A preliminary review and in situ observations of the spookfish genus Harriotta (Holocephali: Rhinochimaeridae)

Abstract

The taxonomic status of two species of the spookfish genus Harriotta Goode and Bean 1895 is revised and discussed. On the basis of a literature review along with a comparison between the two species formerly considered valid, H. haeckeli Karrer 1972 is synonymized with H. raleighana Goode and Bean 1895, and Anteliochimaera chaetirhampha Tanaka 1909 previously regarded as a junior synonym of the latter is resurrected as a valid species. The revised H. raleighana is newly recorded from Japan as well as the North Pacific based on two voucher specimens collected from Hyuga-nada off Kyushu, southern Japan; the record extends the species’ known range approximately 8000 km northward from the South Pacific. In addition, secondary sexual characteristics of H. raleighana are documented for the first time, which further illuminates pronounced differences between the two species of Harriotta; H. raleighana is also revealed to have a smaller size at maturity compared with H. chaetirhampha. In the northwestern Pacific, the species show bathymetric zonation with a narrow sympatric zone at depths around 1600 m (1535–2611 m in H. raleighana vs. 906–1654 m in H. chaetirhampha). In situ behavior of these species is described and discussed from video footage.

Introduction

Comprising two valid species, the spookfish genus Harriotta Goode and Bean 1895 is widely distributed in deep-waters of the world’s oceans. The type species Harriotta raleighana Goode and Bean 1895 is considered cosmopolitan, being a senior synonym of Anteliochimaera chaetirhampha Tanaka 1909, Harriotta curtissjamesi Townsend and Nichols 1925, and Harriotta opisthoptera Deng, Xiong and Zhan 1983; the second species Harriotta haeckeli Karrer 1972 is known sporadically from the North and East Atlantic Ocean, southern Indian Ocean, and southwestern Pacific Ocean off southeastern Australia (Last and Stevens 2009; Ebert 2014; Weigmann 2016). The genus is unique within the family Rhinochimaeridae in having the following combination of features: upper caudal-fin lobe well developed, without tubercles; anal fin absent; mouth located below or only slightly anterior to eye; tooth plates covered with ridges and knobs (Last and Stevens 2009; Didier et al. 2012; Ebert and Mostarda 2013; Ebert 2014).

During a bottom trawl survey conducted by the R/V Shinkai-maru of the Japan Marine Fishery Resources Research Center, two (mature male and female) specimens of an unusual Harriotta were collected from the northwestern Pacific off southern Japan. A subsequent examination confirmed that they represent the first North Pacific records of what many authors have called H. haeckeli, with the male exhibiting previously unknown secondary sexual characteristics of the species. However, a review of the literature and a comparison between the two species formerly considered valid highlighted important taxonomic problems of the genus, which resulted in name changes. We also report useful characters for in situ species identification of the genus based on video footage. Among the JAMSTEC E-library of Deep-sea Images (J-EDI; JAMSTEC 2019), which comprises about 38 thousand-hour long videos and more than 1.5 million photographs showing various deep-sea organisms and geological features worldwide, were many records of in situ individuals of Harriotta in Japanese waters. Swimming behavior of the two species is also discussed here for the first time.

Materials and methods

Methods for taking counts and making measurements follow procedures described by Compagno et al. (1990), Didier and Stehmann (1996), and Didier and Nakaya (1999). Total and body lengths are expressed as TL and BDL, respectively. Chimaera length (CL) was measured from the tip of the snout to the posterior edge of the upper lobe of the caudal fin (Finucci et al. 2017). Abbreviations for morphometric characters are listed in Table 1. Institutional codes follow Fricke and Eschmeyer (2019). All Japanese specimens examined are deposited in the Laboratory of Marine Biology, Faculty of Science and Technology, Kochi University (BSKU). The specimens of Harriotta raleighana (species formerly known as H. haeckeli) (BSKU 49576, male, 501 mm TL, 186 mm BDL; BSKU 49396, female, 629 mm TL, 239 mm BDL) were collected on 3 April 1991 from Hyuga-nada off Miyazaki, Kyushu (32°18ʹN, 132°11ʹE–32°16ʹN, 132°11ʹE), at a depth of 1481 m. Fourteen specimens of H. chaetirhampha (species previously regarded as a junior synonym of H. raleighana) (530–951 mm TL, 205–385 mm BDL) were examined as comparative materials: BSKU 23063 (female, 530 mm TL, 205 mm BDL), BSKU 23064 (female, 515 mm TL, 241 mm BDL), BSKU 120781 (female, 915 mm TL, 377 mm BDL), Tosa Bay, 32°58.8ʹN, 133°51.3ʹE, 1043 m depth, R/V Kaiyo-maru, cr. SK-75-2, sta. 19, tr. 2, bottom trawl, coll. by O. Okamura et al., 26 Jan. 1975; BSKU 26659 (male, 670 mm TL, 294 mm BDL), Okinawa Trough, East China Sea, 30°1.8ʹN, 128°21.9ʹE, 900 m depth, F/V Yuryo-maru No. 8, sta. T-16-1, bottom trawl, coll. by Y. Kinoshita and S. Hagino, 3 Feb. 1978; BSKU 49467 (female, 860 mm TL, 354 mm BDL), BSKU 49556 (female, 571 mm TL, 257 mm BDL), BSKU 49557 (female, 546 mm TL, 259 mm BDL), BSKU 49558 (female, 659 mm TL, 260 mm BDL), BSKU 49559 (female, 620 mm TL, 254 mm BDL), BSKU 49560 (female, 651 mm TL, 256 mm BDL), BSKU 49561 (female, 951 mm TL, 385 mm BDL), BSKU 49562 (female, 563 mm TL, 282 mm BDL), BSKU 49563 (female, 666 mm TL, 265 mm BDL), BSKU 49564 (female, 473 mm TL, 223 mm BDL), collected with BSKU 49576 and BSKU 49396. In addition, the lectotype of H. raleighana (USNM 35520) was briefly examined based on photographs (Fig. 1d–e).

Table 1 Morphometric comparison between two species of Harriotta
Fig. 1
figure1

Type specimens of two species of Harriotta. a Paralectotype of H. raleighana, USNM 38200, ca. 500 mm TL; b, de lectotype of H. raleighana, USNM 35520, ca. 100 mm TL; c holotype of Anteliochimaera chaetirhampha, ZMUT 2155, 800 mm TL. ab and c reproduced from Goode and Bean (1895: pl. XIX, figs. 1, 3) and Tanaka (1909: pl. I) respectively; de photographed by K. Murasaki

Video footage capturing in situ individuals of Japanese Harriotta are deposited in the JAMSTEC E-library of Deep-sea Images (J-EDI; JAMSTEC 2019). These records were obtained from a series of investigations using submersibles operated by the Japan Agency for Marine-Earth Science and Technology (JAMSTEC); their accession IDs within the database (J-EDI ID), full locality information, and species and behavior observed in each record are summarized in Electronic Supplementary Material (ESM) Table S1. Photographs available in the database were not used in this study because most individuals occurring in the photographs also appeared in the examined video footage, and it was often difficult to determine the individual identity of fish across the two document types. Statistical analysis was performed using the R 3.2.1 software package (R Development Core Team 2015).

The datasets generated during and/or analyzed during the current study are partly included in this published article (ESM Table S1); others are available from the corresponding author on reasonable request.

Results and discussion

Synonymy of two species ofHarriotta. A review of the literature shed light on an important taxonomic problem regarding the two species of Harriotta. Goode and Bean (1895) originally described H. raleighana based on four specimens collected from the northwestern Atlantic without a holotype designation, noting “two of them young, and with proportions quite unlike those of the adults”. Their description also depicts a number of differences between the adult and juvenile specimens they examined (see below for detail), with excellent illustrations (Goode and Bean 1895: pl. XIX, figs. 1–4) of an immature male (USNM 38200, ca. 500 mm TL; Fig. 1a) and a small juvenile (USNM 35520, ca. 100 mm TL; not USNM “25520”, see Jordan and Evermann 1900: 3234; Fig. 1b). Interestingly, Jordan and Evermann (1900: 3234) deemed the juvenile illustrated in the original description (USNM 35520) as “the type” of H. raleighana, and according to ICZN (1999: Art. 74.5), their act is regarded as a lectotype designation for the species (Ebert 2014; Fricke et al. 2019). However, most subsequent authors, including Karrer (1972) who described H. haeckeli, overlooked Jordan and Evermann’s (1900) treatment, assuming the adult (paralectotype) illustrated by Goode and Bean (1895) to be a typical specimen of H. raleighana.

The issue of discussion is whether the small lectotype is conspecific with the large paralectotype. Judging from the description and figures given by Goode and Bean (1895), the lectotype of H. raleighana represents a small individual of what many authors recently referred to as H. haeckeli, especially in having the following characters: broadly rounded pectoral and pelvic fins (vs. bluntly pointed in typical specimens of “H. raleighana”, including the large paralectotype USNM 38200); a narrow interspace between the second dorsal and caudal fins (vs. broad interspace); a poorly developed caudal filament (vs. long and whip-like); and a well-developed upper lobe of the caudal fin (vs. relatively poorly developed), with its height being slightly higher (vs. lower) than the depth of the lower lobe, its base length being longer (vs. shorter) than that of the second dorsal fin, and its origin located distinctly anterior (vs. slightly posterior) to that of the lower lobe (Fig. 1a–b). Furthermore, Karrer (1972: 212), who considered the lectotype as “the smallest syntype”, also recognized that the specimen “must be regarded as belonging to H. haeckeli” generally on the basis of the aforementioned features. Unfortunately, the lectotype of H. raleighana is in bad condition, with the head and body deteriorated into several parts (Fig. 1d–e; see also Karrer 1972: 212), which made it impossible to reconfirm the species’ diagnostic features.

The small size and poor condition of the lectotype of H. raleighana, combined with the paucity of comparable-sized specimens of “H. haeckeli”, make it difficult to provide a definitive conclusion on their conspecificity. Nevertheless, there is little doubt that the two names represent the same species as discussed above, and H. haeckeli is thereby regarded as a junior synonym of H. raleighana in this study. Consequently, Anteliochimaera chaetirhampha Tanaka 1909, previously (and mistakenly) considered the oldest synonym of “H. raleighana”, is resurrected here as a valid species. Although this species was originally described as a representative of a new genus, it was subsequently transferred to Harriotta by Bean and Weed (1910), and then synonymized with “H. raleighana” by Fowler (1941: 505). As pointed out by Karrer (1972: 209), the original description of A. chaetirhampha given by Tanaka (1909) agrees well with the morphology of what many authors have called “H. raleighana” (i.e., USNM 38200, paralectotype of the latter species) (Fig. 1a, c). According to Kazuo Sakamoto of the University Museum, the University of Tokyo (pers. comm. to NN on 28 January 2019), the holotype of the former (ZMUT 2155, 800 mm TL) has unfortunately been lost.

Occurrence ofH. raleighanain the northwestern Pacific. General features of the two species of Harriotta are best seen in Fig. 2. Their morphometric features are summarized in Table 1. The two Japanese specimens collected from Hyuga-nada were identified as revised H. raleighana, as they exhibited the following diagnostic features of the species given by previous authors (as H. haeckeli: Karrer 1972; Last and Stevens 2009; Didier et al. 2012): eye small, its length 7% BDL (vs. 7–9% in the H. chaetirhampha specimens examined); interorbital space broad, 11–16% BDL (vs. 6–9%; Fig. 3c–d); snout tip smooth (vs. armed with small knob-like projections; only prominent in male); first dorsal fin low, length of dorsal spine anterior margin 16% BDL (vs. 19–24%); pectoral and pelvic fins broadly rounded (vs. bluntly pointed; Fig. 3g–j); interdorsal space narrow, 4.5–8.4% BDL (vs. 24.8–26.8%); length of caudal dorsal margin (CDM) longer (vs. shorter) than that of caudal ventral margin, CDM 74–79% BDL (vs. 49–62%); length of caudal upper ray (CUR) longer (vs. shorter) than that of lower ray, CUR 10–11% BDL (vs. 4–5%); infraorbital canal strongly curved anterior to eye, forming S-shaped loop (vs. only gently curved). Previous Japanese records of the species (e.g. Nakaya 1982, 1988; Nakabo et al. 2013) should be referred to as H. chaetirhampha (see discussion in the former section). The occurrence of H. raleighana in the North Pacific off Japan extends its known range approximately 8000 km northward from Australia. It brings the total number of Japanese rhinochimaerids to four (Nakabo et al. 2013).

Fig. 2
figure2

Two species of Harriotta collected from Hyuga-nada off Miyazaki, Kyushu, Japan, at a depth of 1481 m. aHarriotta raleighana, BSKU 49576, male, 501 mm TL, 186 mm BDL and bH. chaetirhampha, BSKU 49467, female, 860 mm TL, 354 mm BDL. Lateral views of fresh specimens

Fig. 3
figure3

Two species of Harriotta. a, c, e, g, i, m, m′, m″, m‴, o, q, q′, sHarriotta raleighana, BSKU 49576, male, 501 mm TL, 186 mm BDL; b, d, f, h, j, l, n, n′, n″, n‴, p, r, r′, tH. chaetirhampha, BSKU 26659, male, 670 mm TL, 294 mm BDL; ab dorsal views of snout tip; cd dorsal and ef ventral views of head; gh and ij outer views of pectoral fin; ij outer views of pelvic fin; kl ventral views of trunk; mn mesial, m′–n′ dorsal, m″–n″ ventral, and m‴–n‴ lateral views of tip of right clasper; op lateral views of frontal tenacula; qr posterior and q′–r′ anterior views of pelvic tenacula; st posteroventral views of anus (white and black arrows indicate the position of the anus and abdominal pores respectively)

The new standard Japanese name, Yomino-tsukai, is proposed here for H. raleighana based on the specimen BSKU 49576 (Fig. 2a). The name Azuma-ginzame, which Jordan et al. (1913: 33) originally proposed for H. chaetirhampha and was formerly used for what many authors called H. raleighana, is applied again to the former species.

Secondary sexual characteristics. One of the specimens examined represents the first mature male specimen of H. raleighana (Fig. 2a), allowing documentation of previously unknown secondary sexual characteristics of the species. Our examination confirmed that H. raleighana is further distinguished from its only congener, H. chaetirhampha, by morphology of the clasper, and frontal and prepelvic tenacula.

Three striking differences were found in the clasper. First, H. raleighana had distinctly longer and thicker claspers compared with H. chaetirhampha (its outer length 25 vs. 16% BDL; its base width 3 vs 1% BDL; Fig. 3k–l). The large values of the former species appear to be significant, considering the smaller size of the specimen examined (501 mm TL in H. raleighana vs. 670 mm TL in H. chaetirhampha) and that the character is secondary sexually dimorphic. The second feature concerns the shape and spinulation of the distal knob of the clasper. In H. raleighana, the tip of the clasper was excessively inflated so as to form a large, elongate, fleshy knob (Fig. 3k); it was covered with 16 (17 in right side) small, multificated, hemp-leaf shaped spines, most of which were serially arranged along its dorsomesial margin (Fig. 3m, m′, m″, m‴). By contrast, the knob of H. chaetirhampha was a small bulb, on which several simple spines were only sparsely distributed (Fig. 3n, n′, n″, n‴). The third feature concerns the development of the slit along the clasper. In H. raleighana, a deep slit run longitudinally from the dorsolateral base of the rod to the ventromesial surface of the knob, running along the dorsal side of the clasper; the clasper of H. chaetirhampha lacked the prominent slit.

The frontal tenaculum of H. raleighana was also proportionally longer and thicker than that of H. chaetirhampha (its length 12 vs. 5% BDL; its base width 4 vs. 1% BDL). Furthermore, the tenaculum of the former species was only gradually arched from its base to the distal end when viewed laterally (Fig. 3o), (vs. strongly angulated near the base; Fig. 3p). In both species, the mesial surface of the tenaculum was heavily covered with small spines, although each spine was hemp-leaf shaped in H. raleighana but simple and slender in H. chaetirhampha. Also, the spinulated area of the former species was confined to about the anterior one-third of the tenaculum length (Fig. 3o) (vs. mesial surface almost fully spinulated; Fig. 3p). However, Last and Stevens’ (2009: 503) figure of the frontal tenaculum of H. chaetirhampha agreed well with that of the H. raleighana specimen examined, and additional study is needed to verify the difference.

The morphology of the prepelvic tenaculum was only slightly different. In both species, the tenaculum was a small flap armed along its posterolateral edge with four strong spines (Fig. 3q–r′), but that of H. raleighana was proportionally larger compared with H. chaetirhampha (its length 6 vs. 4%; its distal width 5 vs. 3% BDL).

Males of the two species also differ from each other in the presence/absence of a pair of prominent pores (= excretory pores; sensu Lombardi 1998) between the inner bases of the claspers, although it is uncertain whether the character is secondary sexually dimorphic. The pores were completely closed in H. raleighana but well developed in H. chaetirhampha (Fig. 3s–t).

The pronounced differences highlighted above, especially those of the clasper, may indicate that the two species belong to their own genera. A more in-depth study especially based on both morphological and molecular analyses will evaluate their generic status, but is beyond the scope of this paper.

The discovery of the mature male specimen of H. raleighana also revealed a smaller size at maturity of this species. Finucci et al. (2017: 79), who investigated reproductive biology of H. chaetirhampha (as H. raleighana) in New Zealand waters, reported that the mature males they examined (n = 67) ranged from 602 to 796 mm CL, with a mean size of 686 mm CL. By contrast, the H. raleighana male examined was 464 mm CL, being distinctively smaller than the minimum size at maturity in the male H. chaetirhampha. While this suggests that the two species exhibit different reproductive strategies, additional investigation of the differences should be conducted when more male specimens of H. raleighana become available.

In situ observations. The J-EDI database (JAMSTEC 2019) included 232 videos capturing in situ individuals of rhinochimaerids; of these, 137 records contained 121 individuals identified as species of Harriotta by having a prominent upper lobe of the caudal fin (vs. poorly developed in Rhinochimaera) and in lacking an anal fin (vs. present in Neoharriotta). Furthermore, 34 individuals (in 43 records) were identified as H. raleighana (Fig. 4; ESM Table S1) by having a broadly rounded pectoral fin (vs. bluntly pointed in H. chaetirhampha), a well-developed upper lobe of the caudal fin (vs. rather low), and a short caudal filament (vs. long and whip-like). The other diagnostic features mentioned in the former sections were often difficult to determine from the video footage, and, therefore, considered not useful for in situ species identification. While 71 individuals (in 78 records) were identified as H. chaetirhampha, the remaining 16 individuals (in 16 records) were not identified to species level with certainty. Although species identification based on in situ observations may be problematic in most deep-sea organisms (Hoving and Robison 2016), it was possible in most cases with Harriotta, as the genus includes only two species, both of which display distinctive external features as characterized above. In addition, an in situ individual previously reported as Harriotta sp. by Senou (2012: fig. 39.1) was reidentified here as H. raleighana, based on a reexamination of its original record (J-EDI ID: 2K0652IN0143Hp05-01).

Fig. 4
figure4

Radical photo sequences showing in situ behavior of Harriotta. a Hovering behavior of H. raleighana (10.0 sec.; J-EDI ID: 6K0588C2SV408_00140500_00144700), Kumano-nada, 2001–2003 m; b fast-swimming behavior of H. raleighana (2.5 sec.; J-EDI ID: KAIKO0402TV2SV1016_00361200_00364300), Kumano-nada, 2057 m; c fast-swimming behavior of H. chaetirhampha (2.5 sec.; J-EDI ID: 3K0549SHDB402_00052100_00053200), Sagami Bay, 1123 m

It was surprising that many in situ individuals of H. raleighana occurred in the northwestern Pacific off Japan, considering that the species is poorly represented in Japanese museum collections. The paucity of specimens is attributable to the deeper occurrence of the species (1400–2600 m; Last and Stevens 2009). The in situ individuals observed here occurred between 1535 and 2611 m (n = 34), where a limited number of trawl hauls were previously conducted. Furthermore, the range in the study area was much deeper than, and according to a Mann-Whitney U test (P < 0.001; based on the shallowest data of each observation) significantly different to that of H. chaetirhampha (vs. 906–1654 m; n = 71). The bathymetric zonation strongly suggests that the two species occupy different niches in the northwestern Pacific with a narrow sympatric zone at depths around 1600 m. The two museum specimens of H. raleighana reported here were collected together with 10 specimens of H. chaetirhampha at 1481 m depth, which implies their apparent sympatric occurrence in southern Japan. Stehmann and Bürkel (1984) also reported a similar distribution pattern in the northeastern Atlantic: 1800–2600 m in the former (as H. haeckeli) vs. 360–2000 m in the latter (as H. raleighana). According to Last and Stevens (2009), the two species are wholly allopatric in Australian waters, with their depth ranges vertically separated by a 400 m gap (1480–1950 m vs. 350–1080 m, mainly 700–900 m). However, Weigmann (2016) summarized the global depth distribution of the two species as 1114–2603 m and 350–2600 m respectively, and it needs to be confirmed whether the two species show bathymetric zonation in various parts of their range.

In our observations, in situ individuals of Harriotta were almost exclusively confined to demersal and benthopelagic habitats, suggesting their close association with the seafloor. They usually hovered or swam above muddy bottoms, sometimes swimming actively against the current (ESM Table S1). In H. raleighana, the large pectoral fins were used when hovering (Fig. 4a); whereas when swimming fast (especially to escape from submersibles), the pectoral fins were firmly adpressed against the body, and the caudal area undulated strongly (Fig. 4b). While H. chaetirhampha also showed similar behavior, the orientation of the caudal area was different when swimming fast: in H. chaetirhampha, the lower lobe of the caudal fin is much deeper than the upper lobe, so the caudal area became slightly upturned during the tail beat (Fig. 4c). The dorsal upturn is presumably due to lift forces generated by an asymmetrical thrust, which is commonly found in heterocercal fishes (Patterson 1968; Gosline 1971; Lauder 2000). The nearly symmetrical tail of H. raleighana is likely more effective to produce thrust than the heterocercal tail of H. chaetirhampha. Although continuous fast-swimming behavior was observed in both H. raleighana (e.g. J-EDI ID: 6K0616C2DV406_00080400_00081700) and H. chaetirhampha (e.g. J-EDI ID: 3K0549SHDB402_00052100_00053200), it was impossible to compare their swimming speed on the basis of limited and unstandardized footage. To our knowledge, this study is the first to discuss in situ behavior of the genus.

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Acknowledgments

We are grateful to D. A. Didier (Millersville University, Millersville) for sharing her knowledge on rhinochimaerid taxonomy, S. Tanaka (Tokai University, Shizuoka) for providing valuable comments on this study, and K. Sakamoto (ZMUT) for his curatorial assistance; K. Murasaki (Tokai University, Shizuoka) kindly provided photographs of the lectotype of H. raleighana. We also thank Y. Toyoda (JAMSTEC, Yokohama) for helping us to access the high-resolution footage examined here, and G. Yearsley (Hobart) for editing the English text. This study was supported by JSPS KAKENHI Grant Number JP18K14509.

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Correspondence to Naohide Nakayama.

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Nakayama, N., Matsunuma, M. & Endo, H. A preliminary review and in situ observations of the spookfish genus Harriotta (Holocephali: Rhinochimaeridae). Ichthyol Res 67, 82–91 (2020). https://doi.org/10.1007/s10228-019-00703-y

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Keywords

  • Chimaeriformes
  • Synonymy
  • Range extension
  • Secondary sexual characteristics
  • Bathymetric zonation
  • Japan