Collection and Research (2019) 32: 9-18 9

Histioteuthis miranda (Berry, 1918) (Cephalopoda: Histioteuthidae) from the North Pacific Ocean

Kwen-Shen Lee1 and Chung-Cheng Lu2*

¹ Department of Biology, National Museum of Natural Science, Taichung 40453, Taiwan: [email protected] 2 Department of Life Sciences, National Chung Hsing University, Taichung 40227, Taiwan: [email protected]

(Received November 12, 2018; Accepted December 18, 2018; Published online July 28, 2019) DOI : 10.6693/CAR.201912_(32).0002

Abstract. Histioteuthis miranda was previously only known from the South Pacific, eastern South Atlantic, and Indian Oceans. The species was reported in 2000 to be abundant in the vicinity of the Pratas Islands, North Pacific Ocean, but was never described. More specimens were obtained from southern Taiwan in subsequent years. In this paper, we present a description of these North Pacific specimens and compare them to specimens from the southern hemisphere and recently reported Eastern Arabian Sea material. The morphology of all these specimens appears to be similar with the exception of the number of tubercles on arms I and II which are lower in North Pacific specimens.

Key words: Histioteuthis miranda, North Pacific Ocean, Taiwan.

INTRODUCTION continental land masses and nearby islands and submarine rises from “off the southwestern coast Histioteuthis miranda was first described of South Africa eastward in southern subtropical as Calliteuthis miranda from off Gabo Island, waters to the Australia-New Zealand area”. Victoria, Australia (Berry 1918). When Nancy Roeleveld et al. (1992) reported the species as the Voss reviewed the family for the first time, only dominant cephalopod in demersal trawl catches four specimens were available (Voss 1969). at depths of 700~900 m on the lower continental Many more specimens have been collected since slope off the west coast of South Africa. then. The comprehensive revision of the family Lu (2000) recorded specimens of H. miranda by Voss et al. (1998) was based on examination captured in the vicinity of the Pratas Islands (circa of specimens and data of over 100 specimens 21°N, 116°E), South China Sea in the North covering all life stages. Pacific during a survey cruise onboard of the FRV According to Voss et al. (1992, 1998) the Fishery Researcher No. 1 in 1995. The result of species is found in association with the slopes of that survey cruise showed that the species was

*Corresponding author. E-mail: [email protected] 10 Collection and Research (2019) 32: 9-18 abundant in the area: 37 specimens weighing from the anterior-most tubercle to posterior-most 48.6 kg with mantle lengths of 84~315 mm were tubercle; captured by bottom trawls at 10 stations from depths of 458~822 m (Lu 2000). More specimens A2TMLI (arm II tubercle row-mantle length were obtained in subsequent years from waters index)--A2TRL expressed as a percentage of ML; off Donggang, southern Taiwan (ca. 22°27’N, 120°28’E). Although these occurrences were A2TALI (arm II tubercle row-arm length index)- recorded (Lu 2008; Lu and Hsueh 2010; Lu and -A2TRL expressed as a percentage of length of Chung 2017), morphological and morphometric arm II (A2L); comparisons of these animals with their South Pacific, eastern South Atlantic, and Indian Ocean A3TRL (arm III tubercle row length)--length of counterparts have not been published. cartilaginous tubercle row of arm III measured In this paper, we describe these North Pacific from anterior-most tubercle to posterior-most specimens, compare and contrast them with tubercle; descriptions of conspecifics from the southern hemisphere reported by Voss et al. (1998) and A3TMLI (arm III tubercle row-mantle length juvenile specimens from the Eastern Arabian Sea index)--A3TRL expressed as a percentage of ML; recently reported by Sajikumar et al. (2018). A3TALI (arm III tubercle row-arm length index)- -A3TRL expressed as a percentage of length of MATERIALS AND METHODS arm III (A3L);

All specimens were formalin-fixed, stored in NTM--number of tubercles on mantle 70% ethanol, and are lodged in the collection of cartilaginous ridge; the National Museum of Natural Science (NMNS; Taichung, Taiwan). All measurements and indices NTA1--number of cartilaginous tubercles on arm as well as their abbreviations are as defined I; by Roper and Voss (1983). The following new measurements and abbreviations are also used: NTA2--number of cartilaginous tubercles on arm II; MCRL (mantle cartilaginous ridge length)— length of mantle cartilaginous ridge measured NTA3--number of cartilaginous tubercles on arm from the anterior-most tubercle to posterior-most III. tubercle; Histioteuthis miranda (Berry, 1918) MCRLI (mantle cartilaginous ridge length index)- Material Examined. — 2 females, subadults, -MCRL expressed as a percentage of mantle 178.0~199.0 mm ML, Fishery Researcher No. length (ML); 1, Sta. 1, 21°35.5’N, 117°39.7’E~21°34.2’N, 117°37.6’E, near Pratas Is., South China Sea, A1TRL (arm I tubercle row length)—length of Coll. C.C. Lu, 16 Apr. 1995. 520~502 m, bottom cartilaginous tubercle row of arm I measured trawl, NMNS 002157-00027. from the anterior-most tubercle to posterior-most tubercle; 2 females, subadults, 165.0~187.0 mm ML, Fishery Researcher No. 1, Sta. 1, 21°35.5’N, A1TMLI (arm I tubercle row-mantle length 117°39.7’E~21°34.2’N, 117°37.6’E, near Pratas index)--A1TRL expressed as a percentage of ML; Is., South China Sea, Coll. C.C. Lu, 16 Apr. 1995. 520~502 m, bottom trawl, NMNS 002157-00028. A1TALI (arm I tubercle row-arm length index)-- A1TRL expressed as a percentage of the length of 2 males, subadults, 178.0~186.0 mm ML, arm I (A1L); 1 female, subadult, 195.0 mm ML, Fishery Researcher No. 1, Sta. 3, 21°36.5’N, A2TRL (arm II tubercle row length)--length of 117°45.1’E~21°32.9’N, 117°37.7’E, near Pratas cartilaginous tubercle row of arm II measured Lee and Lu : Histioteuthis miranda from the North Pacific 11

Is., South China Sea, Coll. C.C. Lu, 17 Apr. 1995. II; third supports to ventral side of arms III; 458~520 m, bottom trawl, NMNS 002157-00029. fourth supports to dorsal side of arms IV (Fig. 6). Arms I~III joined basally for approximately 1 female, subadult, 184.0 mm ML, Donggang, 1/4 of length by inner web; outer web slightly Pingtung, Taiwan, 22°28’N, 120°26’E, Coll. C.C. developed. Lu, 28 Sept. 2009. NMNS 007924-00019. Arm lengths 1~1.5-times ML, stout basally, tapering to slender tips. Arms II and III longest, 1 female, subadult, 190.0 mm ML, Donggang, subequal; arms IV shortest. Short expanded Pingtung, Taiwan, 22°28’N, 120°26’E, Coll. H.C. swimming keel at mid-length on aboral surface Ho, 5 Jan. 2015. NMNS 007924-00020. of arms III. Aboral surfaces of I, II, and III each with median row of tubercles beneath epithelium 1 female, subadult, 167.0 mm ML, Donggang, for approximately 1/6 ~1/3 length of arm or Pingtung, Taiwan, 22°28’N, 120°26’E, Coll. C.K. 1/3~<1/2 ML (Fig. 7). Numbers of tubercles on Kang, 29 Aug. 2014. NMNS 007924-00024. arms varying, ranging 8~14 on arms I, 8~12 on arms II, and 6~10 on arms III. Keels on aboral surfaces of arms not apparent. Suckers on arms RESULTS biserial. Suckers subequal in size, except near tip of arms. Distal margins of sucker rings with many Description. — A histioteuthid reaching a large low square teeth, often with obscure demarcation; size, largest immature female specimen examined proximal margins ragged to smooth. 199 mm in ML. Mantle conical, robust, walls Tentacles stout, moderately long, about thick, width approximately 40% ML; widest point 2~3-times ML, 6~10-times club length. Club just posterior to anterior margin, sides tapering expanded; manus with about 6 or 7 rows of posteriorly to blunt tip. Median anterodorsal closely set suckers; some median suckers of 2 margin produced into low blunt angle (Fig. 1); dorsomedial rows slightly enlarged. Sucker rings median anteroventral margin slightly emarginate with numerous small sharp teeth around entire between blunt lateral angles (Fig. 2). Ridge margin. Suckers on dactylus uniform, very small, of low, poorly developed tubercles beneath in 6 or 7 rows proximally, reduced to about 4 epithelium extending along dorsal midline rows near tip. Distal half of aboral surface of from just below anterior margin of mantle to club with median swimming keel; no longitudinal approximately 2/3 ML to posterior tip (Fig. 3). cleft apparent on proximal half. Carpal adhesive Number of tubercles ranging 14~21 on specimens apparatus commences at approximately 1/3 examined here. of tentacular length from tip of club, pattern Fins combined, nearly circular in outline; variable: e.g., on a female specimen of 187 mm slightly wider than long, length approximately 1/3 ML (specimen 3, Table 1), it commences with 1 to 1/2 ML on specimens examined here. Posterior sucker (s), followed distally by 1 pad (p), 1 p, 1 s, margins of lobes extending beyond tip of mantle, 1 s, 1 p, all widely spaced, then 2 ss, 2 pp, 1 s, all joined with median notch. closely set, then crossing over to dorsal margin Funnel stout with double bridle. Locking with 1 s, 1 p, 1 s, 1 p, 1 s, 1 p, 1 s, 1 p, 1 s; on a cartilage typically histioteuthid, strong; central female specimen of 165 mm ML (specimen 4, groove of funnel locking cartilage deep. Dorsal Table 1), the pattern is 1 s, 1 p, 1 p, 1 s, 1 s, 1 p, member of funnel organ fleshy and wrinkled, 1 p, all widely spaced, then 2 ss, 1 p closely set, anterior apical papilla present; 2 ventral crossing over to dorsal margin with 1 p, 1 s, 1 p, 1 pads large, oval (Fig. 4). Funnel valve large, s, 1 p, 1 s. semicircular (Fig. 4). Numerous widely spaced photophores set in 9 Head large, with typical asymmetrical eyes, or 10 diagonal rows across entire ventral surface left eye approximately twice size of right eye; of mantle except for closely set anterior marginal a single nuchal fold dorsal to small olfactory row. Photophores on dorsal surface of mantle and papilla (Fig. 5). head markedly fewer and smaller. Photophores on Buccal membrane seven-membered. First ventral surface of head about the same size and support bifurcate, attached to dorsal side of concentration as on ventral surface of mantle; set arms I; second supports bifurcate, attached to in diagonal rows except for posterior marginal ventral side of arms I and dorsal side of arms row and round eyelids. Sixteen large photophores 12 Collection and Research (2019) 32: 9-18

Table 1. Mantle measurements (in mm) and indices of ten specimens of Histioteuthis miranda from the North Pacific Ocean

NMNS Reg. 2157- 2157- 2157- 2157- 2157- 2157- 2157- 7924- 7924- 7924- no. 0027 0027 0028 0028 0029 0029 0029 00019 00020 00024 Specimen no. 1 2 3 4 5 6 7 8 9 10 Sex f f f f f m m f f f ML (mm) 199 178 187 165 195 186 178 184 190 167 MWI 38.9 43.5 43.8 40.8 39.8 38.9 36.9 42.0 45.2 *flattened HLI 42.7 39.9 43.6 50.6 40 39.2 38.2 48.9 57.9 44.1 HWI 29.7 33.3 27.7 33.8 32.1 31.0 32.6 34.4 34.8 40.5 FLI 27.1 34.8 35.8 42.4 36.9 36.6 38.8 * 37.4 28.4 FWI 41.7 42.7 42.8 49.1 44.6 48.4 43.8 46.2 48.9 58.1 A1LI * * 110.7 * 98.5 112.9 * * 124.2 144.3 A2LI * * 131.0 * 100.5 * 96.6 133.7 * 170.6 A3LI * * 122.5 * * 103.8 101.1 115.8 128.9 143.7 A4LI * * 89.3 * 92.3 86.0 91.0 91.3 97.4 123.4 TLI 170.4 182.0 182.9 157.0 156.4 182.8 203.4 200.0 221.1 270.1 ClLI 21.3 20.5 20.6 25.5 23.0 21.4 20.2 26.0 24.7 29.9 MCRLI 33.4 40.4 40.2 40.0 38.5 37.8 35.1 36.5 33.3 42.4 A1TMLI 32.4 43.4 35.1 35.6 34.8 28.2 31.5 29.2 30.2 30.0 A1TALI * * 31.7 * 35.3 24.9 * * 24.3 20.8 A2TMLI 25.0 35.7 25.9 27.3 31.5 30.4 25.3 30.5 25.3 36.5 A2TALI * * 19.7 * 31.4 * 26.2 22.8 * 21.4 A3TMLI 19.4 27.4 21.6 22.4 20.1 21.8 21.6 23.0 16.4 31.4 A3TALI * * 17.7 * * 21.0 21.3 19.8 12.7 21.9 NTM 17 18 19 18 21 19 16 15 19 14 NTA1 10 12 14 14 12 11 12 8 10 10 NTA2 8 11 8 8 11 12 9 9 9 11 NTA3 6 7 7 7 6 9 7 8 6 10 f, female; m, male. All other terms are defined in the text. * Denotes a damaged body part, and no measurement was taken. in complete circlet around margin of right eyelid; to tip (Fig. 8). Arms III, II, and I with 2 or 3 17 or 18 photophores in broken pattern around longitudinal rows of photophores. margin of left eyelid. No mature males available for describing the Base of arms IV with 1 or 2 rows of 5 hectocotylus, genitalia, or spermatophores. photophores arranged diagonally, followed by Gladius, beaks, and radula were not examined. many rows of 4 diagonally arranged photophores Table 1 shows mantle lengths, indices, and distally; rows gradually reduced distally to 2 with counts of the specimens studied. only the original second ventral row extending Lee and Lu : Histioteuthis miranda from the North Pacific 13

DISCUSSION juveniles (ML 13~41 mm). They presented two different, but not grossly dissimilar, sets of data Until publication of the records from the on the number of tubercles on the dorsal three South China Sea (Lu 2000; Norman and Lu pairs of arms. These numbers do not grossly 2000), H. miranda had only been reported differ from the data presented by Voss et al. from the southern hemisphere (Roeleveld et (1998). If these specimens are conspecific, the al. 1992; Voss et al. 1998). Voss et al. (1998) numbers of tubercles on the dorsal three pairs of stated it as having a ‘restricted south subtropical arms appear to be fixed at the juvenile stage, and distributional pattern’ in the Pacific and Indian do not increase with growth after the juvenile Oceans. stage. At the present time, we consider all of Histioteuthis oceani, a closely related species, those specimens reported by Voss et al. (1998), is reported to have a ‘broad, Pacific equatorial Roeleveld et al. (1992), Sajikumar et al. (2018), distribution’, ‘from the Galapagos Islands to and the present study to be conspecific. The the Indo-West Pacific, extending northward to slight differences in the numbers of tubercles on about 30°N, north of Hawaii and southward in the arms perhaps warrant a more-in-depth study adjoining areas peripheral to the oligotrophic to determine whether these differences are due central waters’. The species is distinct from H. to population differences or are due to species miranda in a number of important features, e.g., differences. the size at maturity, the development and length of the cartilaginous strips on arms I~III, the number of tubercles on the cartilaginous strip ACKNOWLEDGEMENTS on the arms, the number of gill lamellae, and the number of photophores on arm IV. Voss et al. We are indebted to Dr. Malcolm Dunning, (1998) summarized these differences between Queensland Museum, Australia and an H. miranda of the southern hemisphere and H. anonymous reviewer for their critical review of oceani in Table 15 of their paper. This table was the manuscript and constructive suggestions. modified and is presented as Table 2 in this paper, with updated data from the present study and from Sajikumar et al. (2018). REFERENCES It is clear from Table 2, that the data of the present material fit well with data presented Khromov, D.N. 1996. Some notes on the shelf for H. miranda from the southern hemisphere, and slope cephalopod fauna of Vietnam, and a except that the numbers of tubercles on arms new species of Sepia (Cephalopoda, Sepiidae) I and II are lower in North Pacific specimens from this region. Ruthenica 5(2): 130-145. (ML165~199 mm) compared to the numbers of Lu, C.C. 2000. Diversity of Cephalopoda from tubercles on arms I and II on specimens from the waters around the Tong-Sha Island the southern hemisphere (ML 38~249 mm; Voss (Pratas Islands), South China Sea. In Y.S. et al. 1998) and the Eastern Arabian Sea. Data Chow, F.K. Hsieh, S.H. Wu, and W.H. Chou of all three groups distinctly differ from the (eds.). Proceedings of the 2000’ Cross- data of H. oceani (Voss et al. 1998). With the strait Symposium on Biodiversity and discovery of this North Pacific occurrence, the Conservation. Taichung, Taiwan: National distributional pattern of the species in the Pacific Museum of Natural Science. pp. 201-214. Ocean requires reconsideration. The distribution Lu, C.C. 2008. A revised checklist of of H. miranda is clearly not confined to the Cephalopoda of Taiwan. In K.-T. Shao, C.-I southern hemisphere. There is no record of its Peng, and W.-J. Wu (eds.). 2008 Taiwan occurrence north of 25°S or south of the present species diversity I. Research and status. study area (21°33’N) in the western North Pacific. Taipei, Taiwan: Forestry Bureau, Council of The record of H. miranda from Vietnam by Agriculture, Executive Yuan. pp. 123-131. Khromov (1996) which was treated as a ‘species Lu, C.C. and W.S. Chung. 2017. Guide to the undetermined’ by Voss et al. (1998) may indeed cephalopods of Taiwan. Taichung, Taiwan: represent this species. National Museum of Natural Science. 560 pp. The 11 specimens from the Eastern Arabian Lu, C.C. and M.-M. Hsueh. 2010. Class Sea studied by Sajikumar et al. (2018) are Cephalopoda. In K.-T. Shao, C.-I Peng, and 14 Collection and Research (2019) 32: 9-18

Table 2. Comparison between members of the Histioteuthis miranda species group (following Voss et al. 1998 with information from North Pacific Ocean and Eastern Arabian Sea specimens added)

Character H. miranda H. miranda H. miranda (Dongsha H. oceani (From Voss et (From Voss et (From Sajikumar & Taiwanese al. 1998) al. 1998) et al. 2018) specimens) Known Southern Eastern Arabian Dongsha Is. (=Pratas Pacific equatorial and geographic range Benguela Sea Is.), adjoining areas peripheral Current, (9°~11°N, Donggang, southern to central water masses of subtropical 73°~72°E) Taiwan N and S Pacific and tropical W Indian Ocean, subtropical waters of Australia Size ranges 93~267 mm 13~41 mm 165~199 mm 35~70 mm studied (ML) Buccal 2nd supports Not stated 2nd supports bifurcate 2nd supports single to membrane bifurcate to to arms I+II arms II arms I+II Head Length ca. Not stated Length ca. 38%~58% Length ca. 56%~62% ML 36%~49% ML ML Width 56%~80% ML Width ca. Width ca. 26%~35% 46%~53% ML ML Development Weakly Not stated Weakly developed, Well developed, on and position developed, deeply embedded in surface, of tubercles on deeply body tissue, Arms I: 46%~83% AL arms I~III embedded in 20.8%~35.3% AL body tissue, Arms II: 19%~39% AL 19.7%~31.4% AL Arms III: 17.6%~21.9% AL Numbers of Arms I: 14~19 Arms I: 12~18 Arms I: 8~14 (11.3 Arms I: 25~36 tubercles on Arms II: 11~16 (14~16)* 1.81) Arms II: 23~30 arms I~III Arms III: 7~13 Arms II: 11~14 Arms II: 8~12 Arms III: 17~21 (11~13)* (9.6 Arms III: 7~12 Arms III: 6~10 (8~12)* (7.3 * Two sets of numbers are presented in the paper Photophores in 5 in first 2 to 5 in first 2 to 3 5 in first 2 to 3 rows, 6 in first 2 to 3 rows, 5 in diagonal rows 3 rows, 4 in diagonal rows 4 in subsequent rows subsequent rows on basal half of subsequent rows arms IV Gill lamellae in 39~41 Not stated 37~40 26~28 outer demibranch Size at maturity Males: 93~262 Not stated Males >186 mm ML; Small to ?medium, ca. mm ML; Females >199 mm 50~?100 mm ML Females: ML 200~267 mm ML ML, mantle length; AL, arm length. Lee and Lu : Histioteuthis miranda from the North Pacific 15

W.-J. Wu (eds.). Taiwan species checklist (Cephalopoda: Histioteuthidae) in the Eastern 2010. Taipei, Taiwan: Forestry Bureau, Arabian Sea and determination of its age from Council of Agriculture, Executive Yuan. statoliths. Thalassas doi:10.1007/s41208-018- pp.713-716. 0076-z. Norman, M.D. and C.C. Lu. 2000. Preliminary Voss, N.A. 1969. A monograph of the checklist of the cephalopods of the South Cephalopoda of the North Atlantic. The family China Sea. Special edition on the Biodiversity Histioteuthidae. Bull. Mar. Sci. 19(4): 713- of the South China Sea. Raffles Bull. Zool. 867. Suppl. 8: 539-567. Voss, N.A., K.N. Nesis, and P.G. Rodhouse. Roeleveld, M.A.C., M.R. Lipiński, C.J. Augustyn, 1998. The cephalopod family Histioteuthidae and B.A. Stewart. 1992. The distribution and (Oegopsida): systematics, biology, and abundance of cephalopods on the continental biogeography. Smithson. Contrib. Zool. slope of the eastern South Atlantic. S. Afr. J. 586(II): 293-372. Mar. Sci. 12: 739-752. Voss, N.A., S.J. Stephen, and Zh. Dong. 1992. Roper, C.F.E. and G.L. Voss. 1983. Guidelines for Family Histioteuthidae Verrill, 1881. In M.J. taxonomic descriptions of cephalopod species. Sweeney, C.F.E. Roper, K.M. Mangold, M.R. Mem. Natl. Mus. Victoria 44: 49-63. Clarke, and S.v. Boletzky (eds.). “Larval” Sajikumar, K.K., V. Venkatesan, C.P. Binesh, and juvenile cephalopods: a manual for their G. Mohan, N.K. Sanil, V. Kripa, and identification. Smithson. Contrib. Zool. 513: K.S. Mohamed. 2018. Presence of the 73-91. wondrous jewel squid Histioteuthis miranda

北太平洋的奇妙帆魷

李坤瑄1 盧重成2

1國立自然科學博物館生物學組 40453 台中市北區館前路一號 2國立中興大學生命科學系 40227 台中市南區興大路145號

奇妙帆魷過去只知分布於南太平洋及印度洋海域，西元2000年被記錄到有豐富的族群棲 息在東沙島附近，但從未被詳細描述發表。近年來，陸續有更多的標本在臺灣南部海域被採 獲，本研究針對這些採自北太平洋的標本進行詳細描述，並與南半球的標本進行比對。

關鍵詞︰奇妙帆魷, 北太平洋, 台灣 16 Collection and Research (2019) 32: 9-18

Fig. 1. Histioteuthis miranda, dorsal view of whole Fig. 2. Histioteuthis miranda, ventral view of whole animal, female, subadult, 165.0 mm ML, NMNS animal, female, subadult, 165.0 mm ML, NMNS 002157-0028 (scale bar, 20 mm). 002157-0028 (scale bar, 20 mm).

Fig. 3. Histioteuthis miranda, dorsal mantle cartilaginous ridge showing tubercles, female, subadult, 165.0 mm ML, NMNS 002157-0028 (scale bar, 20 mm). Lee and Lu : Histioteuthis miranda from the North Pacific 17

Fig. 4. Histioteuthis miranda, funnel valve and funnel organs, male, subadult, 186.0 mm ML, NMNS 002157- 0029 (scale bar, 10 mm).

Fig. 5. Histioteuthis miranda, olfactory papilla, male, subadult, 186.0 mm ML, NMNS 002157-0029 (scale bar, 10 mm). 18 Collection and Research (2019) 32: 9-18

Fig. 6. Histioteuthis miranda, buccal membrane connectives showing attachments to arms, female, subadult, 165.0 mm ML, NMNS 002157-0028.

Fig. 7. Histioteuthis miranda, tubercles on left arms Fig. 8. Histioteuthis miranda, photophores on right arm I and II, female, subadult, 165.0 mm ML, NMNS IV, female, subadult, 165.0 mm ML, NMNS 002157- 002157-0028 (scale bar, 10 mm). 0028 (scale bar, 10 mm).