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Haliphron atlanticus

The giant octopus Haliphron atlanticus (Mollusca: Octopoda) in New Zealand waters

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STEVE O'SHEA
National Institute
of Water and Atmospheric Research (NIWA)
P.O. Box 14-901 Kilbirnie
Wellington, New Zealand



Abstract
Haliphron atlanticus Steenstrup, 1861 (= Alloposus mollis Verrill, 1880) is reported from New Zealand waters on the basis of a single specimen of giant proportions caught recently by fisheries trawl off the eastern Chatham Rise. This specimen, the largest of this species and of all octopods, proves to be the first validated record of Haliphron from the South Pacific. Although extensively damaged, details of its morphology and anatomy are described.

Keywords
Mollusca, Octopoda, Haliphron atlanticus, Alloposidae, New Zealand.

Photos and Illustrations

Figs. 1, 2: Fresh (prefix, post thaw) whole Haliphron animal

Figs. 3-5: Arm suckers

Figs. 6-9: Female reproductive system

Figs. 10-14: Alimentary canal


INTRODUCTION
Since the New Zealand octopus fauna was comprehensively revised (O'Shea 1999) several additional deep-water species of octopus have been caught in New Zealand waters. The systematic status of a number of these remains the subject of continued research, but one of them, Haliphron atlanticus Steenstrup, 1861, is readily identifiable, and is here recorded from both New Zealand waters and the South Pacific.

Haliphron atlanticus (as Alloposus mollis Verrill, 1880) had been prematurely admitted into the New Zealand fauna (Spencer & Willan 1995) on the basis of Clarke & MacLeod (1982) and Imber's (1992) records of beaks attributed to this species recovered from stomach contents of long-distance foraging marine predators caught in or proximal to New Zealand waters. However, neither record truly demonstrated the occurrence of H. atlanticus nor any other similarly identified cephalopod species within our waters, and it was later removed from the New Zealand faunal inventory (O'Shea 1997). Five years hence, a specimen has been caught in our waters — a capture necessitating this, a further and hopefully final contribution on the subject.

Although the single specimen described here was widely reported in popular press, a less-sensational account is warranted wherein new data on the species' recognised bathymetric and geographic distribution, anatomy and diet is presented. The incomplete nature of this specimen, and the lack of comparable descriptions for any specimen of similar size and maturity, precludes differentiating it from others attributed to the cosmopolitan (fide Thore 1949) H. atlanticus.  Unfortunately type material of H. atlanticus is limited to an arm (Kristensen & Knudsen 1983), further precluding meaningful comparison.


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Haliphron atlanticus is likely to be the last of a suite of pelagic octopus species to be reported from our waters to have a global tropical to subtropical distribution. It brings the total number of octopus species reported from New Zealand to 40, and adds a further family of octopuses, the Alloposidae, from our region. With the occurrence of H. atlanticus in New Zealand, the 40-recorded species are distributed throughout each of the 12 currently recognised families of octopus effectively rendering it the highest octopod familial diversity known for any region.

SYSTEMATICS
Alloposidae Verrill, 1881 (= Haliphronidae sensu Hochberg et al. 1992).

DIAGNOSIS: Suckers uniserial proximally, biserial distal to edge of web; web deep between all arms; body short, gelatinous, densely pigmented; mantle opening wide; funnel embedded in gelatinous tissue; radula heterodont; eyes large, diameter about 40% ML, hemispherical; entire right arm III hectocotylised, detachable, developed in pouch in front of eye; shell vestige absent; mantle-locking apparatus distinct, well developed; funnel organ W-shaped.

The following synonymy is complete for New Zealand citations, but is elsewhere limited to substantial accounts wherein specimens are both described and/or illustrated, as opposed to including numerous uncritical citations from regional checklists, or citations based only on paralarvae or juveniles.

Haliphron Steenstrup, 1861
Type species: Haliphron atlanticus Steenstrup, 1861; by monotypy (Hochberg et al. 1992).

Haliphron atlanticus Steenstrup, 1861: 332.
Kristensen & Knudsen 1983: 221; Willassen 1986: 3540, figs 1-4; O'Shea 1997: 265; O'Shea 1999: 6; Norman, Hochberg & Lu 1997: 375, 376, fig. 11e.
Alloposus mollis Verrill, 1880: 394.
Joubin 1895 (1995 English translation): 15-18, pl. 5, figs 1, 3, 10-11, pl. 6; Robson 1932: 215-217; Thore 1949: 67-72, figs 61-69; Voss 1956; Clarke 1980: 297-299, fig. 233; Alvarino & Hunter 1981: 2632, figs 1-4; Clarke & MacLeod 1982: 35; Hochberg, Nixon & Toll 1992: 227-228, figs 244-245.
Alloposus pacificus Ijima, 1902: 87.
Sasaki 1929: 17-19, pl. 8 figs 68, text fig. 5; Robson 1932: 218-219.
?Alloposus hardyi Robson, 1930
397-400, text figs 17, 18, pl. 4 fig. 1; Robson 1932: 217-218.
?Alloposina albatrossi Robson, 1932
220.
Material examined
NZOI Stn Z10911: F, ML 0.69 m, TL 2.90 m, weight 61.0 kg (pre-fix, wet measured defrosted; specimen incomplete), 44°33.37-33.17'S, 175°45.33-44.21'W, 922-920m, 0704 hrs, 26/10/2001, bottom temperature 6.0°C, R.V. Tangaroa Stn TAN0117/03.

Recognised Distribution
New Zealand, Chatham Rise; otherwise tropical to subtropical, cosmopolitan, and nowhere appearing common; surface to 3180 m. Juveniles are pelagic and occur in surface waters; a descent through the water column occurs with increasing maturity; adults are presumed to be bathypelagic.

Description (Figs 1-14)
Mature female large, incomplete, with estimated intact total length and weight 4 m and 75 kg respectively (fig. 1). Mantle sac like, extensively gelatinous, smooth (fig. 2). Eyes laterally oriented, and probably deeply recessed into head tissues; head not clearly differentiated from mantle. Mantle aperture wide; funnel large, almost entirely fused to ventral surface of mantle, head and arm bases 4; funnel organ lost (freezing artefact); gills with 10 lamellae per inner and outer demibranch.

Arms fragments thick, tube-like and extensively gelatinous. Web extensively damaged, thick, with sector remnants present to at least level of 11th proximal sucker. First 8 or 9 suckers uniserial, thereafter biserial (figs 3, 4). Suckers widely spaced proximally, more closely spaced distally, superficially embedded in arm tissues; first 2 suckers marginally smaller than those that follow, the 4th or 5th attaining greatest diameter (16.2 mm absolute), then similarly sized to the 9th sucker, thereafter gradually decreasing in diameter to the distal-most arm fragments; approximately 100 suckers per most complete arm fragment, with one-third to one-half of that arm missing. Suckers (fig. 5) with base wider than aperture; suction aperture and chamber large; suction pad and wall ring muscular; grasping ring poorly developed.

Reproductive system (figs 6-9) with large ovary sac distended with eggs. Proximal oviduct narrow basally, expanding distally, with extensively ridged glandular lumen. Proximal and distal oviducts of comparable length (figs 6, 7); distal oviduct expanded, stout and thick walled, appearing compressed or collapsed, with extensively ridged, glandular lumen; genital pore terminal. Oviducal ball (fig. 8) two chambered, with proximal chamber appreciably smaller than distal chamber. Eggs absent from proximal and distal oviducts, and oviducal ball; ovarian eggs (fig. 9) teardrop shaped, to 16.0 x 5.0 mm greatest dimension, excluding stalk.

Buccal bulb destroyed; beaks (slightly damaged) recovered from trawl; radular ribbon, anterior-most oesophagus and salivary glands lost, limiting description to visceral components of alimentary canal (fig. 10) and beaks only. Anterior oesophagus narrow, thick walled, opening centrally into capacious crop; crop with corresponding substantial anterior diverticulum, thin walled, with extensively ridged lumen; posterior salivary glands paired, ovoid and heart-shaped. Stomach weakly divided into muscular proximal section and thin-walled distal section; lumen continuous. Spiral caecum thin walled, forming single incomplete whorl. Intestine longer than combined length of crop and residual oesophagus, proximally thick walled, centrally thin walled and dilatated, distally constricted proximal to anus. Hepatic ducts paired; digestive gland of metallic mustard colour, disproportionately large, widest proximal to hepatic ducts, constricted proximal to ink duct, and without apparent pancreas. Exposed portion of ink sac short, c. 25% digestive gland greatest length, into which it is imbedded; ink duct long, opening directly into anus.

Beaks (figs 11-14) dark pigmented with narrow translucent hood and lateral wall margins. Upper beak (figs 11, 12) squat;hood large, projecting posteriorly, extending high above the lateral wall crest; hood and lateral wall margins translucent; jaw irregularly micro-serrate, but with serrations possibly attributable to opposing beak wear; rostral tip acutely pointed. Lateral walls with rounded profile and crest, and very shallow wall fold, extending from the jaw to the lateral wall base. Lower beak (figs 13, 14) squat (height 75 % width and 83% base length); hood broad, long, with rounded crest and very shallow posterior notch; rostrum well developed, damaged. Jaw irregularly serrate but similarly possibly damaged; lateral wall with pronounced fold extending posteriorly to lower edge of lateral wall. Upper beak raw measures (mm): rostrum length 5.6, hood length 42.3, crest length 49.3, shoulder length 26.5, lateral wall height 38.5 mm; and lower beak measures (those marked by an asterisk are damaged; reconstructed figures in parentheses): rostrum length 5.0*(~5.5-6.0), hood length ~ 26.0, crest length 41.0, shoulder length 9.0, wing length 34.0, beak height 30.5 and beak base length 55.0.

DISCUSSION
It is often stated (Thore 1949; Nesis 1987; Hochberg et al. 1992; Young 1995, 1998) that Haliphron juveniles occur in shallow water and adults reside at depth. If correct, it is remarkable, given the preponderance of juveniles elsewhere, that Haliphron juveniles have not been captured in New Zealand waters — especially so given the number of fine-meshed-net research trawls that have been undertaken — trawls that have successfully caught numerous other comparatively shallow-dwelling juveniles of other pelagic genera (e.g. Amphitretus, Ocythoe, Tremoctopus and Argonauta). Fragments of the echinoids Gracilechinus multidentatus, Spatangus sp., Dermechinus horridus and the gorgonian Thouarella sp. recovered from the adult Haliphron carcass reveal the trawl did contact the seafloor, consistent with accounts referring to adult Haliphron as bathypelagic, residing on or in close proximity to the sea floor. Given that the southern slopes of Chatham Rise have been extensively bottom and near-bottom trawled to depths of 1200 m, it is even more remarkable that such an apparently widely distributed, slow-moving and large animal such as Haliphron has until now escaped capture. It has long been held that nets are notoriously inefficient at capturing cephalopods in general, and that Haliphron is capable of out-manoeuvring them (fide Alvarino & Hunter 1981), but it is possible that the absence of juveniles from the upper water column is due to their absence from New Zealand waters throughout the early part of the life cycle, and that adults probably reside at greater depths or locations than are regularly trawled.

This female would appear to be mature, in that the ovary sac is completely distended with large eggs (to 16.0 mm length, excluding stalk), despite eggs being absent from both the proximal and distal oviduct and oviducal gland, and no detached male hectocotylus being recovered from the mantle cavity. Brooding is reported for Haliphron, with the egg mass, albeit difficult to see (Cephbase 2002), described around the buccal region of a female estimated to be of 1 m total length; the eggs are further described as 'considerably smaller than the suckers and grouped into numerous grape-like clusters that formed a single mass of eggs' (Young 1995). Both the largest of suckers and ovarian eggs from the New Zealand specimen are of comparable size, and had the specimen been intact it would have measured ~ 4m total length and possessed suckers considerably larger than those of Young's smaller female. Should Young's smaller female be fully mature, at 1 m in length, brooding, and the eggs correctly, relatively sized, then his specimen differs considerably from the New Zealand female, and suggests that more than one species exists in this genus. Several species of Haliphron have been proposed, but the material upon which they were based was limited, and many of the character states cited as diagnostic for individual species have since proven to be of dubious systematic value. A thorough review would require access to far more comprehensive bathymetric, geographic and ontogenetic collections of specimens of both sexes than currently exists.

Alloposus hardyi Robson, the small male type (ML 40 mm) and otherwise only known specimen, has 6 or 7 lamellae per gill demibranch, similar to the 6 lamellae per demibranch described for Alloposina albatrossi Robson, 1932 (considered to be a synonym of A. mollis (= H. atlanticus)); a comparably sized (42 mm ML) male attributed to A. mollis by Voss (1956: 169), however, has 9 lamellae per gill demibranch.  A large female (ML 115 mm) captured south of Newport, Rhode Island (Young 1972), possesses 18 lamellae per whole gill (probably 9 lamellae in the outer demibranch), as does the near-fully mature female from off Norway (Willassen 1986). The small female type of A. pacificus Ijima, 1902 has 10 lamellae per outer gill demibranch, as do both the female attributed to A. mollis of ML 73.2 mm, total length 300 mm, fixed weight 165 g reported from off the Tanimbar Islands (Norman et al. 1997), and the New Zealand specimen.

Variation in gill lamellae counts is known for the pelagic octopus genera Argonauta, Ocythoe and Tremoctopus, with an ontogenetic increase in filament counts established for each; both Amphitretus sexes, however, have comparable lamellae counts (O'Shea 1999). Although females of pelagic octopuses usually attain larger sizes than males, and possess many more lamellae per demibranch of the gill, comparable data for Haliphron is not available. Females of Haliphron dwarf males (Berry 1912, Sasaki 1929), although Alvarino & Hunter (1981: 28) report sexual dimorphism being limited to hectocotylisation, with the male possessing seven functional arms (?= Heptatus Joubin, 1929) as opposed to the female eight. Nevertheless, assuming the later authors are in error, it might be expected that the male Haliphron has fewer gill lamellae.  However, the account of Voss (1956) lends no support to such an argument. There is a case for renewed systematic effort on this group, with an increasing likelihood that more than a single species exists in this complex. Gill lamellae counts may prove useful for preliminary differentiation of species.

Amongst pelagic octopuses this females reproductive system is unusual in that both the proximal and distal oviducts are of comparable length — a condition similar to that described for the extensively gelatinous Amphitretus, but in contrast to that described for other pelagic genera, eg. Argonauta, Ocythoe and to a lesser extent Tremoctopus, wherein the distal oviducts are torturously long relative to the proximal pair (O'Shea 1999). Thore (1949: 71, fig 67) illustrated the reproductive system of an immature female of total length 400 mm, wherein the distal oviducts are marginally longer than the proximal pair, the proximal chamber of the oviducal ball is larger than that of the distal, and a pronounced papilla is apparent in a position consistent with the genital pore. These character states differ in the New Zealand specimen, but such differences could be attributed to the relative immaturity of Thore's smaller female. However, the generally conservative nature of the female reproductive system, the similarity between those of Haliphron and Amphitretus, and indeed the overall facies of these two genera (with the exception of the paired lateral mantle apertures of Amphitretus), suggests a closer relationship between the Alloposidae and Amphitretidae than had earlier been proposed. Appropriate tissue samples of this otherwise rare deep-water octopus are available on request should someone wish to pursue genetic analyses.

With regard to this species' size, beaks attributed to H. atlanticus (as A. mollis) from Durban- and Donkergat-caught sperm whales had lower hood lengths to ~ 2.2 cm. The weight attributed to one (with a LRL of 0.46 cm and crest length 3.71 cm) is clearly in error — cited as 991 g post preservation (Clarke 1980). Two specimens with dorsal mantle lengths of 0.45 m and 0.3 m reported from off the coast of Norway weighed 41 kg (post fixation) and 25 kg (frozen) respectively (Willassen 1986), with the lower hood length of the beak from the largest 41 kg individual being 2.33 cm; the lower beak rostrum length was not given, but the lower crest length was 4.22 cm (there is some confusion as to the cited lower crest length, in legend denoted TLCL and in table form TSCL), all shorter than the New Zealand female.

This present Haliphron female is the largest known of all octopuses. As its lower beak rostrum length is marginally greater than that recorded by Clarke (1986) for the same species, a measure including the delicate membranous margins not present (digested) on Clarke's beaks, it is possible that H. atlanticus attains slightly larger proportions than currently reported. Crop contents reveal its diet to have comprised non-cuticular red-coloured prey, most likely cnidarian (cf. Atolla sp.), several tiny stones (~ 2 mm greatest dimension), and 2 tiny amphipods (~4 mm dimension), although both the stones and amphipods are likely to have been ingested accidentally. This proves to be quite a remarkable diet for a cephalopod — a diet bordering on inconceivably nutritious for an animal so large.

ACKNOWLEDGMENTS
I wish to thank Paul Grimes, Colin Sutton, Di Tracey (all NIWA) and the skipper and crew of R.V. Tangaroa for retaining this unique specimen, Niel Bruce for his valued suggestions on an earlier version of this manuscript, Chris Thomas for his photographic expertise (both NIWA), and the Foundation for Research, Science and Technology (grant CO1X0026) that has enabled this work and ongoing systematic research on cephalopods to proceed.

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