroteuthis muelleri
Eschricht, 1836
North Atlantic and North
Pacific, possibly continuous
through Arctic Ocean. Also
reported from SW Pacific
= Sciadophorus Reinhardt
& Prosch 1846
Eschricht 1836, Reinhardt &
Prosch 1846, Voss & Pearcy
1990, O’Shea 1999, Collins
et al. 2001a, Collins 2002,
Knudsen & Roeleveld 2002
Cirroteuthis hoylei
nomen dubium
SE Pacific 2225 fathoms
(4070 m) (Robson 1932)
Only known from type,
which is small and
damaged, but clearly a
Cirroteuthis
Robson 1932, Guerra et al.
1998
Cirrothauma magna

Hoyle, 1885
Southern Indian Ocean;
Atlantic Ocean
(1300–3351 m)
Only known from four
specimens
Hoyle 1885a,b, Guerra et al.
1998, Collins et al. 2001b
Cirrothauma murrayi
Chun, 1911
Worldwide at bathyal to
abyssal depths
Worldwide distribution
requires critical review to
determine differences
Chun 1911, Aldred et al.
1983, Roper & Brundage
1972, Collins et al. 2001a
Stauroteuthis gilchristi
Robson, 1924
South Atlantic (900–2604 m) = Cirroteuthis gilchristi Robson 1924a, b, 1930,
Collins & Henriques 2000,
Collins et al. 2004
Stauroteuthis syrtensis
Verrill, 1879
North Atlantic at
1500–2500 m, shallower in
Arctic waters
= Chunioteuthis
ebersbachi

Verrill 1879, Grimpe 1916,
Collins & Henriques 2000,
Collins et al. 2001a
Froekenia clara
nomen dubium
Equatorial Pacific (1015 m)
(Hoyle 1904)
Only known from type
specimen, which is now
lost
Hoyle 1904, Nesis 1986,
1987, 1993, Voss 1988a,
Guerra et al. 1998
© 2006 by Taylor & Francis Group, LLC
CIRRATE OCTOPODS
295
Genus Stauroteuthis Verrill, 1879
Diagnosis Large-sized cirroteuthids with moderate fins and U-shaped shell. Arms long with
extremely long cirri on midsection. Cirri absent from distal section of arms. Two species. Type
species: Stauroteuthis syrtensis (Verrill 1879).
Comments The genus Stauroteuthis has previously been included in its own family (Stau-
roreuthidae, Grimpe 1916), but has also been included in the Cirroteuthidae (see Nesis 1987). The
presence of a secondary web suggests that it is closely related to Cirroteuthis and Cirrothauma,
and molecular analysis also supports its inclusion in Cirroteuthidae (Piertney et al. 2003). The
genus includes two species, Stauroteuthis syrtensis and S. gilchristi. S. syrtensis is distributed in
the North Atlantic at depths of 200–3000 m (Verrill 1879, Grimpe 1916, Collins & Henriques 2000,
Collins et al. 2001a, Collins 2002). Males and females are sexually dimorphic, notably in the form
of the suckers, which was partly responsible for the confusion regarding Chunioteuthis ebersbachi
(a junior synonym), which was originally described by Grimpe (1916) from a male specimen,
whilst Stauroteuthis syrtensis was described by Verrill (1879) from a female. Johnsen et al. (1999a,b)

demonstrated the bioluminescent capacity of the suckers. However, given the sexual dimorphism,
it is not clear if both sexes are capable of producing light. It may be that the highly reduced suckers
of the females produce light, perhaps to attract males.
S. gilchristi is known from the type location, off the South African coast (Robson 1924a,b) and
from the Atlantic sector of the Southern Ocean (Collins & Henriques 2000, Collins et al. 2004). It
is morphologically similar to S. syrtensis, but there is no sexual dimorphism in the suckers. It is
possible that the Southern Ocean specimens are different from the type material, but the poor
condition of the two South African specimens prevented proper comparison (Collins & Henriques
2000).
Genus Froekenia Hoyle, 1904
Comments The genus was described from the single specimen of Froekenia clara caught at 555
fathoms (~1015 m) in the Pacific (Hoyle 1904). The species is unusual in, apparently, lacking a
web between the arms. The type specimen has been lost (Sweeney & Roper 1998) and the species
is considered nomen dubium (Voss 1988a). However, Nesis (1986, 1993) reported that new spec-
imens, attributable to a new species of Froekenia, have been found at 500–810 m at the Error
Seamount, Indian Ocean. To date the specimens have not been formally described and the status
of the genus remains in doubt.
Family Opisthoteuthidae Verrill, 1896
Diagnosis Moderate-sized cirrates with small, subterminal fins. Shell a flaring U-shape, lateral
walls tapering to fine points. Optic nerves pass through white body in two to four bundles. Two
fields of enlarged suckers in mature males. Digestive gland entire or bilobed. Radula and posterior
salivary glands absent. Web deep, single. Gills of ‘half-orange’ form. Single genus.
Comments Includes the genus Opisthoteuthis. Various divisions of the cirrates have been proposed,
with Grimpoteuthis included either in Opisthoteuthidae or Cirroteuthidae. O’Shea (1999) proposed
a new family to accommodate Grimpoteuthis, but included Cirroctopus in the Opisthoteuthidae.
However, recent molecular evidence (Piertney et al. 2003) indicates that Cirroctopus is sufficiently
distinct from the other genera to warrant a separate family. Generally Opisthoteuthidae is the
shallowest of the cirrate families, typically found at depths from 300–2200 m.
© 2006 by Taylor & Francis Group, LLC
MARTIN A. COLLINS & ROGER VILLANUEVA

296
Genus Opisthoteuthis Verrill, 1883
Diagnosis As family. Nineteen species. Type species Opisthoteuthis agassizii Verrill, 1883.
Comments The 19 species occur throughout the world’s oceans (Table 2), with new species
recently described from Atlantic and New Zealand waters. O. brunni is included in this genus rather
than Grimpoteuthis (see Collins 2003). O’Shea (1999) separated the genus into three types based
on the form of the digestive gland (bilobed or entire), shell, enlarged suckers and male accessory
glands, but that organisation is not followed here. Six species are reported in the Atlantic, and the
confusion surrounding the identification of these species has been addressed by Villanueva et al.
(2002), with O. borealis subsequently described from the coast of Greenland (Collins 2005).
O. agassizii is found only in the western Atlantic and reports of this species in the eastern Atlantic
and Mediterranean are erroneous (e.g., Chun 1913; Bruun 1945; Adam 1962; Villanueva & Guerra
1991; Villanueva 1992a,b). O. massyae (= O. vossi, in part) was originally described as Cirroteuthis
(Cirroteuthopsis) massyae by Grimpe (1920) from a single specimen caught off Ireland. It is a
large species found at depths of 600–1500 m from the west coast of the British Isles to the Namibian
coast in the southeast Atlantic. O. grimaldii has a similar geographic range to O. massyae, but
appears to live slightly deeper (<2200 m) and may also occur in the northwest Atlantic (Villanueva
et al. 2002). O. calypso is a small species, characterised by extreme enlargement in the distal sucker
field in mature males, it is found in the eastern Atlantic from the coast of Namibia in the south to
the southwest of Ireland in the north and in the Mediterranean. O. hardyi is only known from a
single (male) specimen caught near South Georgia (~1000 m), but a female, probably attributable
to this species has been taken off the Falkland Islands.
Three species, O. phillipi, O. medusoides and O. extensa were described from the Indian Ocean
(Table 2), but little is known about the distribution of any of them. Four species (O. albatrossi,
O. californiana, O. depressa and O. japonica) are known from the North Pacific and their status
is unclear. O. albatrossi was originally described (from south of the Aleutian Islands) as Stauro-
teuthis (Sasaki 1920), and has recently been considered a Grimpoteuthis (Voss 1988a). Although
the holotype (male) is in poor condition, it is clear from the original illustration that the body shape
and pattern of greatly enlarged suckers at the web margin are characteristic of Opisthoteuthis. The
sucker pattern of males is very similar to that of O. californiana, suggesting that an updated

classification of the Opisthoteuthis in the North Pacific is needed. O. brunni is distributed in the
east Pacific, off the central American coast (Voss 1982). O’Shea (1999) described three new species
from New Zealand waters: O. mero occurs at depths of 360–1000 m around New Zealand;
O. chathamensis is slightly deeper (900–1438 m) off the northeast coast of New Zealand with O. robsoni
deeper again (1178–1723 m) off the east coast of the south island. In addition, O. persephone and
O. pluto are described from the south of Australia.
Family Grimpoteuthidae O’Shea, 1999
Diagnosis Medium-to-large sized, bell-shaped cirrates with lateral fins. Web deep and simple.
Shell U-shaped, with lateral walls parallel. Optic nerve passes though white body in single bundle.
Radula reduced or absent. Posterior salivary glands reduced or absent. Cirri of short to moderate
length. Gills of ‘half-orange’ form. Three genera: Grimpoteuthis, Cryptoteuthis and Luteuthis.
Comments O’Shea (1999) split the Family Opisthoteuthidae and created two new families Grim-
poteuthidae and Luteuthidae. O’Shea (1999) proposed that Grimpoteuthidae include Grimpoteuthis
and a new genus Enigmatiteuthis. The family Luteuthidae was proposed to include a single species,
Luteuthis dentatus (from a single specimen). However, whilst Grimpoteuthis is distinct from
© 2006 by Taylor & Francis Group, LLC
CIRRATE OCTOPODS
297
Table 2
Family Opisthoteuthidae: recognised species and distribution
Species Distribution Comments References
Opisthoteuthis agassizii
Verrill, 1883
NW Atlantic (227–1935 m) Restricted to western
Atlantic, reports from
E Atlantic are
misidentifications.
Opisthoteuthis Group 1 of
O’Shea (1999)
Villanueva et al. 2002

Opisthoteuthis albatrossi
(Sasaki, 1920)
Off Japan, NW Pacific
(486–1679 m)
Four specimens;
Opisthoteuthis Group 2 of
O’Shea (1999)
Sasaki 1920, 1929
Opisthoteuthis borealis
Collins, 2005
N Atlantic off Greenland
(957–1321 m)
Similar to O. grimaldii, but
digestive gland entire
Collins 2005
Opisthoteuthis brunni
(Voss, 1982)
East Pacific off the coast of
Peru
Originally described as a
Grimpoteuthis
Voss 1982, Collins 2003
Opisthoteuthis californiana
Berry, 1949
North Pacific (320–620 m) Similar to O. albatrossi Berry 1949,
Laptikhovsky 1999
Opisthoteuthis calypso
Villanueva et al., 2002
NE Atlantic from SW
Ireland to South Africa

and Mediterranean
(365–2208 m)
Previously misidentified as
O. agassizii
Villanueva et al. 2002,
Villanueva 1992b
Opisthoteuthis chathamensis
O’Shea, 1999
Off New Zealand
(850–1500 m)
Opisthoteuthis Group 2 of
O’Shea (1999)
O’Shea 1999
Opisthoteuthis depressa
Ijema & Ikeda, 1895
N Pacific, off Japanese coast Ijima & Ikeda 1895
Opisthoteuthis extensa
Thiele, 1915
Indian Ocean, SW of
Sumatra
Opisthoteuthis Group 1 of
O’Shea (1999)
Thiele in Chun 1915
Opisthoteuthis grimaldii
(Joubin, 1903)
NE Atlantic (1135–2287 m) Only known from male
specimens, no confirmed
females
Joubin 1903,
Villanueva et al., 2002

Opisthoteuthis hardyi
Villanueva et al., 2002
Off South Georgia, Southern
Ocean (800–1100 m)
Single male specimen only Villanueva et al. 2002
Opisthoteuthis japonica
Taki, 1962
Off Japan, West Pacific
(152 m)
Two specimens; similar to
O. albatrossi
Taki 1962, 1963
Opisthoteuthis massyae
(Grimpe, 1920)
NE Atlantic, from Rockall
Trough to Namibia
(778–1450 m)
= Cirroteuthopsis massyae
Grimpe 1920
= Opisthoteuthis vossi
Sanchez & Guerra 1989
Villanueva et al. 2002,
Boyle et al. 1998,
Collins et al. 2001a
Opisthoteuthis medusoides
Thiele, 1915
Off east African coast,
Indian Ocean (400 m)
Thiele in Chun 1915
Opisthoteuthis mero

O’Shea, 1999
Off New Zealand
(360–1000 m)
Opisthoteuthis Group 1 of
O’Shea (1999)
O’Shea 1999
Opisthoteuthis persephone
Berry, 1918
Off South Australian coast
(270–540 m)
Opisthoteuthis Group 1 of
O’Shea (1999)
Berry 1918, Healy 1993
Opisthoteuthis phillipi
Oommen, 1976
Indian Ocean, off SW India Opisthoteuthis Group 1 of
O’Shea (1999)
Oommen 1976
Opisthoteuthis pluto
Berry, 1918
Off South Australian coast
(270–810 m)
Opisthoteuthis Group 2 of
O’Shea (1999)
Berry 1918
Opisthoteuthis robsoni
O’Shea, 1999
Off east coast of New
Zealand (1178–1723 m)
Four specimens only;

Opisthoteuthis Group 3 of
O’Shea (1999)
O’Shea 1999
© 2006 by Taylor & Francis Group, LLC
MARTIN A. COLLINS & ROGER VILLANUEVA
298
Opisthoteuthis and there is molecular support for separating the two families, there is little support
for the separation of Luteuthis from Grimpoteuthis at the familial level. Furthermore, the ‘true’
form of Grimpoteuthis remains unknown because the type species G. umbellata remains poorly
described and is known only from the type, which is in extremely poor condition (see Collins
2003). Therefore, until new material is found from the type locality and G. umbellata is redescribed
it is inappropriate to split Grimpoteuthis. For these reasons Luteuthis should remain in the family
Grimpoteuthidae.
Genus Grimpoteuthis Robson, 1932
Diagnosis Small-to-large grimpoteuthids with medium-to-large lateral fins, each with a distinct
lobe near the anterior fin insertion. Shell vestige U-shaped; lateral sides parallel, not tapered to fine
points. Radula monodont or absent. Posterior salivary glands small or absent. Web supported by
single fleshy nodules on the ventral side of the arms. Digestive gland entire (single lobe). Sucker
sexual dimorphism present in some species, but with single enlarged field. Fourteen species. Type
species: Grimpoteuthis umbellata (Fischer 1883).
Comments The type species, G. umbellata, is known only from a single, badly damaged specimen
caught near the Azores (2235 m) (see Collins 2003). It is possible that G. wuelkeri, G. plena or
G. discoveryi are synonymous with G. umbellata, but this cannot be resolved until new material
has been examined from the type locality.
Of the seven Atlantic species (see Table 3), G. wuelkeri (Grimpe 1920) was described (as
Stauroteuthis wuelkeri) from a single specimen caught off the Moroccan coast. It is found at depths
of 1500–2100 m in the North Atlantic, and has recently been redescribed (Collins 2003).
Piatkowski & Dieckmann (2005) reported a specimen of Grimpoteuthis wuelkeri from 5430 m in
the Angola Basin, but this is considerably deeper than other records of this species and may be
attributable to one of the deeper Grimpoteuthis species. G. boylei and G. challengeri are both large-

sized abyssal species currently known from the northeast Atlantic, whilst G. discoveryi is a smaller
species found throughout the North Atlantic (2600–4870 m). G. megaptera was described from
five specimens from the northwest Atlantic. Of the five specimens that Verrill (1885) attributed to
this species, four are now lost and the small damaged specimen is actually a Cirrothauma murrayi.
Of the four lost specimens, three were caught at abyssal depths (4594–4708 m), with the fourth
taken considerably shallower (1928 m) and, given what is known about the depth ranges of other
Grimpoteuthis, it is unlikely that the shallow specimen is conspecific with the other three. The
larger specimen (4708 m), which was illustrated by Verrill (1885; his Plate XLIII), is clearly a
Grimpoteuthis, but new material is required from the type locality to redescribe G. megaptera.
G. plena is known from a single, small and damaged specimen from the northwest Atlantic
(1963 m). The poor condition of the G. plena type makes comparison difficult but it is somewhat
similar to G. wuelkeri, which is found at equivalent depths in the North Atlantic.
Seven species are known from the Indo-Pacific region (Table 3), but three of them, G. pacifica,
G. meangensis and G. hippocrepium, were described from single specimens caught in the late
nineteenth and early twentieth centuries and only in G. meangensis (one additional specimen) has
new material been found. G. tuftsi and G. bathynectes were described from the northeast Pacific
by Voss & Pearcy (1990). G. tuftsi was described from seven specimens caught on the Tufts Abyssal
Plain at 3585–3900 m and is similar to the Atlantic abyssal species, G. challengeri, in possessing
a (reduced) radula, fine lamellae on the gills, long cirri and with MSD at the web margin. The two
species (G. tuftsi and G. challengeri) are clearly closely related. G. bathynectes was described from
thirteen specimens caught on both the Tufts and Cascadia Abyssal Plains. G. abyssicola is only
known from a single specimen caught between Australia and New Zealand (O’Shea 1999).
© 2006 by Taylor & Francis Group, LLC
CIRRATE OCTOPODS
299
G. inominata was described (as Enigmatiteuthis inominata) from two specimens caught at depths
of 1705–2002 m on the Chatham Rise (O’Shea 1999). O’Shea (1999) suggested that other Grim-
poteuthis species (G. bathynectes, G. meangensis, G. pacifica and G. wuelkeri) be included in
Enigmatiteuthis but Collins (2003) considered that all should be retained in Grimpoteuthis until
the type species of this genus is described in detail.

Table 3
Family Grimpoteuthidae: recognised species and distribution
Species Distribution Comments References
Grimpoteuthis umbellata
(Fischer, 1883)
Azores, NE Atlantic
(2235 m)
Type (and only) specimen
in poor condition, making
comparisons difficult
Fischer 1883, Fischer &
Joubin 1907, Collins et al.
2001a, Collins 2003
Grimpoteuthis abyssicola
O’Shea, 1999
Tasman Sea, SW Pacific
(4660 m)
Single specimen O’Shea 1999
Grimpoteuthis bathynectes
Voss & Pearcy, 1990
NE Pacific (2816–3932 m) Voss & Pearcy 1990
Grimpoteuthis boylei
Collins, 2003
NE Atlantic (4000–4900 m) Large species Collins et al. 2001a,
Collins 2003
Grimpoteuthis challengeri
Collins, 2003
NE Atlantic (4800–4850 m) Large; possesses radula;
allied to G. tuftsi
Collins et al. 2001a,

Collins 2003
Grimpoteuthis discoveryi
Collins, 2003
N Atlantic (2600–4870 m) Small species Collins et al. 2001a,
Collins 2003
Grimpoteuthis hippocrepium
(Hoyle, 1904)
East Pacific (3334 m) Single damaged specimen Hoyle 1904, Voss & Pearcy
1990
Grimpoteuthis inominata
(O’Shea, 1999)
Chatham Rise, SW Pacific
(1705–2002 m)
Two specimens only;
originally described as
Enigmatiteuthis
inominata
O’Shea 1999, Collins 2003
Grimpoteuthis meangensis
(Hoyle, 1885)
North of Celebes, W Pacific
(1100 m); Kermadec
Island, SW Pacific (915 m)
Known only from two
specimens described by
Hoyle; generic status
uncertain
Hoyle 1885a,b, 1886
Grimpoteuthis megaptera
(Verrill, 1885)

NW Atlantic Known only from type
material, now lost
Verrill 1885, Collins 2003
Grimpoteuthis pacifica
(Hoyle, 1885)
Coral Sea, north of Australia Single specimen only Hoyle 1885a
Grimpoteuthis plena
(Verrill, 1885)
NW Atlantic (1963 m) Single small specimen;
similar to G. wuelkeri
Verrill 1885, Collins 2003
Grimpoteuthis tuftsi
Voss & Pearcy, 1990
NE Pacific (3585–3900 m) Large species; possesses
radula; allied to G.
challengeri
Voss & Pearcy 1990
Grimpoteuthis wuelkeri
(Grimpe, 1920)
N Atlantic (1500–2500 m) Similar to G. plena Grimpe 1920, Collins 2003
Luteuthis dentatus
O’Shea, 1999
Tasman Sea, SW Pacific
(991 m)
Single specimen O’Shea 1999
Luteuthis shuishi
O’Shea, & Lu 2002
South China Sea
(754–767 m)
Single specimen O’Shea & Lu 2002

Cryptoteuthis
brevibracchiata
Collins, 2004
NE Atlantic (2274–2300 m) Single specimen Collins 2004
© 2006 by Taylor & Francis Group, LLC
MARTIN A. COLLINS & ROGER VILLANUEVA
300
Genus Cryptoteuthis Collins, 2004
Diagnosis Bell-shaped grimpoteuthids, with small fins and short arms. Gills with seven broad
lamellae. Suckers broad, cirri moderate in length. Shell U-shaped, with parallel lateral walls
terminating in two lobes. Posterior salivary glands absent. Radula absent. Digestive gland entire.
One species. Type species: Cryptoteuthis brevibracchiata (Collins 2004).
Comments The genus Cryptoteuthis was described from a single specimen (C. brevibracchiata)
caught from 2274–2300 m in the Porcupine Seabight, northeast Atlantic (Collins 2004). The species
possesses characters of both Opisthoteuthis and Grimpoteuthis, with the body shape and short fins
characteristic of Opisthoteuthis whilst the form of the shell, optic nerve configuration and the size
and shape of suckers and cirri resemble Grimpoteuthis. There is a superficial resemblance to
Luteuthis shuishi, but Cryptoteuthis brevibracchiata possesses an entire digestive gland, U-shaped
shell, cirri of moderate length and lacks a radula. In a molecular study Cryptoteuthis was found
to differ from both Grimpoteuthis and Opisthoteuthis, although it appeared more closely allied to
Grimpoteuthis (Piertney et al. 2003), which supports inclusion in the family Grimpoteuthidae.
Genus Luteuthis O’Shea, 1999
Diagnosis Grimpoteuthids with moderate-sized fins, short cirri (<2% ML) and a bilobed digestive
gland. Shell W-shaped with lateral wings tapering to acute, offset points. Radula well developed.
Male accessory glands in linear sequence. Web supporting nodules absent. Two species. Type
species: Luteuthis dentatus (O’Shea 1999).
Comments The genus Luteuthis was described by O’Shea (1999) to accommodate a single spec-
imen that differed from other described cirrates in possessing a radula, a bilobed digestive gland
and a unique W-shaped internal shell. O’Shea (1999) included it in a novel family (Luteuthidae),
but molecular evidence suggests it is closely allied to Grimpoteuthis (Piertney et al. 2003) and

should be included in the Grimpoteuthidae. O’Shea (1999) and O’Shea & Lu (2002) suggested
that G. tuftsi should also be included in Luteuthis, although it is probably better retained in
Grimpoteuthis until a full evaluation of the genus is undertaken.
The single Luteuthis dentatus specimen was caught at 991 m in the Tasman Sea (Table 3;
O’Shea 1999). A second species, L. shuishi, was described from the South China Sea (O’Shea &
Lu 2002) and the authors illustrate the dramatic effects of preservation on the form of cirrates, with
the fins appearing considerably larger in the preserved specimen, when the gelatinous tissue of the
mantle has shrunk.
Family Cirroctopodidae n. fam.
Diagnosis Large cirrates with large, paddlelike and broad-based fins. Secondary web absent, shell
V-shaped with lateral walls spikelike. Optic nerve passes though white body in 8–9 bundles. Radula
absent. Posterior salivary glands absent. Digestive gland entire. Cirri of moderate length, approx-
imately equal to maximum sucker diameter, commence between suckers 1 and 2. Gills of ‘half-
orange’ form. Single genus.
Comments The genus Cirroctopus was proposed by Naef (1923) to accommodate C. mawsoni,
which was originally described as Stauroteuthis mawsoni (Berry 1917). Robson (1932) included
both mawsoni and glacialis in his new genus Grimpoteuthis and this generic placement was followed
(e.g., Nesis 1987, Voss 1988a) until the genus was removed from synonymy by O’Shea (1999).
O’Shea (1999) included Cirroctopus within the Opisthoteuthidae and although Cirroctopus shares
some characters with both Grimpoteuthis and Opisthoteuthis, the form of the shell, the fin shape
© 2006 by Taylor & Francis Group, LLC
CIRRATE OCTOPODS
301
and the arrangement of optic nerves are unique and warrant inclusion in a separate family. This
separation is supported by the molecular data of Piertney et al. (2003).
Genus Cirroctopus Naef 1923
Diagnosis As family. Four species. Type species: Cirroctopus mawsoni (Berry 1917).
Comments The genus is restricted to the southern hemisphere (Table 4). C. glacialis was described
from a single specimen trawled near Deception Island (Robson 1930), but has subsequently been
found abundantly around the Antarctic Peninsula (Vecchione et al. 1998). The status of C. antarc-

tica, which was described from 62˚S in the Pacific Sector (Kubodera & Okutani 1986), is unclear.
O’Shea (1999) considered it a junior synonym of C. glacialis, but the description of the beaks
differs from those of C. glacialis (Vecchione et al. 1998). C. mawsoni is recorded from the Indian
Ocean sector (see O’Shea 1999) and C. hochbergi was described from off New Zealand. Voss
(1988a) mentioned, without describing, another Cirroctopus species from Walther Herwig collec-
tions in the Scotia Sea. Bizikov (2004) considers that the shell of Cirroctopus represents a transi-
tional form between the U-shaped shell of Grimpoteuthis and Opisthoteuthis and the paired stylets
of incirrate octopods.
Ecology
Habitat
Evidence from behavioural studies, diet, underwater observations, net catches and interpretation of
morphology suggests that the Opisthoteuthidae are primarily benthic, Cirroctopodidae and Grim-
poteuthidae demersal and Cirroteuthidae benthopelagic. Little is known about habitat preferences.
Most samples are collected from bottom trawls, a selective method that works only on deep-sea
soft sediments and may bias our perspective of the cirrate habitat and distribution toward this type
of substratum. In fact, deep-sea photographic surveys and observations from submersibles showed
cirroteuthids (Roper & Brundage 1972) and Grimpoteuthis (Villanueva et al. 1997) associated with
both soft and rocky bottoms.
Distribution patterns
The cirrates are generally considered a deep-sea group usually found at depths in excess of 300 m,
but have been reported from shallower depths close to the poles, where water temperature remains
Table 4
Family Cirroctopodidae: recognised species and distribution
Species Distribution Comments References
Cirroctopus mawsoni
(Berry, 1917)
Southern Ocean, south of
Australia and in the Indian
Ocean sector (526–911 m)
Type species of genus,

originally described as
Stauroteuthis mawsoni
Berry 1917,
Naef 1923,
O’Shea 1999
Cirroctopus glacialis
(Robson, 1930)
Antarctic Peninsula, Deception
Island (333-914 m)
= Cirroteuthis glacialis
Robson 1930
Robson 1930,
Vecchione et al.
1998
Cirroctopus antarctica
(Kubodera & Okutani, 1986)
Southern Ocean, 62°S in the
Pacific Sector (509–804 m)
Possibly a junior synonym of
C. glacialis (see O’Shea 1999)
Kubodera &
Okutani 1986
Cirroctopus hochbergi
O’Shea, 1999
Off New Zealand only,
750–1200 m
Similar to C. mawsoni O’Shea 1999
© 2006 by Taylor & Francis Group, LLC