Description of a Pelagic Juvenile of the Poorly Known Anglerfish Sladenia Zhui (Lophiidae) from the East China Sea

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Species Diversity 25: 107–116 Published online 15 May 2020 DOI: 10.12782/specdiv.25.107

Description of a Pelagic Juvenile of the Poorly Known Anglerfish Sladenia zhui (Lophiidae) from the East China Sea

Mizuki Matsunuma1,3 and Nozomu Muto2 1 Department of Environmental Management, Faculty of Agriculture, Kindai University, 3327-204 Nakamachi, Nara 631-8505, Japan E-mail: [email protected] 2 Department of Marine Biology and Sciences, School of Biological Sciences, Tokai University, 5-1-1-1 Minamisawa, Minami-ku, Sapporo, Hokkaido 005-8601, Japan 3 Corresponding author (Received 24 September 2019; Accepted 11 March 2020)

A single pelagic juvenile (23.1 mm standard length) of a lophiid fish, collected from 100–115 m in depth in the East China Sea, was identified as Sladenia zhui Ni, Wu, and Li, 2002, originally described from the East and South China Seas, on the basis of meristic counts [I-I-I-I, 10 dorsal-fin rays (2 post-cephalic spines); 7 anal-fin rays; and 19 pectoral-fin rays] and mitochondrial DNA sequences. Reported here for the first time, juveniles ofSladenia Regan, 1908 are uniquely characterized by inflated, balloon-like skin surrounding the head and body, and undeveloped head spines. The Japanese names “Daruma-ankou-zoku” and “Daruma-ankou” are proposed herein for the genus Sladenia and S. zhui, respectively. Key Words: Lophiiformes, morphology, diagnosis, mitochondrial DNA, Japan.

to date. Introduction A single pelagic lophiiform juvenile (23.1 mm standard length; Fig. 1A), encased in an inflated transparent skin, col- The poorly known deep water lophiid genus Sladenia lected by bottom trawl from the East China Sea in the vi- Regan, 1908 is characterized by a rounded, rather than de- cinity of the type locality of S. zhui, was identified as that pressed, head, and compressed, rather than depressed, tail; species. Because no pelagic juvenile of any Sladenia species the nasal sacs which are not constricted at the base; very have ever been reported, the present specimen is described long pseudobranchia; humeral, subopercular, quadrate, pa- in detail. rietal and articular spines absent; epiotic and interopercular spines which are low and rounded; vomerine teeth larger than palatine teeth; the illicial bone and 2nd dorsal-fin spine Materials and Methods inserted very close together on the illicial pterygiophores; the 3rd or 3rd and 4th (post-cephalic) dorsal-fin spines Counts and measurements followed Caruso and Bullis lying under the skin; and a smooth ridge on the frontal (1976), Caruso (1981) and Ho et al. (2016). The terminol- bones anterior to the eye and lateral to the illicial pterygi- ogy of head spines followed Caruso (1981: fig. 1). Osteologi- ophore (see Caruso and Bullis 1976; Caruso 1985). The cal characters were observed from an X-ray photograph of genus comprises four nominal species, all being valid, viz., the specimen, which was judged as being a pelagic juvenile Sladenia gardineri Regan, 1908 (type species; distribution: due to its apparently full complement in number of fin rays Salomon Atoll, Chagos Archipelago, central Indian Ocean), and putative specializations for a pelagic lifestyle (inflated Sladenia remiger Smith and Radcliffe in Radcliffe, 1912 [Su- skin and elongate pelvic-fin rays), following Leis and Trnski lawesi (Indonesia), Australia, New Caledonia, and the Ha- (1989) and Okiyama (2014a). waiian Islands], Sladenia shaefersi Caruso and Bullis, 1976 Standard length is abbreviated as SL. Specimens exam- (Western Atlantic Ocean), and Sladenia zhui Ni, Wu, and ined were deposited in the fish collections of Kyoto Univer- Li, 2012 [South and East China Seas and Java (Indonesia)] sity, Kyoto and Maizuru, Japan (FAKU), the Hokkaido Uni- (Caruso and Bullis 1976; Pietsch et al. 2013; Ho 2015; Ho versity Museum, Hakodate, Japan (HUMZ), the Kagoshima et al. 2016). Although Pietsch et al. (2013) recently provided University Museum, Kagoshima, Japan (KAUM), and Kin- in-situ submersible and ROV observations of S. shaefersi, dai University, Nara, Japan (KUN). the species of this poorly known genus are generally known The present juvenile specimen and a single adult speci- only from a few specimens. Among them, S. zhui was origi- men (HUMZ 191110) of S. cf. zhui (sensu Ho et al. 2016) nally described from four specimens from the South and were subjected to genetic analysis. Total genomic DNA was East China Seas (Ni et al. 2012), the subsequent report by extracted from either a fin clip or muscle tissue sample pre- Ho et al. (2016) of two specimens collected off Java, Indone- served in 99.5% ethanol, using the Wizard Genomic DNA sia (as S. cf. zhui) being the most recently published record Purification Kit (Promega), following the manufacturer’s

Fig. 1. Fresh (A) and preserved (B–D) juvenile specimen of Sladenia zhui, KAUM–I. 70329, 23.1 mm SL, East China Sea in lateral (A, B), dorsal (C) and ventral (D) views. Right side reversed in B. protocol. Partial sequences of three mitochondrial genes Cycle Sequencing Kit v3.1 (Thermo Fisher Scientific) on an obtained from the juvenile specimen included the 5′ end Applied Biosystems 3500 Genetic Analyzer (Thermo Fisher of the Cytochrome c Oxidase subunit I (COI: 648 bp), 12S Scientific). The resulting sequences were edited with BioEdit ribosomal RNA (12S: two separate regions of 181 bp and v7.0.5.3 (Hall 1999) and deposited in the International Nu- 403 bp), and 16S ribosomal RNA (16S: 566 bp). Only the cleotide Sequence Database Collaboration under accession 12S sequence was obtained for HUMZ 191110. Primers for numbers LC499995 to LC500000. each gene were: VF2_t1, FishF2_t1, FishR2_t1 and FR1d_t1 The phylogenetic position of the present juvenile speci- for COI (Ivanova et al. 2007); MiFish-U-F and MiFish-U-R men within Lophiiformes was estimated by Bayesian in- for the 181 bp fragment of 12S (Miya et al. 2015); 12SA-L ference (BI), based on the 12S, 16S and COI sequences. and 12SB-H for the 403 bp fragment of 12S (Palumbi et Sequences from the former were aligned with reference se- al. 2002); and 16Sar and 16Sbr for 16S (Palumbi 1996). quences of lophiiform species, comprising complete mito- PCR was conducted in an 8.0 µl reaction volume contain- chondrial genome sequences of 39 species, representing 15 ing 4.0 µl of 2X KAPATaq HS ReadyMix with dye (KAPA families and five suborders (Table 1). The latter, originally BIOSYSTEMS), 0.20 µM of each primer, and 1.0 µl (approxi- reported by several authors (Miya et al. 2003; Yamanoue mately 20 ng) of template DNA. PCR profiles followed those et al. 2007; Miya et al. 2010), was analyzed by Miya et al. previously described (Palumbi 1996; Palumbi et al. 2002; (2010), who inferred the phylogenetic history of the order. Ivanova et al. 2007; Miya et al. 2015). PCR products were In addition, a sequence of Capros aper (Linnaeus, 1758) purified with ExoSAP-IT (Thermo Fisher Scientific), and (Perciformes: Caproidae) was used as an outgroup, follow- DNA sequencing performed using the Big-Dye Terminator ing Miya et al. (2010). Alignment was done separately for Pelagic juvenile of Sladenia zhui 109

Table 1. International Nucleotide Sequence Database Collaboration (INSDC) accession numbers of mitochondrial genome sequences, used as references in this study. Classifications follow Miya et al. (2010).

Suborder/Family Species INSDC Accession No. Suborder Lophioidei Lophiidae Lophius americanus AP004414 Lophiodes caulinaris AB282826 Lophiomus setigerus AP004413 Sladenia gardineri AB282827 Suborder Antennarioidei Antennariidae Antennarius coccineus AB282830 Antennarius striatus AB282828 Histrio histrio AB282829 Tetrabrachiidae Tetrabrachium ocellatum AB282831 Brachionichthyidae Brachionichthys hirsutus AB282832 Chaunacidae Chaunax abei AP004415 Chaunax penicillatus* AP004416 Chaunax pictus AB282833 Suborder Ogcocephaloidei Ogcocephalidae Coelophrys brevicaudata AB282834 Halieutaea stellata AP005977 Malthopsis jordani AP005978 Zalieutes elater AB282835 Suborder Ceratioidei Caulophrynidae Caulophryne jordani AP004417 Caulophryne pelagica AB282836 Neoceratiidae Neoceratias spinifer AB282837 Melanocetidae Melanocetus johnsonii AB282838 Melanocetus murrayi AP004418 Himantolophidae Himantolophus albinares AB282839 Himantolophus groenlandicus AB282840 Diceratiidae Bufoceratias thele AB282841 Diceratias pileatus AB282842 Oneirodidae Bertella idiomorpha AB282846 Chaenophryne melanorhabdus AB282845 Oneirodes thompsoni AB282843 Puck pinnata AB282844 Thaumatichthyidae Lasiognathus sp. AB282848 Thaumatichthys pagidostomus AB282847 Centrophrynidae Centrophryne spinulosa AB282849 Ceratiidae Ceratias uranoscopus AB282851 Cryptopsaras couesii AB282850 Gigantactinidae Gigantactis vanhoeffeni AB282852 Rhynchactis macrothrix AB282853 Linophrynidae Linophryne bicornis AB282854 Acentrophryne dolichonema AB282855 Haplophryne mollis AB282856 *Reported as Chaunax tosaensis Okamura and Oryu, 1984 by Miya et al. (2010), subsequently synonymized under Chaunax penicillatus McCull- och, 1915 (see Ho et al. 2013). each gene using Clustal W (Larkin et al. 2007) implemented tution model at each partition, GTR+Γ for 12S and the 3rd in BioEdit. Poorly-aligned sites were removed using trimAl codon of COI, SYM+Γ for 16S and the 1st codon of COI, with the ‘automated1’ option (Capella-Gutiérrez et al. 2009). and F81+Γ for the 2nd codon of COI, were selected. As- Optimal substitution models for a concatenated alignment suming these substitution models, BI was conducted using of the 3 genes were inferred using Kakusan4 (Tanabe 2011), MrBayes v3.2.4 (Ronquist et al. 2012). Two independent with the alignment partitioned by gene and codon positions. runs of four Markov chain Monte Carlo (MCMC) chains of Following the Bayesian Information Criterion, the “Pro- 1,000,000 generations were conducted, trees being sampled portional_CodonProportional” model was selected for rate every 100 generations. Trees from the first 10% of MCMC heterogeneity among partitions, which assumed that branch chains were discarded as burn-in. Tracer v1.7 (Rambaut et lengths were proportional among partitions. For the substi- al. 2018) was used to ensure that the chains had reached 110 M. Matsunuma and N. Muto convergence. Trees from the two MCMC runs were sum- 127°01′E). marized by the ‘sumt’ option of MrBayes to construct a ma- Sladenia cf. zhui: Ho et al. 2016: 78, fig. 1 (off Java, Indone- jority-rule consensus tree, which was then visualized with sia; description). FigTree v1.4.3 (Rambaut 2016). Specimen examined. KAUM–I. 70329, 23.1 mm SL, The relationship between the present juvenile and S. cf. East China Sea, 28°45′39″N, 125°44′53″E–28°41′08″N, zhui (sensu Ho et al. 2016) specimens was then inferred 125°45′07″E, 100–115 m depth, bottom trawl, 13 December with respect to four other Lophioidei species, based on a re- 2014. duced dataset comprising 12S sequences. BI was conducted Description. Morphometrics and selected meristics (as outlined above) using Centrophryne spinulosa Regan and shown in Table 2. Pelvic fin with 1 spine (embedded under Trewavas, 1932 (Lophiiformes: Centrophrynidae) as an out- skin) and 5 soft rays. Vertebrae 12+7=19. Body rounded, group (Miya et al. 2010). moderately compressed anteriorly, more compressed pos- teriorly. Head and body encased in inflated (balloon-like) Genus Sladenia Regan, 1908 smooth transparent skin (Figs 1, 2). Gill opening small, [New Japanese name: Daruma-ankou-zoku] below pectoral-fin base, not extending in front of base. Sladenia zhui Ni, Wu, and Li, 2012 Dorsal edge of orbit rim slightly expanded dorsolaterally [New standard Japanese name: Daruma-ankou] with blunt tip; head surface smooth without other spines or (Figs 1–3, 5; Table 2) ridges. Mouth relatively large, its width 28.4% of SL; lower jaw slightly extended beyond upper jaw anteriorly; poste- Sladenia remiger non Smith and Radcliffe in Radcliffe, 1912: rior margin of maxilla anterior to vertical through anterior Ni 1988: 317, fig. 250 (East China Sea; description). margin of eye. Papilliform nasal sacs above upper jaw. Teeth Sladenia gardineri non Regan, 1908: Su 2002: 351, fig. 163 conical, enlarged and well pointed; premaxilla with single (South and East China Seas; description). low of 4 teeth; teeth on maxilla slightly smaller, in a single Sladenia zhui Ni, Wu, and Li, 2012: 211, figs 1–3 (type lo- row; teeth on lower jaw forming ca. 2 irregular rows, inner cality: East China Sea, 28°09′N, 126°58′E–28°14′N, row teeth slightly larger than outer teeth; vomer with 2 dis-

Table 2. Meristic and morphometric data from specimens of Sladenia zhui (expressed as percentages of SL).

KAUM–I. 70329 HUMZ 191110 HUMZ 191516 Localities East China Sea off Java, Indonesia Dorsal-fin spines 4 4 4 Dorsal-fin soft rays 10 9 9 Anal-fin soft rays 7 6 6 Pectoral-fin rays 19 18 18 Pelvic-fin rays I, 5 I, 5 I, 5 Caudal-fin rays 8 9 9 SL (mm) 23.1 271.5 278.2 Head length (% SL) — 33.6 32.5 Head width — — 132.5 Head depth — 31.4 34.4 Pre-dorsal fin length — 62.7 56.1 Illicial length 86.5* 36.0 38.3 2nd dorsal-fin spine length — 20.2 16.6 Pre-preopercle length — 31.5 29.1 Snout length 12.5 18.3 19.1 Snout width — 8.8 8.6 Eye diameter 7.5 5.9 5.3 Upper jaw length 21.1 29.2 28.0 Inter-palatine width — 12.8 13.8 Inter-frontal width — 10.2 10.0 Inter-sphenotic width — 16.3 17.8 Inter-pterotic width — 24.1 25.4 Inter-opercular width — 32.4 31.6 Length between pterotic and sphenotic spines — 8.6 8.6 Length between upper palatine and quadrate spines — 25.6 26.3 Caudal peduncle depth — 13.2 13.6 Tail length — 27.1 31.5 Caudal fin length 71.3* 30.5 32.9 *slightly damaged. Pelagic juvenile of Sladenia zhui 111 crete, elongate teeth patches laterally; palatine without teeth; (Fig. 1A), becoming semi-transparent after preserva- tongue without teeth, covered with numerous papillae. Eye tion (Figs 1B–D, 2), entirely covered with numerous min- moderately large, directed laterally and slightly dorsally. In- ute brown melanophores. Inner surface of head and body terorbital space narrow. brownish, entirely covered with numerous stellate brown Base of illicial bone (tip broken) in interorbital space melanophores. Eye dark blue. Illicial and 2nd dorsal-fin between anterior margins of eyes. Second dorsal-fin spine spine semi-transparent, with scattered minute brown mela- thin, very long, its length 86.5% of SL (tip broken); spine nophores. Dorsal-fin soft-rayed portion and anal fin semi- base at mid-orbit level, close to illicial base (Fig. 3A). Two transparent, with dense melanophores on membranes. post-cephalic dorsal-fin spines embedded under skin (de- Pectoral fin base with scattered minute brown melano- termined from X-ray photograph); well separated from each phores; rays with few scattered melanophores, membranes other and dorsal-fin soft-rayed portion. Dorsal-fin soft- semi-transparent without melanophores. Pelvic fin semi- rayed portion relatively large, with semi-truncate profile; all transparent, with minute brown melanophores scattered rays unbranched. Anal fin without spines, semi-truncate; all on membranes along rays; filamentous portion of pelvic-fin soft rays unbranched; fin base shorter than that of dorsal-fin ray partially brownish. Caudal fin semi-transparent covered soft-rayed portion. Caudal fin very long, its length 71.3% of with minute brown melanophores on basal portion; minute SL (slightly broken); all rays unbranched. Pectoral fin rela- melanophores densely covered with membranes along rays. tively small, fan-shaped, set laterally; all rays unbranched. Distribution. The species has been collected from the Pelvic fin relatively small, with elongate filamentous soft rays central East China Sea, northern South China Sea (east of [3rd ray of right fin only retained (tip broken; other rays Hainan Island) and Indonesia (off Java) (Ni et al. 2012; Ho broken near base), its length 55.9% of SL; Fig. 3B]. et al. 2016; this study) (Fig. 4). Two Indonesian specimens, Coloration. Transparent skin encasing body when fresh reported by Ho et al. (2016) as S. cf. zhui, were identified herein as S. zhui (see below). Adults of the species were collected in depths of 655–979 m (Ni et al. 2012; Ho et al. 2016), whereas the present juvenile specimen was collected on the continental shelf (100–115 m depth), suggesting that the pelagic juvenile of the species have a shallower bathy- metric distribution before settlement. Identification. The present juvenile specimen was as- signed to Lophiidae, differing from currently known larvae and juveniles of other lophiiform families by having 4 dorsal-fin spines (3 in Antennariidae), smooth body skin (covered with spinules in Chaunacidae and Ogcocephalidae), and developed pelvic fins [absent in ceratioid families, ex- cept for Caulophryne Goode and Bean, 1896 (Caulophryni- dae)] (see Pietsch 1984; Bertelsen 1984; Pietsch 2009; Oki- yama 2014b). Among lophiid genera, the specimen conformed to Slad- enia in both meristic counts, and having a rounded head Fig. 2. Preserved juvenile specimen of Sladenia zhui, KAUM–I. and body, and undeveloped head spines (Table 3), compared 70329, 23.1 mm SL, East China Sea, showing melanophores. Right with larvae and juveniles of other lophiid genera, including side reversed.

Fig. 3. Semi-schematic drawings of illicium (il) and 2nd dorsal-fin spine (sec) (A), and pelvic fin (B) of juvenile specimen of Sladenia zhui, KAUM–I. 70329, 23.1 mm SL, East China Sea. Right side reversed in both drawings. SR indicates soft ray. Note: 2nd–4th soft rays partially damaged. Bars indicate 1 mm. 112 M. Matsunuma and N. Muto

Lophius Linnaeus, 1758, Lophiodes Goode and Bean, 1896 such distinguishing characters were absent in the juvenile and Lophiomus Gill, 1883, generally characterized as having specimen, the genetic similarity between it and a published a moderately depressed head with relatively well developed sequence of S. gardineri (see Genetic analysis), and the dis- spines, and laterally compressed body (Caruso 1983; Everly junct distribution of the two species (S. gardineri, central and Caruso 2003; Okiyama 2014c; Okiyama and Minami Indian Ocean; Table 4), pointed to the former being S. zhui. 2014a, b; this study: Fig. 5). The genetic analysis also sup- Genetic analysis. A Bayesian phylogenetic tree based on ported the generic identification of the present specimen a concatenated alignment of 12S, 16S and COI sequences (see below). (626, 564 and 648 bp, respectively, including gaps) is shown The specimen was further identified as S. zhui, due to in Fig. 6A. Among the 39 lophiiform species subjected having 4 dorsal-fin spines (2 post-cephalic spines), com- to the analysis, S. gardineri was most closely related to the pared with 3 dorsal-fin spines (1 post-cephalic spine) in present specimen, supporting its generic identification. On S. remiger and S. shaefersi (Table 4). Although similar to S. the other hand, the overall tree topology was largely consis- gardineri in meristic counts, Ni et al. (2012) distinguished S. tent with that of Miya et al. (2010), who analyzed the com- zhui from the former due to the wider snout, sturdy blunt plete mitogenome sequences (ca. 16,000 bp) of the same 39 head spines, and uniformly brown body without vermicula- species (each of five suborders being recovered as mono- tions or other contrasting markings in the latter. Although phyletic). Such consistency implied that the present analysis had successfully resolved the phylogenetic relationships among lophiiform species to some extent, despite the lim- ited lengths of the sequences analyzed. A second Bayesian phylogenetic tree based on a reduced dataset [a 598 bp (including gaps) alignment of 12S sequences from six lophioid specimens, including both the present juvenile specimen and HUMZ 191110 (S. cf. zhui sensu Ho et al. 2016)], is shown in Fig. 6B. Notably, the latter two specimens possessed identical sequences, being clearly separated from other tree branches. On this basis, together with their similarity in meristic counts, the present juvenile and S. cf. zhui (sensu Ho et al. 2016) specimens can be safely considered as conspecific. Remarks. Sladenia zhui was originally described by Ni et al. (2012) on the basis of four specimens collected from the northern South China and central East China Seas, the species having previously been reported as S. remiger or S. gardineri by Ni (1988) and Su (2002) (see synonym list). Ho et al. (2016) subsequently reported two specimens collected off Java, Indonesia asC . cf. zhui (Fig. 7C, D), commenting that they differed slightly from the original description of the species, having a narrower snout (mostly due to a differ- ent measurement method). Meristic and morphometric data of the Indonesian specimens are given in Table 2. However, since all congeners are known from only a few specimens of each, intraspecific variations and interspecific differences between them are poorly known (Caruso and Bullis 1976; Fig. 4. Distributional map of Sladenia zhui. Star and open circles Ho 2015). indicate present and previous records, respectively. Larval or juvenile Sladenia specimens have not previous-

Table 3. Selected diagnostic characters of lophiid genera.

Sladenia Lophiodes Lophiomus Lophius 1, 2, 3 2, 4 2, 5, 6 2, 5, 7 Head and body rounded depressed depressed depressed Third cephalic dorsal-fin spine absent present present present Humeral, articular, quadrate and subopercular spines absent present present present Dorsal-fin soft rays 9 or 10 8 7–9 9–12 Anal-fin soft rays 6 or 7 6 or 7 5–7 8–10 Pectoral-fin rays 18 or 19 13–22 20–25 19–28 Vertebrae 19 18 or 19 18 or 19 26–31 1, this study; 2, Caruso (1985); 3, Ni et al. (2012); 4, Caruso (1981); 5, Everly and Caruso (2003); 6, Okiyama and Minami (2014a); 7, Caruso (1983). Pelagic juvenile of Sladenia zhui 113

Fig. 5. Lateral (A) and dorsal (B) views of preserved juvenile specimen of Lophius litulon, FAKU 109453 (1 of 3 specimens), 26.6 mm SL, Japan.

Table 4. Distribution and selected diagnostic characters of Sladenia species.

S. zhui S. gardineri S. remiger S. shaefersi 1, 2, 3 4 4, 5 4, 6, 7 Distribution East and South China Seas Chagos Archipelago Western and Western Atlantic and Indonesia (central Indian Ocean) Central Pacific Size (mm SL) 23.1–525 (n=4) 351 92.3 146.2–397 (n=4) Dorsal-fin spines 4 4 3 3 Post-cephalic dorsal-fin spines 2 2 1 1 Dorsal-fin soft rays 9 or 10 9 9 8 or 9 Anal-fin rays 6 or 7 6 7 6 Pectoral-fin rays 18 or 19 18 19 17 or 18 Vermiculate body pattern absent present absent? present 1, this study; 2, Ni et al. (2012); 3, Ho et al. (2016); 4, Caruso and Bullis (1976); 5, Ho (2015); 6, Prokofiev and Kukuev (2009); 7, Sepúlveda et al. (2013). ly been reported (Richards 1990; Everly and Caruso 2003). Similarly, a Sladenia individual reported by Senou (2012) In his comprehensive work, entitled “An atlas of early stage as “Chaunacidae gen. et sp. 2” from the Mokuyo Seamount fishes in Japan”, Okiyama (2014b) provided keys to larval (Ogasawara Islands) also had a vermiculate pattern. Such stages of the lophiiform suborders, and stated that Ceratioi- body markings have been regarded as a diagnostic feature dei differed from the other suborders by having an inflated, of Sladenia species (Caruso and Bullis 1976; Ni et al. 2012; balloon-like skin surrounding the body, and the pelvic fin Table 4). In-situ images of S. shaefersi in the Gulf of Mexi- absent. The juvenileSladenia specimen also had the former co showed obvious widespread vermiculations on the body feature. In addition, the latter also possessed the following (Pietsch et al. 2013), and the drawing of the 500 mm TL- external adult Sladenia features (Fig. 7C, D): rounded head holotype of S. gardineri also showed maze-like vermicula- and body [depressed in adults of other lophiid genera (Fig. tions on the body (Regan 1908: pl. 32). In contrast, adults of 7A, B)], and absence of distinct humeral, articular, quadrate S. zhui have a uniformly brownish body without vermicu- and subopercular spines (present) (see Caruso 1985). lations (Ni et al. 2012: fig. 1; Ho et al. 2016: fig. 1; Fig. 7C, The fin rays of the present juvenile are considered to D), suggesting that the in-situ images and footage of Slad- reach the full complement in number (Table 2). A difference enia from the Ogasawara Islands were not consistent with S. of the number of caudal-fin rays between the juvenile speci- zhui. Although Caruso and Bullis (1976) stated that S. remi- men (8) and adults (9) is regarded here as an intraspecific ger lacked vermiculations or other contrasting markings, variation. A series of larvae and juvenile examples are neces- as originally described by Smith and Radcliffe in Radcliffe sary to reveal the development of the numbers of fin rays in (1912), an underwater photograph of S. remiger, reported the species. by Chave and Mundy (1994) from the Hawaiian Islands, In-situ observations of Sladenia from seamounts around showed dark vermiculations on a whitish body. Ho (2015) the Ogasawara Islands, Japan, archived in the Japan Agen- reported an underwater photograph of S. cf. remiger from cy for Marine-Earth Science and Technology data base the Kermadec Ridge, with similar vermiculations, suggest- [JAMSTEC E-library of Deep-sea Images (J-EDI)], showed ing that the specimen may have represented an undescribed several Sladenia individuals characterized by vermiculate species. markings on the body (e.g., J-EDI: HPD0747HDTV0088). The new Japanese names “Daruma-ankou-zoku” and 114 M. Matsunuma and N. Muto

“Daruma-ankou” are proposed herein for the genus Slad- enia and S. zhui, respectively, such names being derived Comparative material examined from a combination of the overall rounded body of the species (=daruma), plus the Japanese name for lophiid fishes Lophius litulon (Jordan, 1902): FAKU 109453, 3 speci- (=ankou); “zoku” refers to “genus”. mens, 19.0–26.6 mm SL, Japan (further locality unknown), 1960’s; FAKU 137621, 32.4 mm SL, off Miyazu, Kyoto Pre- fecture, Japan, 8 May 2015; KUN-P 50268, 196.4 mm SL, off Saikazaki, Wakayama Prefecture, Japan, 27 February 2019. Sladenia zhui: HUMZ 191110, 271.5 mm SL, off Java, Indo- nesia, 08°40.3′S, 111°15.5′E–08°45.5′S, 111°14.2′E, 680– 706 m depth, 10 September 2004; HUMZ 191516, 278.2 mm SL, off Java, Indonesia, 08°20.1′S, 109°54.2′E–08°19.3′S, 109°53.3′E, 850–916 m depth, 12 September 2004.

Acknowledgments

We are grateful to H. Motomura (KAUM), Y. Kai (FAKU) and F. Tashiro (HUMZ) for providing an opportunity to ex- amine specimens; N. Nakayama (Tokai University, Shimizu, Japan) for providing information on records of Sladenia in the JAMSTEC archive and helpful comments on this study; A. Ogino (formerly KUN) for taking an X-ray photograph Fig. 6. Bayesian phylogenetic trees of (A) Lophiiformes, based of the juvenile specimen; T. Pietsch (University of Washing- on 1838 bp of concatenated sequences of 12S rRNA, 16S rRNA and ton, Seattle), M. Takami (Tokai University) and anonymous Cytochrome c Oxidase subunit I genes; and (B) Lophioidei, based reviewers for providing helpful comments on the manu- on 598 bp of 12S rRNA gene sequences. Numbers beside nodes script; and G. Hardy (Ngunguru, New Zealand) for reading represent Bayesian posterior probabilities.

Fig. 7. Preserved adult specimens of Lophius litulon (A, B) and Sladenia zhui (C, D) in dorsal (A, C) and lateral (B, D) views. (A, B) KUN-P 50268, 196.4 mm SL, Wakayama Prefecture, Japan; (C, D) HUMZ 191516, 278.2 mm SL, off Java, Indonesia. Pelagic juvenile of Sladenia zhui 115 the manuscript and providing help with English. This study and Iwasaki, W. 2015. MiFish, a set of universal PCR primers for metabarcoding environmental DNA from fishes: detection of was supported in part by the Sumitomo Fund to the 2nd au- more than 230 subtropical marine species. Royal Society Open thor. Science 2: 150088. Miya, M., Takeshima, H., Endo, H., Ishiguro, N. B., Inoue J. G., Mukai, T., Satoh, T. P., Yamaguchi, M., Kawaguchi, A., Mabuchi, K., Shi- References rai, S. M., and Nishida, M. 2003. Major patterns of higher teleos- tean phylogenies: a new perspective based on 100 complete mito- Bertelsen, E. 1984. Ceratioidei: development and relationships. Pp. chondrial DNA sequences. 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