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

Fin size varies from large in Cirroctopus, Cirroteuthis and Cirrothauma through moderate Grimpoteuthis, Luteuthis and Stauroteuthis to small Cryptoteuthis and Opisthoteuthis.. A dorsal v

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 OCTOPODSMARTIN A COLLINS1& ROGER VILLANUEVA2

1 British Antarctic Survey, Natural Environmental Research Council,

High Cross, Madingley Road, Cambridge, CB3 0ET, U.K.

E-mail: macol@bas.ac.uk

2 Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas (CSIC),

Passeig Marítim de la Barceloneta 37-49, E-08003 Barcelona, Spain

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, teuthis species, the biology of the cirrates is poorly studied The data on reproductive biology indicate

Opistho-that spawning is extended, with growth continuing during a reproductive period Opistho-that probablyoccupies much of the life cycle, an unusual strategy in cephalopods Diet studies suggest that benthiccirrates feed on small-sized organisms with low swimming speeds and the main prey are amphipodsand polychaetes Cirrate predators include sharks, teleost fishes, fur seals and sperm whales Behav-ioural observations, based on underwater photographs, submersible observations and aquariumstudies, show a range of postures, modes of locomotion and responses to disturbance that differbetween the families Behavioural observations also help interpret the unusual morphology andphysiology 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, pairedfins, 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 evolutionhave 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 foundshallower in cold waters at high latitudes (Voss 1967, 1988a) and include some of the largest

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 therecent 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 isimportant to all studies, but taxonomic work has been handicapped by the poor state of typespecimens, 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 workhas been undertaken on the deeper species The existing data indicate important differences inreproduction between the cirrate and incirrate octopods, notably in lack of seasonality associatedwith spawning and the continuous production of eggs and spermatophores in adult individuals ofthe 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 externaldisturbance (e.g., Boletzky et al 1992, Vecchione & Young 1997, Villanueva et al 1997, Villanueva2000) These behavioural observations have been indispensable in interpreting the morphologicalcharacteristics 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 newfindings and help explain the function of other unusual morphological features such as the areolarspots and mantle ‘windows’

Here the taxonomy of the group is reviewed and updated and the limited data on ecology andbehaviour summarised To underpin the taxonomic review, the first section briefly compares theanatomy 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 areconsidered modifications to deep-sea life (reduction or loss of radula and posterior salivary glands;

CIRRATE OCTOPODS

loss of ink sac; reduction of gills; narrowing of funnel aperture; large eggs), which are shared by deepincirrate species (Robson 1925, Voss 1988b) The gelatinous nature and few hard parts of the cirratesmean 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 fordealing 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 pairedcirri, which are interspersed between a single row of suckers that are highly variable in form Thebody 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 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).

Opistho-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) topus glacialis Sources (with permission where required): (A, B, F) Collins unpublished; (C) from Collins &

Cirroc-Henriques (2000); (D) from Collins (2003); (E) from Villanueva et al (2002) Scale bars = 100 mm.

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.

CIRRATE OCTOPODS

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 inthe 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 notpossess 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 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

Opistho-to it by a single, delicate vertical membrane (the intermediate or secondary web) that is attachedalong the dorsum of the arm (Figure 3A; see Vecchione & Young 1997) The secondary web ofthe 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.

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 incirrateoctopods (Villanueva & Guerra 1991) (Figure 5A,B) and the suckers of the other Opisthoteuthidaeand 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 & Henriques2000) (Figure 5E) In both sexes the first 5–6 (oral) suckers are close together, then 7–23 are spacedout, with maximum intersucker distance between suckers 13 and 14, with the distal suckers smalland 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 isnot clear if the suckers of both males and females produce light (Collins & Henriques 2000) Thesefindings 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 distalsuckers, with the infundibulum resembling a small cap (Figure 5C,D) It has been suggested thatthere 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 acetabulumchamber; 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 extremelylong, particularly on the midsection of the arms (approximately 50% of mantle length (ML) in

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.

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.

CIRRATE OCTOPODS

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 usefultaxonomic character in the incirrate octopods, is rather indistinct in the cirrates, but in those speciesfor 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 mantleaperture and either side of the funnel in all cirrate species They are served by a complex nervenet, 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 sepioidform 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 ofthe cirrate heart

The internal shell is distinct in each of the genera (Figure 7; see Bizikov 2004 for detail of theform 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

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 centralcartilaginous core, which is covered by thick bundles of muscle fibres, parallel to the fin axis, thatinsert 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 tothe fin plane

The digestive system is similar in all the cirrates (Figure 9) consisting of buccal mass andbeaks, 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 purplecolour that may be associated with the consumption of bioluminescent prey (Vecchione & Young1997) A swelling of the oesophagus (crop?) has been reported for some species, but is ratherindistinct The stomach, which lies in a groove in the digestive gland, is lined with a thick cuticleand leads, via a narrow duct, to the caecum, which typically has a single turn and is connected tothe 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.

CIRRATE OCTOPODS

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 incolour between species The form of the optic nerve is an important taxonomic character: in theCirroteuthidae and Grimpoteuthidae the optic nerve passes through the white body as a singlebundle of fibres (Figure 13), whilst in Opisthoteuthidae there are two to four bundles of nerve fibresand in Cirroctopodidae there are eight or nine bundles The form of the stellate ganglion andepistellar body has also been used as a taxonomic character (e.g Robson 1932, Voss & Pearcy1990) 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.

The female reproductive system is similar in all the cirrates consisting of ovary, thin-walledproximal 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 sizesand developmental stages (see section on reproduction, p 302) The oviducal gland consists of twosections, both striated, but differing distinctly in colour The proximal section, which is usuallylighter in colour functions as a spermatheca (Aldred et al 1983) and is the presumed location offertilisation, whilst the distal section is responsible for providing the tough egg case.

The male reproductive system is more variable, consisting of testes, seminal vesicle, accessorygland(s) and terminal organ (or penis) (Figure 14) The testis is located posteriorly in the mantlecavity, and leads via the vas deferens to the seminal vesicle, which passes through the accessorygland(s) to the terminal organ The number and size of the accessory glands vary between generaand 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.

CIRRATE OCTOPODS

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.

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.

CIRRATE OCTOPODS

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.

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 sectionsthrough the spermatophores show aggregations of spermatozoids, with the heads oriented towardthe 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.

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 morphologicaldata 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 secondaryweb linking arms to primary web Digestive gland entire Cirri long Radula and posterior salivaryglands 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 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 inthe high Arctic to 4500 m in the ocean basins, with distribution probably limited by temperaturerather than depth A specimen tentatively attributed to this species was caught off New Zealandbut may represent a new species (O’Shea 1999)

circum-Cirroteuthis hoylei was described from a single specimen caught during the Challenger dition (Station 298) and was originally identified as C magna by Hoyle (1885a) The specimen is

Expe-small and badly damaged, but Robson (1932) considered that it represented a new species, which

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 (seeAldred et al 1983) However, geographic variability in these specimens has not been criticallyreviewed Recent captures in the northeast Atlantic have been taken in bottom trawls at depths from3900–4800 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).

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

CIRRATE OCTOPODS

Genus Stauroteuthis Verrill, 1879

Diagnosis Large-sized cirroteuthids with moderate fins and U-shaped shell Arms long withextremely 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 poorcondition of the two South African specimens prevented proper comparison (Collins & Henriques2000)

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 aweb 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 imens, attributable to a new species of Froekenia, have been found at 500–810 m at the Error

spec-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, lateralwalls tapering to fine points Optic nerves pass through white body in two to four bundles Twofields of enlarged suckers in mature males Digestive gland entire or bilobed Radula and posteriorsalivary 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 theshallowest of the cirrate families, typically found at depths from 300–2200 m

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 teuthis (Sasaki 1920), and has recently been considered a Grimpoteuthis (Voss 1988a) Although

Stauro-the holotype (male) is in poor condition, it is clear from Stauro-the original illustration that Stauro-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

CIRRATE OCTOPODS

Table 2 Family Opisthoteuthidae: recognised species and distribution

Opisthoteuthis agassizii

Verrill, 1883

NW Atlantic (227–1935 m) Restricted to western

Atlantic, reports from

E Atlantic are misidentifications.

Similar to O grimaldii, but

digestive gland entire

Previously misidentified as

O agassizii

Villanueva et al 2002, Villanueva 1992b

Ijema & Ikeda, 1895

N Pacific, off Japanese coast Ijima & Ikeda 1895

Opisthoteuthis extensa

Thiele, 1915

Indian Ocean, SW of Sumatra

Joubin 1903, Villanueva et al., 2002

lobe near the anterior fin insertion Shell vestige U-shaped; lateral sides parallel, not tapered to finepoints Radula monodont or absent Posterior salivary glands small or absent Web supported bysingle fleshy nodules on the ventral side of the arms Digestive gland entire (single lobe) Suckersexual 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 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

large-five specimens from the northwest Atlantic Of the large-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 fourthtaken 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)

CIRRATE OCTOPODS

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 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

Grim-the type species of this genus is described in detail

Table 3 Family Grimpoteuthidae: recognised species and distribution

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

Voss & Pearcy, 1990

Known only from two specimens described by Hoyle; generic status uncertain

Hoyle 1885a,b, 1886

Grimpoteuthis megaptera

(Verrill, 1885)

material, now lost

Voss & Pearcy, 1990

NE Pacific (3585–3900 m) Large species; possesses