BULLETINOFMARINESCIENCE.49(1-2): 137-147, 1991

GROWTH STAGES OF MOROTEUTHIS ROBUSTA (VERRILL, 1881) WITH THE RE-EV ALUATION OF THE GENUS

Kotaro Tsuchiya and Takashi Okutani

ABSTRACT Based on sequential growth stages of Moroteuthis robusta. M. japonica and M. pacifica are synonymous with M. robusta. and smaller stages are bridged to the Onykia "carribaea" species complex. Within the family Onychoteuthidae, the genus Onykia has in common with the genus Moroteuthis the absence of both visceral photophores and dorsal nuchal folds. Young Moroteuthis have a smooth mantle surface with a distinct iridescence, a small number of marginal suckers on the tentacular club and an indistinct cartilageous cap on the endocone. While, large Onykia develop rhomboidal fins, an inverted Y-shaped cartilageous ridge in the funnel groove, and a reduced number of marginal suckers on the club, all of which characterize Moroteuthis. Close examination of a series of O. "carribaea" specimens reveals that the species is not monospecific, but contains more than one species. It is thus suggested that the genus Onykia. therefore, appears to represent juvenile stages of the genus Moroteuthis.

Moroteuthis robusta (Verrill, 1881) is a gigantic squid distributed in the North Pacific. However, its life cycle and growth stages have never been determined. Three smaller species of Moroteuthis were described from the North Pacific, namely, M. loennbergii Ishikawa and Wakiya, 1914, M. japonica (Taki, 1964) and M. pacifica Okutani, 1983, of which the latter two are apparently based on im- mature specimens. Within the family Onychoteuthidae, the genus Moroteuthis Verrill, 1881 and Onykia Lesueur, 1821 have common features that separate them from the other genera, such as, absence of crowded dorsal nuchal folds and visceral photophores, as well as the characters of the mantle surface texture, presence of marginal suckers on the club, and the shape of the gladius (Thiele, 1931; Filippova, 1972). Most species of the genus Onykia have been described from juveniles alone (Pfeffer, 1912). The only exception is O. rancureli Okutani, 1981. On the contrary, in the genus Moroteuthis, a very early juvenile specimen has been reported only for M. robsoni by Dubinina (1980), and information on the early growth stages of this genus is very scarce. The present study re-evaluates the generic characters of Onykia and Moroteu- this, and demonstrates the linkage of these two genera mainly through comparison of a growth series of M. robusta which is compared with early juveniles referable to so-called Onykia carribaea.

MATERIALS EXAMINED

Moroteuthis robustalOnykia carribaea from northwest Pacific: 3 unsexed (94, 135, 181 mm DML), 35°43.7'N 148"00.2'E, 0-100 m, 29 Apr. 1987, R/V KAIYO-MARU,midwater trawl. 1 unsexed (100 mm DML), 35°27.8'N 145°59.4'E 0-105 m, 24 Apr. 1987, R/V KAIYO-MARU,midwater trawl. 1 unsexed (60.7 mm DML), 32°30'N 158°30'E, 0-1,000 m, 29 May 1984, R/V KAIYO-MARU,midwater trawl. 2 unsexed (19.4, 42.8 mm DML), 35°59'N 142°31.8'E, surface, 12 May 1972, R/V SOYO-MARU, dip-netted.

Reference Materials

Moroteuthis ingens (Smith, 1881): I female (137 mm DML), 49°47'S I66°40'E, 136 m, 14 Jan. 1985, R/V SHINKo-MARu,jigging. 1 female (77.0 mm DML), 46°34'S 165°59'E, 155 mm, 3 Dec. 1984, R/V SHINKO-MARU,jigging.

137 138 BULLETINOFMARINESCIENCE,VOL.49, NO. 1-2, 1991

Figures 1-4. Moroteuthis robusta. Mantle texture. 1. 42.8 mm DML. 2. 60.7 mm DML. 3.100 mm DML. 4. 135 mm DML. [Scale bar: 10 mm.]

Moroteuthis loennbergii Ishikawa and Wakiya, 1914: I female (350 mm DML), 30"N I35°E, 0-3392 m, 3 Aug. 1986, R/V KAlYO-MARU,midwater trawl. I male (307 mm DML), 31°37'N 128°13'E, 163 m, 18 July 1988, R/V TANsHu-MARu, bottom trawl. 1 female (102.1 mm DML), 29°N 135°E, surface, date unknown, 1968, P/V NOHMA,dip-netted, National Science Museum, Tokyo. Moroteuthis robsoni Adam, 1962: 3 unsexed (69.5,81,82 mm DML). 43°01'S 167°35'E, 27 Nov. 1984, R/V SHINKO-MARU. Moroteuthis sp.: 1 female (105.3 mm DML), 39°59'N 143°30'E, 18 July 1986, R/V OYASHIO-MARU, jigging. Onykia carribaea auctt.: Onykia sp.A: 1 un sexed (43.7 mm DML), 12°22'S 83°03'W, surface, 26 Aug. 1984, R/V SHINKo-MARU,dip-netted. Onykia sp.B: 1 un sexed (41.6 mm DML), 37°14.5'S 168°15.9'W, 25 Sept. 1956, R/V SHOYo-MARU,from stomach contents of Alepisaurus jerox. Onykia sp.C: I unsexed (40.0 mm DML), 14°56'S 81005'W, 28 July 1984, R/V SHINKo-MARU,long line, National Science Museum, Tokyo. Onykia sp.D: I unsexed (39.0 mm DML), 29°N 135°E, surface, 27 July 1969, PlY NOJIMA,dip-netted, National Science Museum, Tokyo.

RESULTS Several M. robusta specimens of different sizes were compared with each other. The results exhibit quantitative and qualitative sequential morphological changes with growth. Mantle. -In specimens smaller than 42.8 mm DML, the mantle is ornamented with a distinct iridescent epidermis, under which numerous indistinct ridges are observed. The mantle ~mrfaceofthe 60.7 mm DML specimen is ornamented with not only fleshy ridges, but also a weak iridescent layer. The surface texture of the mantle is rugose with numerous fleshy ridges in specimens larger than 94 mm DML (Figs. 1-4). Fins. - The outline of fins are oval in the specimens smaller than 20 mm DML (Fig. 5). In the 42.8 mm specimen, the posterior angle of fins has become acute with the development of tail (Fig. 6). The fins of the 60.7 mm specimen are rhombic (Fig. 7), and those of the specimens larger than 94 mm are sagittate (Figs. 8-10). The fin length is about 50 to 60% ofDML in all specimens, while its width is largest (68.7% ofDML; 152.9% of fin length) at 60.7 mm DML, and smallest (49% ofDML; 84.2% affin length) at 181 mm. The fins are wider than long at smaller than 100 mm, while longer than wide over 135 mm DML. Cartilageous Ridge in the Funnel Groove. The specimens larger than 60.7 mm DML have a cartilageous, inverted Y-shaped ridge in the funnel groove (Figs. 12, 13). The similar ridge is also observed in the 42.8 mm specimen on the border TSUCHIYA AND OKUTANI: GROWTH STAGES OF MOROTEUTH/S ROBUSTA 139

Figures 5-10. Moroteuthis robusta. Ventral view. 5.19.4 mm DML. 6. 42.8 mm DML. 7. 60.7 mm DML. 8. 135 mm DML. 9. 181 mm DML. 10. 1615 mm DML after Sasaki (1929). [Scale bar: 20 mm.] 140 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2,1991

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FiguresII-B. Moroteuthis robusta. Ventralviewof headshowinginvertedV-shapedridgein the funnelgroove.II. 42.8 mm DML. 12. 100 mm DML. 13. 181 mm DML. [Scalebar: 10 mm.] of the funnel retractor muscle (Fig. 11). In specimens smaller than 20 mm DML, the ridge has not developed. The ridge moves anteriorly with growth. Tentacular Club. - The club is short, compact and curved dorsally with a broad aboral keel and protective membranes in the specimens smaller than 42.8 mm DML (Figs. 14, 15). However, the club in the specimens exceeding 60.7 mm is elongate, straight and lanceolate, with a narrow aboral keel and narrow protective membranes (Figs. 16, 17). The carpus consists of 10 or 11 suckers and 8 to 10 fleshy pads. The carpal group is completely fi)rmed in specimens over 42.8 mm as a disc-like cluster or fixing apparatus. At 19.4 mm DML, at least 27 hooks are present on the manus (Fig. 14). The suckers distal to hooks are compressed. One of distal teeth of the inner ring is modified into an incomplete hook which has a long and narrow space under the cusp. The specimens larger than 42.8 mm DML have 30 to 32 hooks on the manus. All marginal suckers of the manus are present in the 19.4 mm specimen. At 42.8 mm DML, nine dorso-distal and eight ventro-proximal suckers are repre- sented only by vestigial pedicels. The specimens larger than 60.7 mm DML completely lack marginal suckers. However, the vestiges and some remnants of sucker pedicels are still present in the 60.7 mm specimen (Fig. 16). Gladius, - The cartilageous cap of the gladius endocone of a 42.8 mm specimen is only about 20% of DML, rather gelatinous and transparent with a brownish color (Figs. 19, 21). The specimens larger than 100 mm DML have an opaque and solid cartilageous cap, about 30% ofDML (Figs. 18,20).

DISCUSSION Three other species of the genus Moroteuthis are reported from the North Pacific, namely, M. loennbergii Ishikawa and Wakiya, 1914, M.japonica (Taki, 1964) and M. pacifica Okutani, 1983. Moroteuthis loennbergii is easily separable by having smaller number of hooks on the club (26 to 28 is more than 30 in M. robusta) and by maturation at a smaller size. The penis elongate and protrudes from the funnel opening in a 307 TSUCHIYA AND OKUTANI: GROWTH STAGES OF MOROTEUTH1S ROBUSTA 141

Figures 14-17. Moroteuthis robusta. Left tentacular club. 14. 19.4 mm DML. 15.42.8 mm DML. 16.60.5 mm DML. 17. 135 mm DML. [Scale bar: 10 mm.]

mm DML specimen. The inverted Y-shaped ridge in the funnel groove is evident even in a spent specimen (350 mm DML). Moroteuthis pacifica was described based on immature specimens, 90.3 to 159.5 mm DML. The numbers of tentacular hooks and carpal suckers of these specimens overlaps those in M. robusta and do not exhibit species difference from M. robusta. Specimens over 94 mm DML but less than 160 mm DML among the examined material match this species well. Moroteuthisjaponica was originally placed in the genus Onykia by Taki (1964). According to the original description this species is characterized by the rhom- boidal fins, presence of an inverted Y-shaped ridge in the funnel groove and a small number (18) of club hooks. The club of the holotype specimen was possibly damaged to some extent and several hooks seemed to be effaced off. The mea- surements and indices of a 60.7 mm M. robusta specimen (Fig. 22) almost match those of Taki, except for the number of hooks on the manus (31 versus 18 in M. japonica). We conclude that both M. japonica (Taki, 1964) and M. pacifica Okutani, 1983 are found to be growth stages of M. robusta and are synonymized with this species. M. loennbergii is a valid species. The genera Onykia and Moroteuthis have been defined and separated from each 142 BULLETIN OF MARINE SCIENCE, VOL. 49, NO, 1-2,1991

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Figures 18-21. Moroteuthis rohusta. Gladius, 18. 181 mm DML, ventral view. 19.42.8 mm DML, ventral view. 20. 181 mm DML, cartilageous cap. 21. 42.8 mm DML, cartilageous cap. [Scale bar: 17-18,10 mm.] TSUCHIYA AND OKUTANI: GROWTH STAGES OF MOROTEUTHIS ROBUSTA 143

Figures 22-26. Small specimens of Moroteuthis species. 22. M. robusta. 60.7 mm DML. 23. M. loennbergii, 102.1 mm DML. 24. M. sp., 105.3 mm DML. 25. M. robsoni, 81 mm DML. 26. M. ingens. 77.0 mm DML. [Scale bar: 20 mm.] 144 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, ]991

Figures 27-31. Large Onykia-type specimens. 27. Moroteuthis robusta, 42.8 mm DML. 28. Onykia sp.C, 40 mm DML. 29. Onykia sp.D, 39 mm DML. 30. Onykia sp.A, 43 mm DML. 31. Onykia sp.B, 41.6 mm DML. [Scale bar: 10 mm.]

other by the texture ofthe mantle surface, fin shape, presence/absence of marginal sucker on the manus, and presence/absence of the cartilageous cap on the gladius (Lesueur, 1821; Verrill, 1881; Thiele, 1931; Nesis, 1987). However, the present study on the growth series of specimens has revealed that these characters are all transitional and sequential with growth. Mantle. -In Onykia, the shape of mantle is rather short, bursiform in small specimens. However, the mantle shape transforms to conieo-cylindrical with growth. In Moroteuthis, the mantle shape is conico-cylindrical to cylindrical. The entire mantle surface is ornamented by an iridescent layer in Onykia. This character is not observed in large Moroteuthis. However, young Moroteuthis ro- busta have a distinct iridescence on the whole body surface (Fig. 22). An iridescent layer is also common in other young Moroteuthis specimens, such as M. loennbergi Ishikawa and Wakiya, 1914 (102.1 mm DML) (Fig. 23), M. robsoni Adam, 1962 (69.5-82 mm DML) (Fig. 25), M. sp. (105.3 mm DML) (Fig. 24) and HAncistro- teuthis lichtensteini" of Rancurel (1970), which is also a juvenile of Moroteuthis as it has no dorsal nuchal fold. This iridescent layer becomes fragile and is lost with growth. The genus Moroteuthis except for M. knipovitchi Filippova, 1972, is also char- acterized by the presence of cutaneous tubercles or fleshy ridges which develop from cartilageous tissue on the mantle surface. The present study determined that large Onykia-type specimens possess numerous cutaneous granules or ridges under the iridescent epidermis (Figs. 27-31). Dubinina (1980) described the papillation on the mantle of a paralarval M. robsoni. Body color is one of the key characters for identification of Moroteuthis, such as reddish (M. robsoni) or pale creamy (M. ingens). The color of the iridescence in small specimens is also variable, such as bronze (M. robsoni), brownish (M. TSUCHIYA AND OKUTANI: GROWTH STAGES OF MOROTEUTHIS ROBUSTA 145

33 34

Figures 32-35. Left tentacular club of Onykia and Moroteuthis. 32. Onykia sp.D, 39.0 mm DML. 33. Onykia sp.C, 40.0 mm DML. 34. Onykia sp.A, 43.7 mm DML. 35. Moroteuthis ingens, 77.0 mm DML. [Scale bar: 10 mm.] loennbergil), white (M. ingens) or blue (M. sp.) (Figs. 22-26). In Onykia species, several types of coloration were previously discriminated by Pfeffer (1912). For example, Pfeffer (1912, p. 62, Taf. 2, figs. 7-12) reported that almost all species of Onykia have bronze-colored iridescence with many purplish brown chromato- phores, while Teleoteuthis verrilli has a pale body color with weak iridescence. This latter combination is common to one of the Onykia sp.B under examination and is similar to that of small M. ingens. Fins. - The present observations revealed that round fins transform to rhombic ones with growth. Pfeffer (1912) described the variable form of fins in several growth stages with a transformation from round to rhombic. Dubinina (1980) described the round fins on paralarvae of M. robsoni. Only Onykia rancureli has paddle-shaped fins, which extend posteriorly beyond the level of the posterior end of the mantle. Funnel Groove. - The existence of an inverted Y-shaped cartilageous ridge in the funnel groove is a common character of immature Moroteuthis, and is found as M. japonica (Taki, 1964) and M. pacifica Okutani, 1983. Only in M. loennbegii, this ridge is observed in mature specimens. This ridge also is present in large Onykia specimens (Pfeffer, 1912, p. 50, Taf. 1, fig. 3). 146 BULLETINOFMARINESCIENCE,VOL.49, NO. 1-2,1991

Tentacle. - The presence of marginal suckers on the club is an important character ofthe genus Onykia (Lesueur, 1821) and Moroteuthis is characterized by absence ofthese suckers (Thiele, 1931). The present study revealed that young specimens of Moroteuthis have marginal suckers, e.g., the 77 mm specimen of M. ingens (Figs. 26, 35). On the contrary, Onykia decreases the number of marginal suckers with growth (Pfeffer, 1912). All marginal suckers are lost in large Onykia (e.g., Onykia sp.D, 39.0 mm DML, Figs. 29, 32). The number of club hooks is another important character for these two genera. The distal-most club suckers in Onykia are in the process of transformation into hooks in many cases (Pfeffer, 1912). Therefore, almost all Onykia species in the literatures are in the juvenile stage. The numbers of hooks and remaining marginal suckers are variable between specimens (Figs. 32-34). This range of club armature variation suggests that several species could be lumped together under a single name, Onykia carribaea. The number of suckers and pads of the carpal group are usually fixed at a very early stage. It is therefore a more useful character for identification. Gladius. - Possession of a short endocone, slightly widened vane and strong rachis are common characters of the gladius of both Moroteuthis and Onykia. (Only O. rancureli has a distinctly different gladius.) The cartilageous cap on the endocone is considered to be an important generic character of the genus M oroteuthis (Thiele, 1931). The present examination shows that large Onykia specimens have a ves- tigial cartilageous cap on the endocone enclosed in a flexible tail (Figs. 27-31). Many nominal species of Onykia were synonymized by Clarke (1966) into one species, O. carribaea. On the contrary, Voss (1975, in Roeleveld) considered that Onykia carribaea is a complex of multi-species. We agree with his latter view. We, therefore, conclude that Onykia represents juvenile stages of Moroteuthis. The genus Moroteuthis Verrill, 1881, therefore, is a junior synonym of the genus Onykia Lesueur, 1821. However, the holotype specimen of Onykia carribaea Lesueur, 1821, the type species of the genus, is no longer extant and the original description is not satisfactory to determine the exact taxon. To stabilize the tax- onomical status of the genus Onykia, the designation of a neotype is needed. For one of the nominal species of the genus Onykia, O. rancureli, the estab- lishment of a new genus is needed (Tsuchiya, unpubl.).

ACKNOWLEDGMENTS

We wish to extend our thanks to the staff of the Hokkaido, Tohoku, Central and Seikai National Fisheries Research Institutes, and the Japan Marine Resource Research Center for the materials under study. We are also grateful to the captains and crews of the R/Vs KAIYo-MARu, Soyo-MARu, SHOYo-MARu, TANSHU-MARU,OYASIO-MARU,SHINKo-MARUand PlY NOHMAfor their great effort in collecting the biological specimens. We also send our gratitude to Dr. T. Kubodera, National Science Museum, Tokyo, for the loan of the specimens under his care. We thank the anonymous reviewers for their kind and careful comments which much improved the paper.

LITERATURE CITED

Adam, W. 1962. Cephalopodes de l' Archipel du Cap-Vert, de l'Angola et du Mozambique. Trabalhos do Centro de Biologia Piscatoria (32): 7-64. Clarke, M. 1966. A review ofthe systematics and ecology of oceanic squids. Adv. Mar. BioI. 4: 91- 300. . Dubinina, T. S. 1980. On a finding of larval Moroteuthis robsoni (Oegopsida, Onychoteuthidae) in south-west Atlantic. Zoo!. Zh. 59: 1094-1096 (In Russian with English title and abstract). Filippova, J. A. 1972. New data on the squid (Cephalopoda: Oegopsida) from the Scotia Sea (At- lantic). Malacologia 11(2): 391-406. Ishikawa, C. and Wakiya, Y. 1914. On a new species of Moroteuthis from the Bay ofSagami, M. LOnnbergii. J. Coll. Agric. Imp. Univ. Tokyo 4: 445-460. 2 pIs. TSUCHIYAANDOKUTANI:GROWTHSTAGESOFMOROTEUTHIS ROBUSTA 147

Lesueur, C. A. 1821. Descriptions of several new species of cuttlefish. J. Acad. Sci. Philad. 2: 86- 101. Nesis, K. N. 1987. Cephalopods of the world. P.F.H. Publications, Inc., New Jersey. 351 pp. Okutani, T. 1981. Two new species of the squid genus Onykia from the tropical Indian Ocean (Cephalopoda, Onychoteuthidae). Bull. Natn. Sci. Mus., Tokyo, (A) 7: 155-163. ---. 1983. A new species of of an oceanic squid, Moroleulhis pacifr:a from the North Pacific (Cephalopoda: Onychoteuthidae). Bull. Natn. Sci. Mus., Tokyo, (A) 9: 105-112. 1 pI. Pfeffer, G. 1912. Die Cephalopoden der Plankton-Expedition. Zugleich eine monographische Uberscht der oegopsiden Cephalopoden. Ergebnisse der Plankton-Expedition der Humboldt-Stiftung 2: 1- 815,48 pis. Rancurel, P. 1970. Les contenus stomachaux d'Alepisaurus ferox dans Ie Sud-Ouest Pacifique (ce- phalopodes). Cah. ORSTOM, SeT. Oceanog. 8(4): 4-87. Roeleveld, M. A. 1975. A revision of Massy's checklists of 'South African' Cephalopoda. Ann. S. AfT. Mus. 66(11): 233-255. Sasaki, M. 1929. A monograph of the dibranchiate cephalopods of the Japanese and adjacent waters. J. Coli. Agr. Hokkaido Imp. Univ., 20. suppl., 1-357,30 pis. Taki, 1. 1964. On eleven new species of the Cephalopoda from Japan, including two new genera of Octopodinae. 1. Fac. Fisheries Animal Husbandry, Hiroshima Univ., 5: 277-343. Thiele, J. 1931. Handbuch der systematischen Veichtierkunde. 2, Classis Cephalopoda. Gustav Fischer, Jena. pp. 948-995. Verrill, A. E. 1881. Report on the cephalopods and on some additional species dredged by the U.S. Fish Commission Streamer "FISH-HAWK", during the season of 1880. Bull. Mus. compo Zool. Harh. 8: 99-116.

DATEACCEPTED: October 23, 1990.

AnDRESS: Laboratory of Invertebrate Zoology, Tokyo University of Fisheries, 4-5-7 Konan, Minato- ku, Tokyo 108, Japan.