Research Article
Print
Research Article
Seahorses of the Hippocampus coronatus complex: taxonomic revision, and description of Hippocampus haema, a new species from Korea and Japan (Teleostei, Syngnathidae)
expand article infoSang-Yun Han‡, Jin-Koo Kim‡, Yoshiaki Kai§, Hiroshi Senou|
‡ Pukyong National University, Busan, Korea, South
§ Kyoto University, Kyoto, Japan
| Kanagawa Prefectural Museum of Natural History, Kanagawa, Japan

Corresponding author: Jin-Koo Kim ( taengko@hanmail.net )

Academic editor: Sven Kullander
© 2017 Sang-Yun Han, Jin-Koo Kim, Yoshiaki Kai, Hiroshi Senou.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Han S-Y, Kim J-K, Kai Y, Senou H (2017) Seahorses of the Hippocampus coronatus complex: taxonomic revision, and description of Hippocampus haema, a new species from Korea and Japan (Teleostei, Syngnathidae). ZooKeys 712: 113-139. https://doi.org/10.3897/zookeys.712.14955
ZooBank: urn:lsid:zoobank.org:pub:215D1C08-3E19-4865-83E7-40DBF07D353D
Open Access

Abstract

Morphological and molecular analyses were conducted on 182 specimens belonging to the Hippocampus coronatus complex (H. coronatus sensu lato), collected in Korea and Japan 1933–2015, in order to clarify the taxonomic status of the species within this complex. Three species are recognized based on the shape of the coronet, the number of trunk rings (TrR) and tail rings (TaR), and presence or absence of a wing-tip spine (WS) at the dorsal fin base. Hippocampus coronatus Temminck & Schlegel, 1850 (H. coronatus sensu stricto), is diagnosed by 10 TrR, 37–40 TaR, an extremely high coronet (55.7–79.0 % head length) with four tips on the corona flat (CoT), and one WS. Hippocampus sindonis Jordan & Snyder, 1901 is diagnosed by 10 TrR, 35–38 TaR, a moderately high coronet (36.3–55.4 % HL) with five CoT, and no WS. A new species, H. haema is described on the basis of 140 specimens, characterized by 10 TrR, 35–38 TaR, a moderately high coronet (34.1–54.9 % head length) with four CoT, and two WS. Hippocampus haema is only known from the Korea Strait, western Kyushu, and East/Japan Sea. Recognition of the three species is supported by differences in mitochondrial DNA fragments (cytochrome b, 16S rRNA, and 12S rRNA).

Keywords

Genetic distance, morphology, molecular systematics, Pacific Ocean, taxonomy

Introduction

The seahorse genus Hippocampus (Teleostei: Syngnathidae) exhibits a wide range of inter- and intra-specific variation, for example in skin filaments, color, and body proportions. Therefore, taxonomic relationships within Hippocampus have been controversial (Lourie et al. 1999, 2016), and more than 140 species have been named within this genus (Lourie et al. 2016; Eschmeyer et al. 2017). For example, Lourie et al. (2016) reviewed the genus and considered 41 species as valid, while Kuiter (2009) recognized ca. 79 valid species. Six species of Hippocampus have been recorded from Korea and Japan, viz., H. coronatus Temminck & Schlegel, 1850, H. mohnikei Bleeker, 1853, H. histrix Kaup, 1856, H. kuda Bleeker, 1852, H. trimaculatus Leach, 1814, and H. sindonis Jordan & Snyder, 1901. Another two species, H. kelloggi Jordan & Snyder, 1901 and H. bargibanti Whitley, 1970, were only recorded from Japan (Choi et al. 2002; Lourie et al. 2004; Kim et al. 2005; Senou et al. 2006; Kim et al. 2013; Senou 2013; Lourie et al. 2016).

The species (or species group) H. coronatus sensu lato has been defined by possessing ten trunk rings, 34–40 tail rings, a bony armor, double gill openings (Lourie et al. 1999, 2004; Kim et al. 2005; Kuiter 2009; Foster and Gomon 2010; Senou 2013; Lourie 2016), and a tall coronet on the head, which exhibits a wide range of height variation (Jordan and Snyder 1901; Mitani 1956; Lourie et al. 1999, 2004). Some authors have stated that this group includes two species, H. coronatus (sensu stricto), which has an extremely high coronet and a snout length ~2.33 times the head length, and H. sindonis, which has a moderately high coronet and a snout length ~3 times the head length (Jordan and Snyder 1901; Okada and Matsubara 1938; Matsubara 1955; Lourie et al. 1999; Senou 2002; Lourie et al. 2004; Senou 2013), while others considered the variation in coronet height only as intraspecific variation (Mitani 1956; Araga 1984; Senou 1993). Based on variation in mitochondrial DNA (partial 12S rRNA), Mukai et al. (2000) suggested that the H. coronatus complex (H. coronatus sensu lato) consists of two genetically diverged groups.

Although the Korean seahorse (Korean name: Haema) has been identified as H. coronatus (Mori 1928; Chyung 1977; Kim et al. 2001; Kim et al. 2005), the height of its coronet and the number of tail rings appear to agree better with that described for H. sindonis (Jordan and Snyder 1901; Lourie et al. 1999, 2004; Kim et al. 2013; Senou 2013; Han et al. 2014). In fact, H. sindonis has often been confused with H. coronatus (Lourie et al. 1999, 2016), and the height of the coronet in the type series of H. coronatus varies (Boeseman, 1947). These controversies have contributed to the uncertainty about the distribution of H. coronatus in both Korea and Japan, and led to its classification in the Data Deficient (DD) category of the International Union for Conservation of Nature and Natural Resources (IUCN) Red List, as there is a lack of information on population trends (Zhang and Pollom 2016). The present study aims to clarify the taxonomic status of Korean seahorses, redescribing H. coronatus and H. sindonis and describing a new species, all belonging to the H. coronatus complex.

Materials and methods

Material examined

A total of 182 specimens of H. coronatus sensu lato collected from Korean and Japanese waters (Fig. 1) were subjected to morphological analyses. Voucher specimens were deposited in Korea [Department of Marine Biology, Pukyong National University (PKU); National Institute of Biological Resources (NIBR)], Japan [Maizuru Fisheries Research Station, Field Science Education and Research Center, Kyoto University (FAKU); Kagoshima University Museum (KAUM); Kanagawa Prefectural Museum of Natural History (KPM)], Europe [Naturalis Biodiversity Center (RMNH), The Netherlands], and the United States [Smithsonian National Museum of Natural History (USNM)].

Figure 1. 

Distribution of the species within the Hippocampus coronatus complex: H. haema (red circles; the filled red circle indicates the holotype), H. coronatus (green triangles), and H. sindonis (blue squares; the filled blue square indicates the holotype).

Morphological analysis

Procedures used for counts and measurements follow Lourie (2003) and are presented in Fig. 2.

Morphological terms are abbreviated as:

TrR trunk rings

TaR tail rings

DsRTrR and TaR supporting the dorsal fin

D dorsal fin rays

A anal fin rays

P pectoral fin rays

CS cheek spine below the operculum

ES eye spine above the eye

FTrDS first TrR dorsal spine

LTrDS last TrR dorsal spine

WS wing-tip spine: a thick-recurved spine on dorsal fin base as in H. coronatus and H. haema

ACS anterior coronet spine

PCS posterior coronet spine: 5th tip on corona flat

Coa corona: posterior crest of coronet

CoT number of tips on corona flat

Measurements are abbreviated as:

SL standard length

HL head length

CHGO coronet height from gill opening to the median groove on corona (along central depression between 1st and 2nd tip on it)

CHMC coronet height from mid-point of cleithral ring to the median groove on corona

SnL snout length

ED eye diameter

TrL trunk length

TaL tail length

Meristic data were obtained from soft X-rays of the 182 H. coronatus sensu lato specimens. Measurements were obtained using the microscope-integrated Active Measure software (Shinhanoptics, Seoul, Korea). The coronet height was measured as CHMC (Lourie 2003) and CHGO (Temminck and Schlegel 1850; Jordan and Snyder 1901) (Fig. 2) so that our results could be compared to those reported in previous studies (Temminck and Schlegel 1850; Jordan and Snyder 1901; Lourie et al. 1999). Sexual dimorphism analysis was conducted on the 152 adults (80 females and 72 males). These are all the specimens over 53.9 mm, which is the minimum SL at maturation defined for H. coronatus sensu lato (Choi et al. 2006).

Figure 2. 

Meristic and morphometric characters used in Hippocampus analyses following Lourie (2003). Abbreviations: eye spine (ES), cheek spine (CS), anterior coronet spine (ACS), posterior coronet spine (PCS), corona (Coa), dorsal spine of the first trunk ring (FTrRDS), dorsal spine of the last trunk ring (LTrRDS; Wing-tip spine [WS] as in H. coronatus and H. haema). Points used for measurements: a tip of snout (upper jaw) b anterior side of tubercle/spine c anterior edge of orbit d posterior edge of orbit e mid-point of cleithral ring f median groove (central depression) of coronet g gill opening h mid-point of lateral ridge of the last trunk ring i tail tip. Measurements: a–b snout length (SnL) c–d eye diameter (ED), a–e head length (HL) e–f coronet height from mid-point of cleithral ring (CHMC) f–g coronet height from gill opening (CHGO) e–h trunk length (TrL) h–i tail length (TaL) a–e–h–i standard length (SL). Photographed specimen H. haemaPKU 10129 (paratype).

Molecular analysis

Tissue from the right eye ball or from the right-side of the tail was used to isolate genomic DNA from 22 specimens with moderately high coronets, collected in Busan, Tongyeong, Boseong, Soan Island, Maizuru, and Minami-ise, and from four specimens with extremely high coronets collected in Miura. Isolation was performed using an AccuPrep® Genomic DNA Extraction Kit (Bioneer, Daejeon, Korea), according to the manufacturer’s instructions.

Three partial mitochondrial DNA loci (cytochrome b [cyt b], 16S rRNA, and 12S rRNA) were amplified via polymerase chain reaction (PCR), which was conducted on an S1000™ Thermal Cycler (Bio-Rad, Hercules, CA, USA). The PCR solutions consisted of 3 μl 10× Ex Taq buffer (20 mM Mg2+ plus), 2.4 μl 2.5 mM dNTPs, 1 μl each primer, 0.1 μl TaKaRa Ex Taq DNA polymerase (Takara Bio, Kusatsu, Shiga, Japan), 3 μl genomic DNA, and distilled water to bring the total volume to 30 μl. The PCR amplification of cyt b was conducted using primers Shf2 (5'-TTGCAACCGCATTTTCTTCAG-3') and Shr2 (5'-CGGAAGGTGAGTCCTCGTTG-3') under the following conditions: initial denaturation at 94°C for 2:30 min; 35 cycles of denaturation at 94°C for 30 s, annealing at 50°C for 30 s, and extension at 72°C for 1:15 min; final extension at 72°C for 5 min (Lourie and Vincent 2004). Using the universal primers 16Sal-L (5'-CGCCTGTTTATCAAAAACAT-3') and 16Sbr-H (5'-CCGGTCTGAACTCAGATCACGT-3'), 16S rRNA was amplified as follows: initial denaturation at 94°C for 5 min; 35 cycles of denaturation at 94°C for 30 s, annealing at 50°C for 1 min, and extension at 72°C for 1 min; final extension at 72°C for 10 min (Palumbi 1996). The amplification of 12S rRNA was conducted using primers OMT16SF (5'-TGCCAGCCACCGCGGTTATACCT-3') and tRNA02 (5'-GGATGTCTTCTCGGTGTAAG-3') (both from Mukai et al. 2000), under the following conditions, which were modified from Mukai et al. (2000): initial denaturation at 95°C for 2:30 min; 30 cycles of denaturation at 95°C for 1 min, annealing at 55°C for 1 min, and extension at 70°C for 2 min; final extension at 70°C for 5 min. Amplified PCR samples were purified using a Davinch™ PCR Purification Kit (Davinch-K, Seoul, Korea), according to the manufacturer’s instructions. Sequencing reactions were performed in a DNA Engine Tetrad 2 Peltier Thermal Cycler (Bio-Rad) using an ABI BigDye(R) Terminator 3.1 Cycle Sequencing Kit (Applied Biosystems, Waltham, MA, USA).

Sequences of the three gene regions belonging to members of the H. coronatus complex (H. coronatus and H. sindonis), its sister species (H. mohnikei), some members of the H. kuda complex (H. kuda, H. reidi, and H. ingens) (Lourie et al. 1999, 2004), and one outgroup (Syngnathus schlegeli) were retrieved from the GenBank database (www.ncbi.nlm.nih.gov) (Table 1). Sequences obtained for each species were concatenated and each gene region was treated as a partition. To compare our results with that of Mukai et al. (2000), an additional analysis focusing on 12 rRNA sequence variation was performed. GenBank sequences were aligned with those obtained in the present study using BioEdit7 (Hall 1999), and pairwise genetic distances were calculated using the Kimura 2-parameter model (Kimura 1980) on MEGA6 (Tamura et al. 2013). Neighbor-joining (NJ) trees were constructed in MEGA6, and confidence levels were assessed using 1000 bootstrap replications.

Table 1.
Download as
CSV
XLSX

GenBank accession numbers and sources of the mitochondrial gene sequences used in the evaluation of the phylogenetic relationships among species belonging to the Hippocampus coronatus complex.

Species Locus Accession No. Source
Hippocampus haema sp. n. cyt b KP744863–>KP744882 Present study
16S rRNA KP744883–>KP744902
12S rRNA KP744903–>KP744922
H. coronatus cyt b KT167545–>KT167548 Present study
16S rRNA KT167549–>KT167552
12S rRNA KT167553–>KT167556
12S rRNA AB032030 Mukai et al. (2000)
H. sindonis cyt b KT167539–>KT167540 Present study
16S rRNA KT167541–>KT167542
12S rRNA KT167543–>KT167544
12S rRNA AB032029 Mukai et al. (2000)
H. mohnikei complete mitogenome KT780446 Zhang et al. (2017)
12S rRNA AB032028 Mukai et al. (2000)
H. kuda complete mitogenome AP005985 Kawahara et al. (2008)
H. reidi complete mitogenome KJ123692 Wang et al. (2016)
H. ingens complete mitogenome KF680453 Zhang et al. (2015)
Syngnathus schlegeli complete mitogenome AP012318 Song et al. (2014)

Systematics

Hippocampus coronatus Temminck & Schlegel, 1850

Figs 3F–G, 4B, 5C, 6B, 6E, Tables 2, 3 English name: Crowned seahorse, New Korean name: -haema, Japanese name: Tatsu-no-otoshigo

Hippocampus coronatus Temminck and Schlegel 1850: 274, pl. 120 (fig. VII) (Lectotype: RMNH.PISC.D 1543; Paralectotype: RMNH.PISC.D 1544; type locality: Japan; Boeseman 1947: 196); Kaup 1853: 229; Jordan and Snyder 1901: 18; Matsubara 1955: 431; Jordan et al. 1913: 100; Boeseman 1947: 195; Burgess and Axelrod 1972: 212; Araga 1984: 89; Senou 1993: 489, 1294; Lourie et al. 1999: 88; Mukai et al. 2000: 139; Senou 2000: 536; Senou 2002: 536, 1508; Lourie et al. 2004: 42; Yoshino and Senou 2008: 76; Kuiter 2009: 129; Kohno et al. 2011: 127; Senou 2013: 635, 1911; Lourie 2016: 106; Lourie et al. 2016: 21.

Material examined

Japan. RMNH.PISC.D 1543 (lectotype of H. coronatus, photograph from RMNH), female, 103.3 mm SL, von Siebold collection. RMNH.PISC.D 1544 (paralectotype of H. coronatus, photograph from RMNH), female, 100.2 mm SL, von Siebold collection. FAKU 137348–137351, 4, 96.4–112.6 mm SL, Miura, Kanagawa, Nov 2014, H. Sugawara. KAUM-I 20721, 1, 73.7 mm SL, Takane, Hamasa, Tateyama, Chiba, 34°58'38"N; 139°47'19"E, depth 20 m, 2 Dec 2008, M. Aizawa. KPM-NI 1375, 1, 82.0 mm SL, 6 Sep 1964. KPM-NI 7301–7302, 2, 110.5–117.9 mm SL, depth 4 m, 12 Jul 2000; KPM-NI 7535, 1, 124.1 mm SL, 19 Dec 2000, S. Gosho; KPM-NI 7718–7720, 3, 113.1–115.6 mm SL, depth 1–12 m, 18 Jan 2001, S. Gosho; KPM-NI 8075, 1, 115.3 mm SL, depth 3–4 m, 26 Jul 2001, K. Uchino & D. Kanbayashi; in front of Misaki Marine Biological Station, The University of Tokyo, Aburatsubo Bay, Koajiro, Miura, Kanagawa. KPM-NI 14854, 1, 24.1 mm SL, in front of Keikyu Aburatsubo Marine Park, Koajiro, Miura, Kanagawa, T. Mukai. KPM-NI 19270, 1, 113.7 mm SL, Cape of Manazuru, Obaradai, Yokosuka, Kanagawa, 1 Jul 2000, T. Yokoo. KPM-NI 19272, 1, 108.5 mm SL, Kannonzaki, Tatara-hama, Obaradai, Yokosuka, Kanagawa, 12 Dec 1998, T. Yokoo. KPM-NI 18765, 18772, 2, 27.8–28.4 mm SL, 14 Jun 2006, Y. Miyazaki; KPM-NI 21540, 1, 39 mm SL, 6 Jul 2003; KPM-NI 21541, 1, 53.4 mm SL; 19 Jun 2004; KPM-NI 25371, 1, 103.5 mm SL, depth 7 m, 27 Jun 2009, S. Shimizu; in front of Tateyama Station of Field Science Center, Tokyo University of Marine Science and Technology, Banda, Tateyama, Chiba. KPM-NI 27901–27903, 3, 51.4–67.5 mm SL, 2–6m depth, 5 Oct 2010, N. Takeuchi; KPM-NI 29380, 1, 47.8 mm SL, depth 2–6 m, 3 Jun 2011, N. Takeuchi; Gouchome, Shimoda, Shizuoka. KPM-NI 30596, 1, 133.0 mm SL, Sagami bay, Kanagawa Hadano High School, Kanagawa.

Figure 3. 

Specimens within the Hippocampus coronatus complex examined in the present study. A–E H. haema APKU 9641 (holotype, Busan, Korea) BFAKU 135644 (paratype, Maizuru, Japan) CKPM-NI 24769 (paratype, Akita, Japan) DRMNH.PISC.D 1541 (paratype, Japan) ERMNH.PISC.D 1542 (paratype, Japan) F–G H. coronatus FRMNH.PISC.D 1543 (lectotype, Japan) GRMNH.PISC.D 1544 (paralectotype, Japan) H–I H. sindonis HRMNH.PISC 3924 (Japan) IUSNM 49730 (holotype, Hamamatsu, Japan).

Diagnosis

A species of Hippocampus having a bony body; double gill openings; ring (R: TrR + TaR) 10 + 37–40, mode 10 + 39 (lectotype: 10 + 38); extremely high coronet, straight or inclined backwards; CoT 4; CHGO 43.0–60.1 % HL; CHMC 55.7–79.0 % HL; WS thick and recurved.

Description

Head and trunk folded at approximately right angle; snout elongated and fused; pelvic and caudal fins absent; prehensile tail; D 12–15, mode 14 (lectotype: 14); A 4; P 10–13, mode 12 (lectotype: 12); D always greater than or equal to P; CS 1; ES 1; SnL 35.6–44.2 % HL; ED 32.3–62.9 % SnL; HL 56.6–71.3 % TrL; TrL 42.6–64.5 % TaL; flat and smooth skin generally covering armor-plated body; ACS degenerative; Coa expanded; CoT 4 arising from degenerative PCS; WS two fused LTrRDS (lower more developed than upper and recurved; upper LTrRDS occasionally standing out [Fig. 6E]); dorsal and lateral spines more prominent on 1st, 4th, 7th, and 10thTrR than on other TrRs, except occasionally for lateral spines on 10thTrR, occasionally; usually no skin filaments on body, but, occasionally, a strand was observed on ACS or on the forward part of Coa; blunt (or absent) body spine; often whitish radial blotches from iris to surrounding eye and striped-pattern body; occasionally semicircular band present on dorsal fin; variable color, light to dark red-brown or yellow, sometimes showing numerous thin whitish striations and/or dark small dots along body; male brood pouch sometimes speckled with fine white and dark spots (Kuiter 2009); no particular sexual dimorphism, apart from male brood pouch.

Distribution

Southeastern coast of Honshu (Japan), from Izu Peninsula (Shizuoka Prefecture) to Boso Peninsula (Chiba Prefecture) (Fig. 1). Hippocampus coronatus lives in weed habitats, especially in floating Sargassum (Kuiter 2009; Senou 2013), within shallow areas (0–20 m depth).

Figure 4. 

Coloration of fresh specimens. A Hippocampus haema (paratype, PKU 9424) B H. coronatus (FAKU 137351) C H. sindonis (FAKU 137339).

Etymology

The Latin word coronatus means crowned. The new Korean name, Wanggwan-haema means ‘crowned seahorse’, in agreement with the English and scientific names. In fact, Haema, which has the connotation ‘common’ and ‘fish species belonging to the genus Hippocampus’ in Korean, has been used to name seahorses commonly found in Korea, whereas Wanggwan-haema has been informally used to refer to H. coronatus in Korean. In addition, the word wanggwan [crown] is more suited for H. coronatus, whose coronet is considerably higher than that of H. haema. The Japanese name Tatsu-no-otoshigo literally means ‘dragon’s bastard child’.

Remarks

Temminck and Schlegel (1850) described H. coronatus based on five specimens. Boeseman (1947) designated one of these specimens RMNH.PISC.D 1543 as the lectotype. As a consequence the other three specimens RMNH.PISC.D 1541, RMNH.PISC.D 1542, and RMNH.PISC.D 1544 became paralectotypes, except that RMNH.PISC 3924 was reidentified as H. mohnikei (see remarks of H. sindonis below). However, two of the specimens described in Boeseman (1947), RMNH.PISC.D 1541 and 1542, have a moderately high coronet, not agreeing with the H. coronatus described in the present study and being more similar to H. haema (see species description below). The lectotype RMNH.PISC.D 1543 and the paralectotype RMNH.PISC.D 1544 have an extremely high coronet, which agrees with the present description of H. coronatus. Our 28 specimens have an extremely high coronet, a wing-tip spine on the dorsal fin base, and CoT 4, as described and illustrated in Temminck and Schlegel (1850). The phylogenetic trees obtained in the present study also support the differentiation of these 28 specimens from H. sindonis and H. haema (Fig. 7).

The type series does not match Temminck and Schlegel (1850)’s description on the basis of five dried specimens and an illustration which was based on a small male seahorse (Temminck and Schlegel 1850; Kaup 1853). The lectotype (RMNH.PISC.D 1543) and the paralectotype (RMNH.PISC.D 1544) are large female seahorses (100.2–103.3 mm SL), and RMNH.PISC.D 1541, 1542, and RMNH.PISC 3924 are small female seahorses (67.5–74.0 mm SL). RMNH.PISC 3924 is preserved in spirits unlike the other specimens, therefore Boeseman’s inclusion of this sample is questionable. The original illustration of H. coronatus from Temminck and Schlegel (1850) might be the missing fifth dry specimen (personal communication, M. van Oijen).

The type locality of H. coronatus has not been established. Although it is thought to be Nagasaki (Eschmeyer et al. 2017), no specific locality information is provided for the type series or in previous studies (Temminck and Schlegel 1850; Boeseman 1947; Lourie et al. 1999). Seahorses are used historically as charm for safe-birth in East Asia (Korea, Japan, and China) and as a trinket in western culture (Lourie et al. 1999; Scales 2009). Thus, we cannot exclude the possibility that dried specimens might be from someone’s folkloric collection (MacLean, 1973). This historical element might support that the type series was not caught in the Nagasaki area. Therefore, it is possible that collectors not only gathered specimens from Nagasaki, but Edo (present-day Tokyo) as well, which is the habitat of H. coronatus in this study (see Fig. 1; personal communication, M. van Oijen; MacLean 1973; Compton and Thujsse 2013; Nofuji et al. 2013).

Although H. coronatus sensu stricto was considered to be distributed along the coast of Japan and southern coast of Korea, we only found records from the Pacific Ocean. Mori (1928) reported H. coronatus off Korea for the first time, but the original data consisted only of checklists, not providing descriptions; thus, Mori (1928) might be reporting the occurrence of H. haema or H. coronatus. Therefore, the distribution of H. coronatus needs to be reviewed. In Korea and Japan, seahorse identification has been generally treated as a laborious task, leading to taxonomic controversy and misidentifications; thus, we recommend a careful revision of H. coronatus recorded from Korea and Japan.

Senou (2002) and (2013) suggested that the publication date for H. coronatus was in 1847. However, based on Sherborn and Jentick (1895), Boeseman (1947), Mees (1962), Bauchot et al. (1982), and Eschmeyer et al. (2017), the year should be 1850.

Figure 5. 

X-radiographs of Hippocampus specimens. A H. haemaPKU 9641 (holotype) B H. haemaNIBR-P 5412 (paratype) C H. coronatusFAKU 137348 D H. sindonisFAKU 137340 E H. sindonisUSNM 49730 (holotype) F H. mohnikeiFAKU 135643. a' indicates the anterior coronet spine; 5' indicates the posterior coronet spine (the 5th tip on the corona); the first (1) and last (10 or 11) trunk rings are marked.

Hippocampus sindonis Jordan & Snyder, 1901

English name: Painted seahorse, Korean name: Sindo-haema, Japanese name: Hanatatsu Figs 3H–I, 4C, 5D–E, 6C, 6F, Tables 2, 3

Hippocampus sindonis Jordan and Snyder 1901: 17, pl. 11 (Holotype: USNM 49730; type locality: Totomi bay, off Hamamatsu, Totomi Province, Shizuoka, Japan); Jordan et al. 1913: 100; Matsubara 1955: 431; Araga 1984: 89; Lourie et al. 1999: 119; Mukai et al. 2000: 139; Senou 2000: 536; Senou 2002: 536, 1508; Lourie et al. 2004: 74; Yoshino and Senou 2008: 76; Kuiter 2009: 131; Senou 2013: 635, 1911; Lourie 2016: 108; Lourie et al. 2016: 39.

Hippocampus coronatus : Burgess and Axelrod 1972: 211; Araga 1984: 89; Senou 1993: 489 (left fig.), 1294 (non Temminck & Schlegel).

Hippocampus mohnikei : Jordan and Snyder 1901: 18; Jordan et al. 1913: 98; Boeseman 1947: 196; Matsubara 1955: 431; Burgess and Axelrod 1972: 210; Araga 1984: 89 (non Bleeker).

Hippocampus japonicus : Burgess and Axelrod 1972: 211 (non Kaup).

Material examined

Japan. USNM 49730 (holotype of H. sindonis, photograph and radiograph from USNM), male, 49.1 mm SL, Totomi bay, off Hamamatsu, Totomi Province, Shizuoka, dredged by the U.S. Fish Commission Steamer Albatross (Jordan and Snyder 1901). RMNH.PISC 3924 (photograph from RMNH), 1 female, 74.0 mm SL. FAKU 121388, 1, 69.4 mm, Tanabe, Wakayama, Jan 1969. FAKU 137339, 1 93.0 mm, Hozaura, Minami-ise, Watarai, Mie, depth 20–25 m, Nov 2014, H. Sugawara. FAKU 137340, 1, 95.9 mm, Nayaura, Minami-ise, Watarai, Mie, depth 25–30 m, Mar 2014, H. Sugawara. KPM-NI 19257, 1, 59.4 mm SL, 16 May 1999, D. Sugita; KPM-NI 19258, 1, 44.4 mm SL, 18 Oct 1997, M. Kojima; KPM-NI 19259, 1, 30.1 mm SL, 5 Jul 1998, T. Kamano; KPM-NI 19261, 1, 43.3 mm SL, 7 Aug 1998, N. Ogata; KPM-NI 19262, 1, 32.2 mm SL, 25 Aug 1998, N. Ogata; Kannonzaki, Tatara-hama, Obaradai, Yokosuka, Kanagawa. KPM-NI 19475, 1, 82.1 mm SL, 23 Sep 2007 K. Okubo; KPM-NI 19797–19798, 2, 75.1–99.8 mm SL, 18 Oct 2007, K. Okubo; KPM-NI 21947, 1, 75.4 mm SL, K. Okubo; Manatsuru, Ashigarashimo, Kanagawa.

Diagnosis

A species of Hippocampus having a bony body; double gill openings; R 10 + 35–38 (holotype: 10 + 37); coronet moderately high; CoT 5; CHGO 26.8–41.0 % HL; CHMC 36.3–55.4 % HL; a very blunt or truncated spine on the dorsal fin base; no WS on dorsal fin base.

Description

Head and trunk folded at approximately right angle; snout elongated and fused; pelvic and caudal fins absent; prehensile tail; D 11–15, mode 12 (holotype: 15); A 4; P 11–14, mode 11 (holotype: 14); D always greater than or equal to P; CS 1; ES 2 (anterior ES smaller than posterior ES); SnL 28.7–37.2 % HL; ED 41.5–69.0 % SnL; HL 57.2–80.1 % TrL; TrL 38.3–52.1 % TaL; coarse skin often covering armor-plated body; moderately high coronet; CoT, 5; body spines blunt, truncated, or absent; spines on 1st, 4th, 7th, and 10thTrR more prominent than on other TrRs, except for the lateral spine on the 10thTrR; several skin filaments on ACS and ES, and prominent TrR and TaR spines, or skin filaments absent on these structures; variable coloration on fresh specimens, including white, red, yellow, brown, and grey; variable patterns on fresh specimens, often presenting white radial blotches on iris and surrounding eye, stripes and/or blotches on body, and, occasionally, a semicircular stripe on dorsal fin; preserved specimens, black, pale white, brown, or grey; no sexual dimorphism apart from male brood pouch.

Figure 6. 

Distinctive morphological characters among species within the Hippocampus coronatus complex. A–C Tips on the corona flat A H. haema (PKU 9641, holotype) B H. coronatus (KPM-NI 7720) C H. sindonis (KPM-NI 19797). Numbers indicate coronet tips; the 5th coronet tip (posterior coronet spine) is indicated in red. The * indicates the appendage growing on the anterior coronet spine, which is a skin filament D–F Dorsal fin base spines (red arrows; wing-tip spines in D and E) D H. haema (PKU 9641, holotype) E H. coronatus (KPM-NI 7720) F H. sindonis (KPM-NI 19797).

Distribution

Southeastern coast of Honshu (Japan), from Tanabe (Wakayama Prefecture) to Boso Peninsula (Chiba Prefecture) (Fig. 1). Hippocampus sindonis lives in a wide range of habitats, from shallow high-energy algae reefs to soft bottom habitats (Kuiter 2009), at 2–30 m depth (Senou 2013).

Etymology

The specific name sindonis was derived from the name of M. Sindo, an assistant curator of fishes at Stanford University (Jordan and Snyder 1901; Lourie 2016). The English name was coined by Kuiter (2009). The Japanese name Hanatatsu literally means ‘hana (flower or blossom, which indicates gorgeous) + tatsu (dragon, or the abbreviation of the word “Tatsu-no-otoshigo: seahorse”)’, and refers to the beautiful color and skin filaments of the species.

Remarks

The 14 Japanese specimens of H. sindonis have a moderately high coronet with five CoT, and a couple of prominently blunted or truncated spines on the dorsal fin base, therefore corresponding to the description and holotype of H. sindonis provided by Jordan and Snyder (1901). In the 12S rRNA tree, our H. coronatus specimens (voucher number: FAKU 137348–137351) appeared in the same clade as Mukai et al.'s (2000) high coronet specimen (GenBank accession number AB032030) whereas our H. sindonis specimens (voucher numbers FAKU 137339–137340) formed a clade with Mukai et al.'s (2000) low coronet specimen (accession number AB032029) (Fig. 7B). Hippocampus sindonis is considered the most external group within the H. coronatus complex because of its homogenous CoT (= 5) and no WS, as found in H. coronatus complex outgroups (e.g., H. mohnikei and H. trimaculatus).

RMNH.PISC 3924 was labeled ‘Hippocampus fasciatus Kaup 1853’ (Boeseman 1947), which is a nomen nudum in Hippocampus. Boeseman (1947) noted that RMNH.PISC 3924 was related to H. coronatus and H. mohnikei, and that its morphology agreed with Jordan and Snyder’s (1901) description as well as with Bleeker’s (1853)H. mohnikei specimens. However, we found that Bleeker’s H. mohnikei (RMNH.PISC 7259, 3 specimens) differ from RMNH.PISC 3924 in their TrR number (11 in Bleeker’s specimens vs. 10 in RMNH.PISC 3924). Thus, RMNH.PISC 3924 belongs to the H. coronatus complex, and its ES 2 and coronet features (moderately high coronet with 5 CoT) allow identifying it as H. sindonis. Jordan and Snyder (1901) stated that H. sindonis was distinguished from H. mohnikei by dorsal fin features (D 15 and long dorsal fin base in H. sindonis vs. D 11–13 and short dorsal fin base in H. mohnikei), but their key did not consider individual variations. Our H. sindonis specimens agree with both H. mohnikei and H. sindonis descriptions, but the paradoxical inconsistency between the original description and type series of H. mohnikei requires a further taxonomic review of this species, and, therefore, we compared our specimens with ‘H. mohnikei’ holotype and not to the original description of the species (Lourie et al. 1999; Eschmeyer et al. 2017).

Nakamura (1999a) described a single specimen of H. sindonis caught off Kumamoto, Japan, which is questionable, as there are no other records of H. sindonis from western Kyushu. This record may have been based on H. haema because spines were not mentioned in Nakamura’s description. Kim et al. (2013) recorded a H. sindonis specimen from Korean waters (voucher: NIBR-P 5412; Fig. 5B). However, the morphology of this specimen indicates that it rather belongs to H. haema and we include it in the type series of H. haema. Thus, there are no reliable records of H. sindonis from Korea.

Figure 7. 

Neighbor-joining tree showing the relationships among species of Hippocampus based on mtDNA sequences. A tree produced using multiple loci (cytochrome b, 16S rRNA, and 12S rRNA) as partitions B tree produced using 12S rRNA, only. Numbers in branches indicate bootstrap probabilities obtained from 1000 bootstrap replications. Scale bar = genetic distance of 0.02.

Hippocampus haema sp. n.

http://zoobank.org/13F12FB3-B435-4AD4-B02F-110E20C06C56
New English name: Korean seahorse, Korean name: Haema, New Japanese name: Himetatsu Figs 3A–E, 4A, 5A–B, 6A, 6D, Tables 2, 3

Hippocampus coronatus : Jordan and Snyder 1901: 19; Mori 1928: 5; Boeseman 1947: 195; Mitani 1956: 30; Chyung 1977: 272; Araga 1984: 89; Senou 1993: 489 (right fig.), 1294; Kim and Lee 1995: 76; Nakamura 1999b: 125; Senou 2000: 536; Choi et al. 2002: 141; Senou 2002: 536, 1508; Kim et al. 2005: 203; Choi et al. 2006; Yoshino and Senou 2008: 76; Kohno et al. 2011: 127; Senou 2013: 635, 1911; Han et al. 2014: 423 (non Temminck & Schlegel).

Hippocampus cf. coronatus : Kuiter 2009: 128.

Hippocampus sindonis : Nakamura 1999a: 124; Yoshino and Senou 2008: 76; Kim et al. 2013: 42 (non Jordan & Snyder).

Hippocampus kuda : Kim et al. 2001: 67, Myoung et al. 2002: 74 (non Bleeker).

Hippocampus sp.: Kim and Ryu 2017: 110.

Holotype

PKU 9641, 1, female, 90.3 mm SL, Namcheon Harbor, Namcheon 1-dong, Suyeong-gu, Busan, Korea, 35°08'16"N; 129°06'51"E, 9 Aug 2013, H. J. Kwun, hand net.

Paratypes

139 specimens: specimens (74.0–99.0 mm SL). Korea: NIBR-P 5412, 1, female, 74.0 mm SL, off Geomun Island, Yeosu-si, Jellanam-do, depth 18 m, 17 Apr 2009, T. S. Park, SCUBA Diving & hand net. NIBR-P 1602, 1, 59.4 mm SL, Wonpo, Yeosu-si, Jeollanam-do, 27 Aug 2006, J. H. Ryu. NIBR-P 19724, 3, 58.4–71.8 mm SL, 25 Jan 2012, H. G. Cho & S. H. Lee; NIBR-P 19725–19727, 19729, 7, 33.3–102.2 mm SL, 13 Sep 2012, Y. Eun, S. Lee & S. S. Hong; Jisepo-ri, Irun-myeon, Geoje-si, Gyeongsangnam-do. PKU 6097, 1, 77.5 mm SL, 30 Aug 2011; PKU 9422–9424, 3, 80.6–92.3 mm SL, 12 Jul 2013, hand net; PKU 9704, 1, 82.3 mm SL, 1 May 2013, J. M. Lee; PKU 9705–9712, 8, 65.7–98.1 mm SL, 26 Jul 2012, J. M. Lee; PKU 9713–9717, 9719–9720, 7, 61.6–85.1 mm SL, 9 Dec 2012, J. M. Lee; PKU 9721–9723, 3, 80.8–91.5 mm SL, 20 Aug 2012, J. M. Lee; PKU 9724–9731, 8, 73.2–113.9 mm SL, 17 Jul 2012, J. M. Lee; PKU 9732–9740, 9, 62.4–100.2 mm SL, 17 Aug 2012, J. M. Lee; PKU 9741–9747, 7, 56.4–81.9 mm SL, 21 Jun 2012, J. M. Lee; PKU 9748, 1, 56.8 mm SL, 11 Sep 2012, J. M. Lee; PKU 10128–10129, 2, females, 52.2–62.7 mm SL, 23 Oct 2013, H. J. Kwun; PKU 54069–54074, 6, 32.3–77.5 mm SL, 21 Mar 2015, J. M. Lee; Namcheon Harbor, Namcheon 1-dong, Suyeong-gu, Busan, 35°08'16"N; 129°06'51"E, hand net. PKU 7230–7233, 4, 41.9–83.7 mm SL, Ulsan, 14 Sep 2012, hand net. PKU 10277, 1, 72.7 mm SL, Minrak Harbor, Millak-dong, Suyeong-gu, Busan, 35°09'14"N; 129°07'51"E, 20 Feb 2014, H. J. Yu & W. J. Lee, hand net. PKU 11159, 1, 30.9 mm SL, Hak-ri, Ilgwang-myeon, Gijang-gun, Busan, 22 Jul 2014, J. Y. Bae, hand net. PKU 11170–11180, 11, 74.2–102.4 mm SL, Soan Island, Soan-myeon, Wando-gun, Jeollanam-do, May 2014, S. Rho, bottom trawl. PKU 11181–11182, 2, 71.8–84.2 mm SL, Gunhak village, Jeonil-ri, Hoecheon-myeon, Boseong-gun, Jeollanam-do, 24 Dec 2013, S. Rho, bottom trawl. PKU 11266, 1, 74.1 mm SL, 24 Jul 2014; PKU 11634, 1, 69.9 mm SL, 25 Sep 2014; Hwayang-myeon, Yeosu-si, Jeollanam-do, hand net. PKU 11395–11401, 7, 62.3–98.7 mm SL, Jangu Island, Suwol-ri, Dosan-myeon, Tongyeong-si, Gyeongsangnam-do, Sep 2014, K. S. Han & H. D. Mun, Shrimp beam trawl. PKU 11449, 1, 81.0 mm SL, Jul 2014; PKU 11635–11637, 3, 15.9–84.7 mm SL, 24 Sep 2014; Gijang-gun, Busan, hand net. Japan: RMNH.PISC.D 1541–1542 (photograph by RMNH), 2, female, 67.5–68.5? mm SL, von Siebold collection. FAKU 109359, 1, 58.0 mm SL, Tassha, Sado Island, Niigata, 24 Oct 1955. FAKU 135638, 2, 82.7–88.9 mm SL, 22 Sep 2011; FAKU 135639, 2, 53.2–86.0 mm SL, 23 Aug 2010; FAKU 135640, 135644, 2, 76.2–86.8 mm SL, 29 Jul 2011; FAKU 135641, 1, 61.4 mm SL, 20 Aug 2008; FAKU 135642, 1, 57.4 mm SL, 6 Sep 2008; Maizuru Bay, Maizuru, Kyoto, Y. Kai. FAKU 136087, 1, 76.1 mm SL, Tsuruga, Fukui, 28 Jun 2014. FAKU 136119, 1, 59.2 mm SL, Kamai, Kyotango, Kyoto, 19 Jul 2014, F. Tashiro. KPM-NI 1615, 1, 91.6 mm SL, Aug 1933. KPM-NI 6770, 1, 57.9 mm SL, Azo, Tsuruga, Fukui, depth 5 m, 13 Aug 1999, T. Nomura. KPM-NI 24769, 1, female, 83.3 mm SL, Akita, H. Sugiyama. KPM-NI 31204, 1, 47.5 mm SL, Takahama-cho, Ooi, Fukui, 2 Oct 2012, M. Mune. KPM-NI 31620, 1, 72.7 mm SL, 27 Feb 2013; KPM-NI 31707, 1, 60.6 mm SL, 11 Mar 2013; Ogurui, Takahama-cho, Ooi, Fukui, depth 7 m, M. Mune. KPM-NI 31880–31883, 4, 76.6–85.5 mm SL, depth 0–2 m, 7 May 2013; KPM-NI 36111–36112, 2, 77.1–78.6 mm SL, depth 1–3 m, 28 Apr 2014; Agurizaki Point, Ooshima, Ooi-cho, Ooi-gun, Fukui, M. Mune. KPM-NI 35122–35123, 2, 46.3–46.8 mm SL, Tanoura, Takahama, Ooi-cho, Ooi, Fukui, depth 0–1 m, 3 Jul 2013, M. Mune. KPM-NI 35291–35297, 7, 54.5–74.9 mm SL, Koda Fishing Port, Notojimakouda-machi, Notojima Island, Nanao, Ishikawa, depth 1–3 m, 2013, H. Masaki. KAUM-I 12745, 1, 100.5 mm SL, 12 Oct 2007, depth 5 m, kept in Kagoshima Aquarium and dead on 8 Dec 2008; KAUM-I 12746, 1, 96.9 mm SL, 13 Feb 2008, kept in Kagoshima Aquarium and dead on 4 Aug 2008; off Nagashima Station, Faculty of Fisheries, Kagoshima University, Usui, Azuma, Izumi, Kagoshima, M. Yamada. KAUM-I 19885, 1, male, 99.0 mm SL, off Nagashima Station, Faculty of Fisheries, Kagoshima University, Usui, Azuma, Izumi, Kagoshima, 32°13'22"N; 130°10'31"E, 13 Feb 2008, Kagoshima Aquarium, hand net, kept in Kagoshima Aquarium and dead on 30 Apr 2007.

Diagnosis

A species of Hippocampus having a bony body; double gill openings; R 10 + 35–38, mode 10 + 36 (holotype: 10 + 36); coronet moderately high and turned back on top; CoT 4; CHGO 22.7–41.6 % HL; CHMC 34.1–54.9 % HL; a WS on the dorsal fin base.

Description

Head and trunk folded at approximately right angle; snout elongated and fused; pelvic and caudal fins absent; prehensile tail; D 11–14, mode 13 (holotype: 14); A 4; P 10–13, mode 12 (holotype: 13); D always greater than or equal to P; CS 1; ES 1–2 (in ES 2, anterior ES smaller than posterior ES), mode 1 (holotype: 2); SnL 28.8–49.0 % HL; ED 27.1–68.9 % SnL; HL 57.3–88.7 % TrL; TrL 37.4–57.2 % TaL; often flat and smooth skin covering armor-plated body; coronet turned back on top; CoT 4 arising from degenerative PCS (5th coronet tip); WS two fused spines (lower spine more developed than upper spine, recurved; occasionally, upper spine stands out giving appearance of two dorsal fin base spines); dorsal and lateral spines at 1st, 4th, 7th, and 10thTrR more prominent than on other TrRs, except for lateral spines on 10thTrR (occasionally none or degenerative spine); Several skin filaments on body, ACS, and prominent dorsal and lateral spines on 1st, 4th, and 7thTrR; Several colors when fresh: black, white, orange, yellow, magenta, claret, brown, grey with black, red, or white stripe, and frostlike whitish or grey striations along prominent TrR and TaR; whitish radial blotches from iris to surrounding eye often present; semicircular band on dorsal fin occasionally present; when fixed in alcohol, specimens become black, white, brown, and grey; blunt (or absent) body spine; no particular sexual dimorphism except for male brood pouch. Minimum size at sexual maturity, 53.9 mm SL in males.

Distribution

Korea: southern and southeastern coasts of the Korean Peninsula (from Soan Island to Ulsan); Japan: western coast of Kyushu (western Kagoshima Prefecture), northwestern coast of Honshu (from Kyoto Prefecture to Akita Prefecture) (Fig. 1). Lives in floating Sargassum and weeds on shallow soft bottom habitats from 0–18 m depth (e.g. Kim et al. 2016).

Etymology

The Korean word Haema means ‘seahorse’, which connotes ‘representative’ and ‘common’. Thus, the scientific and Korean names Haema were chosen to indicate that this seahorse is the one most commonly found in Korea. The Japanese name Himetatsu means ‘princess seahorse’ or ‘dwarf seahorse’, and refers to its lower coronet and smaller body compared to H. coronatus.

Remarks

Temminck and Schlegel (1850) described the extremely high coronet as follows: coronet height (CHGO, based on the inquiry of type specimens and on Jordan and Snyder [1901]’s description) of H. coronatus is identical to its SnL, 1/5 shorter than remaining HL (i.e., 4/9 of HL). All H. haema specimens present a moderately high coronet (CHGO 22.7–41.6 % HL and CHMC 34.1–54.9 % HL) when compared to H. coronatus (extremely high coronet, CHGO 43.0–60.1 % HL and CHMC 55.7–79.0 % HL). Our H. sindonis specimens (including the holotype, USNM 49730) differ from H. haema in their 5 CoT and blunt or truncated LTrDS (vs. CoT 4 and WS [recurved LTrDS] in H. haema) (Fig. 6). The genetic distance between H. haema and H. coronatus is greater than that between species of the H. kuda complex (i.e., H. kuda, H. reidi, and H. ingens), supporting specific distinctness (Fig. 7; Table 4).

Our data also suggest the existence of two subgroups, one from Korea and another from Japan: cyt b sequences of H. haema collected in these two areas consistently present two base pairs (bp) differences (0.3%–0.8% genetic distance). Based on molecular results, H. haema is more closely related to H. coronatus than to H. sindonis (Fig. 7; Table 4), but based on coronet height and on the number of TaR, except for CoT and WS, it is more similar to H. sindonis (Tables 2 and 3).

Hippocampus haema was collected off the southern and southeastern coasts of Korea, but we were not able to collect H. haema off the western or northeastern coasts of Korea; only H. mohnikei was collected from all Korean waters. A few studies have reported H. coronatus from the western coast of Korea (Lee and Seok 1984; Hwang 1998; Hwang et al. 1998; Hwang et al. 2005), but these publications are mostly checklists, similar to that of Mori (1928), and H. mohnikei is not referred to in written records. Such inconsistency might be the result of misidentifications. The northern boundaries of H. coronatus in Korean waters determined in our study are similar to the distributions found by Choi et al. (2002) and Kim et al. (2005), who stated H. coronatus was limited to the southern coast of Korea, similarly to H. mohnikei. We found that the habitat of H. haema is affected by the Tsushima Warm Current (Briggs 1995; Nakabo 2009; Ishizu et al. 2017) and, therefore, H. haema might only rarely be found off the western and northeastern coasts of Korea.

Discussion

The NJ trees based on cyt b (670 bp), 16S rRNA (405 bp), and 12S rRNA (344 bp) recovered three monophyletic groups within the H. coronatus complex, all supported by high bootstrap probabilities (Fig. 7): viz. Hippocampus coronatus group, H. sindonis group, and H. haema group. This evidence strongly supports the existence of three species, H. coronatus, H. cf. coronatus, and H. sindonis, as suggested by Kuiter (2009).

Lourie et al. (1999, 2004), based on the rings supporting the dorsal fin base (DsR), stated H. coronatus had ‘2 + 0 (TrR + TaR)’ and H. sindonis had ‘2 + 1’. However, Jordan and Snyder (1901) described H. sindonis as ‘2 + 0’ and H. coronatus as ‘2 + 1’, which is the reverse. Moreover, all species within the H. coronatus complex described in the present study include ‘2 + 0’ and ‘2 + 1’ forms (Table 2). Thus, DsR is an inappropriate characteristic to diagnose the species studied here. Hippocampus coronatus has only one supraorbital spine whereas H. sindonis has two and H. haema has either one or two spines. Many ichthyologists have attempted to distinguish H. coronatus and H. sindonis based on color and skin filaments (especially Jordan and Snyder 1901). However, Curtis (2006) refuted the use of skin filaments on its key to distinguish H. hippocampus from H. guttulatus, as skin filaments grow irregularly in both species. Lourie et al. (1999) and Szabó et al. (2011) also suggested that color and skin filaments were affected by environment and/or growth, and therefore should be considered of limited diagnostic value. In the present study, several color and skin filament patterns were found in H. haema, which is in agreement with Mitani’s (1956) data for specimens sampled from Maizuru Bay, Japan. This author interpreted these as intraspecific variations, but, given the results obtained in this study by molecular analyses, we do not agree that H. coronatus and H. sindonis should be treated as a single species.

Table 2.
Download as
CSV
XLSX

Meristic and morphometric characters assessed in the species comprising the Hippocampus coronatus complex.

H. haema sp. n. H. coronatus H. sindonis
Present study Present study Temminck and Schlegel (1850) Jordan and Snyder (1901) Lourie et al. (1999) Present study Jordan and Snyder (1901) Lourie et al. (1999)
N 140 28 5 – 7 14 1 6
SL (mm) 15.9–113.9 24.1–133.0 ?–127.0 90.0–115.0 – 30.9–108.3 38.0 –
Counts
TrR 10 10 – 10 10 10 10 10
TaR 35–38 (36) 37–40 (39) – 38–40 38–40 (39) 35–38 (36) 37 36–38 (37)
DsR 2 + 0, 2 + 1 2 + 0, 2 + 1 – 2 + 1 2 + 0 2 + 0, 2 + 1 2 + 0 2 + 1
D 11–14 (13) 12–15 (14) – 13–14 14 11–15 (12) 15 11–15 (12)
A 4 4 – – – 4 – –
P 10–13 (12) 10–13 (12) – 11 12 11–14 (11) 14 12–14
CS 1 1 – – 1 1 – 1
ES 1–2 (1) 1 – – 1 2 2 2
WS 1 1 1 – 1 0 – 0
CoT 4 4 4 – – 5 – –
Measurements
% HL
CHGO 22.7–41.6 (32.2) 43.0–60.1 (51.6) 44.4 42.9 – 26.8–41.0 (33.9) 35.7 –
CHMC 34.1–54.9 (44.5) 55.7–79.0 (67.4) – – – 36.3–55.4 (45.9) – –
SnL 28.8–49.0 (38.9) 35.6–44.2 (39.9) 44.4 42.9 40.0–43.4 (41.7) 28.7–37.2 (33.0) 35.7 30.3–35.7 (33.0)
% SnL
ED 27.1–68.9 (48.0) 32.3–62.9 (47.6) – 33.3 – 41.5–69.0 (55.3) 57.1 –
% TrL
HL 57.3–88.7 (73.0) 56.6–71.3 (64.0) – 60.0–66.7 (63.4) – 57.2–80.1 (68.7) 75.0 –
% TaL
TrL 37.4–57.2 (47.3) 42.6–64.5 (53.6) – 50.0–71.4 (60.7) – 38.3–52.1 (45.2) 50.0 –

N (number of samples), SL (standard length), TrR (trunk rings), TaR (tail rings), DsR (rings supporting dorsal fin), D (dorsal fin rays), A (anal fin rays), P (pectoral fin rays), CS (cheek spine), ES (eye spine), WS (wing-tip spine on dorsal fin base), CoT (tips on corona flat), HL (head length), CHGO (coronet height from gill opening), CHMC (coronet height from mid-point of cleithral ring), SnL (snout length), ED (eye diameter), TrL (trunk length), TaL (tail length). Bracket represents mode in counts and median in measurements

Hippocampus coronatus is ranked as DD in the IUCN Red List due to the lack of information on its population trends and to the uncertainty of its distributions, originating from taxonomic controversies (Zhang and Pollom 2016). Hippocampus sindonis is ranked as Least Concern (LC) because no major threat has been reported for its distribution (Fritzsche et al. 2010). The distribution of H. coronatus is similar to that of H. sindonis (i.e., southeastern coast of Honshu, Japan), and there is no data supporting its potential threat with distribution uncertainty. However, H. coronatus distribution has a narrower range than that of H. sindonis (Fig. 1), so it is more likely to be affected by human pressure. For these reasons, H. coronatus will likely be ranked above or equal to H. sindonis after further surveys of its population trends. To improve the conservation of these species, a better taxonomic understanding is required to resolve the DD rank of H. coronatus regarding the uncertainty of its distribution, as well as more data on its biology, habitat, and abundance. Previous studies considering the biology of H. coronatus conducted on local Korean areas (Choi et al. 2006, 2012; Huh et al. 2014; Park and Kwak 2015), might, in fact, indicate the biology of H. haema. Overfishing could potentially threat H. haema due to by-catch, given the species low density and patchy distribution (Choi et al. 2012; Zhang and Pollom 2016), and its wide distribution requires the study of populations across the entire area.

Table 3.
Download as
CSV
XLSX

Frequency distribution of meristic counts among species within the Hippocampus coronatus complex. Holotypes and lectotypes are marked by an asterisk.

Tail rings
35 36 37 38 39 40 N
Hippocampus haema sp. n. 17 53* 50 18 138
H. coronatus 1 9* 15 3 28
H. sindonis 4 4 4* 2 14
Dorsal fin rays
11 12 13 14 15 N
H. haema 1 22 89 28* 140
H. coronatus 1 6 18* 3 28
H. sindonis 1 8 1 3 1* 14
Pectoral fin rays
10 11 12 13 14 N
H. haema 6 45 65 24* 140
H. coronatus 2 4 18* 4 28
H. sindonis 7 5 1 1* 14
Table 4.
Download as
CSV
XLSX

Pairwise genetic distances between Hippocampus species and the outgroup Syngnathus schlegeli based on multiple loci (cytochrome b, 16S rRNA, and 12S rRNA) and on 12S rRNA only. Asterisks indicate intraspecific pairwise distances calculated from one base pair difference.

Multiple loci 1 2 3 4 5 6 7 8
Hippocampus haema sp. n. (1) 0.000–0.004
H. coronatus (2) 0.025–0.028 0.000–0.001*
H. sindonis (3) 0.075–0.079 0.082 0.000
H. mohnikei (4) 0.104–0.108 0.114–0.115 0.121 –
H. kuda (5) 0.131–0.135 0.139–0.140 0.148 0.110 –
H. reidi (6) 0.134–0.138 0.143–0.144 0.153 0.111 0.020 –
H. ingens (7) 0.131–0.136 0.139–0.140 0.151 0.109 0.031 0.028 –
Syngnathus schlegeli (8) 0.241–0.244 0.247–0.248 0.251 0.232 0.217 0.219 0.231 –
12S rRNA 1 2 3 4 5 6 7 8
Hippocampus haema sp. n. (1) 0.000
H. coronatus (2) 0.015 0.000
H. sindonis (3) 0.042–0.046 0.042–0.045 0.000–0.003*
H. mohnikei (4) 0.049–0.052 0.058 0.042–0.052 0.006
H. kuda (5) 0.074 0.074 0.055–0.058 0.039 –
H. reidi (6) 0.074 0.074 0.074–0.078 0.049–0.052 0.055 –
H. ingens (7) 0.068 0.068 0.071–0.074 0.046–0.049 0.055 0.009 –
Syngnathus schlegeli (8) 0.216 0.208 0.204–0.208 0.211–0.213 0.195 0.180 0.191 –

Key to species of the genus Hippocampus in Korea and Japan

1 No lump on bony body; double gill openings; 10–11 trunk rings 2
– Reddish lumps on fleshy body; single gill opening; 12 trunk rings Hippocampus bargibanti Whitley, 1970
2 11 trunk rings 3
– 10 trunk rings 6
3 Blunt spine or no spine on body 4
– Sharp spine on body Hippocampus histrix Kaup, 1856
4 One blunt cheek spine; trapezoid-shape coronet; no dorsal spot 5
– Two blunt cheek spines; moderately high triangle-shape coronet; no dorsal spot Hippocampus mohnikei Bleeker, 1853
– One recurved and sharp cheek spine; very low triangular coronet (degenerative coronet); three dorsal spots (on the 1st, 4th, and 7th trunk rings) but sometimes absent Hippocampus trimaculatus Leach, 1814
5 Wide body; 34–38 (36) tail rings Hippocampus kuda Bleeker, 1852
– Narrow body; 39–41 (40) tail rings Hippocampus kelloggi Jordan & Snyder, 1901
6 Four tips on corona flat (5th tip degenerated, and separated from the other four); wing-tip spine on dorsal fin base 7
– Five tips on corona flat (5th tip developed, and combined with the other four); no wing-tip spines on dorsal fin base Hippocampus sindonis Jordan & Snyder, 1901
7 37–40 (39) tail rings; coronet height from gill opening 43.0–60.1 % head length; coronet height from mid-point of cleithral ring 55.7–79.0 % head length Hippocampus coronatus Temminck & Schlegel, 1850
– 35–38 (36) tail rings; coronet height from gill opening 22.7–41.6 % head length; coronet height from mid-point of cleithral ring 34.1–54.9 % head length Hippocampus haema sp. n.
*This key was compiled from Lourie et al. (1999, 2004), Senou (2013), Lourie (2016), and the current study data.

Acknowledgements

We sincerely thank J. M. Lee (MarineCom, Korea), S. Rho, G. E. Noh, and S. O. Shin (Haecheonma, Korea), and W. G. Park and J. Y. Bae (PKU, Korea) for specimen donations, S. M. Kweon and H. G. Cho (NIBR, Korea) for NIBR-P specimen loans and photographs, H. Motomura (KAUM, Japan) for KAUM-I specimen loans, R. de Ruiter for photographs and information on RMNH type specimens (RMNH, The Netherlands), J. T. Williams and S. J. Raredon for photographs and information on USNM type specimens (USNM, USA), H. J. Kwun (Marine Biodiversity Institute of Korea, Korea), K. S. Han (Dongwon Institute of Science and Technology, Korea), H. Sugawara, and H. D. Mun for assistance with specimens collection, H. Ayoub for the translation of Fauna Japonica, and R. Fricke (Staatliches Museum für Naturkunde Stuttgart, Germany), M. Norén (Swedish Museum of Natural History, Sweden), and M. van Oijen (RMNH, The Netherlands) for constructive reviews on the manuscript. This research was supported by the Marine Fish Resources Bank of Korea (MFRBK) under the Ministry of Oceans and Fisheries, Korea (http://www.mof.go.kr).

References

  • Araga C (1984) Family Syngnathidae. In: Masuda H, Amaoka K, Araga C, Uyeno T, Yoshino T (Eds) The fishes of the Japanese Archipelago. Tokai University Press, Tokyo, 84–88 (v. 1), pls. 76–77, 343 (v. 2). [In Japanese]; 85–89 (v. 3). [In English]
  • Bauchot ML, Whitehead PJP, Monod T (1982) Date of publication and authorship of the fish names in Eydoux & Souleyet’s zoology of La Bonite, 1841–1852. Cybium 6: 59–73.
  • Bleeker P (1853) Bijdrage tot de kennis der ichthyologische fauna van Japan. Verhandelingen der Koninklijke Akademie van Wetenschappen (Amsterdam) 1: 1–16.
  • Briggs JC (1995) Global biogeography. Elsevier, 452 pp.
  • Boeseman M (1947) Revision of the fishes collected by Burger and von Siebold in Japan. Zoologische Mededelingen (Leiden) 28: 1–242, 5 pls.
  • Burgess WE, Axelrod HR (1972) Fishes of southern Japan and the Ryukyus: Pacific marine fishes (book 1). T. F. H. Publications, Inc., 280 pp.
  • Choi Y, Kim JH, Park JY (2002) Marine fishes of Korea. Kyohaksa, Seoul, 646 pp. [In Korean]
  • Choi YU, Rho S, Jung MM, Lee YD, Noh GA (2006) Parturition and early growth of crowned seahorse, Hippocampus coronatus in Korea. Korean Journal of Aquaculture 19(2): 109–118. [In Korean]
  • Choi YU, Rho S, Park HS, Kang DH (2012) Population characteristics of two seahorses, Hippocampus coronatus and Hippocampus mohnikei, around seagrass beds in the southern coastal waters of Korea. Ichthyological Research 59(3): 235–241. https://doi.org/10.1007/s10228-012-0285-z
  • Chyung MK (1977) The fishes of Korea. Iljisa, Seoul, 728 pp. [In Korean]
  • Compton JA, Thijsse G (2013) The remarkable P. F. B. von Siebold, his life in Europe and Japan. Curtis’s Botanical Magazine 30(3): 275–314. https://doi.org/10.1111/curt.12047
  • Foster R, Gomon MF (2010) A new seahorse (Teleostei: Syngnathidae: Hippocampus) from south-western Australia. Zootaxa 2613(1): 61–68.
  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
  • Han SY, Lee JM, Kim JK (2014) New record of the short-tailed pipefish, Microphis brachyurus brachyurus (Teleostei: Syngnathidae), with a key to the species of the family Syngnathidae from Korea. Ocean Science Journal 49(4): 419–424. https://doi.org/10.1007/s12601-014-0039-0
  • Huh SH, Park JM, Kwak SN, Seong BJ (2014) Abundances and feeding habits of Hippocampus coronatus in an eelgrass (Zostera marina) bed of Dongdae Bay, Korea. Journal of the Korean society of Fisheries Technology 50(2): 115–123. [In Korean]
  • Hwang SD (1998) Diel and seasonal variations in species composition of fishery resources collected by a bag net off Kogunsan-gundo. Korean Journal of Ichthyology 10(2): 155–163. [In Korean]
  • Hwang SD, Im YJ, Kim YC, Cha HK, Choi SH (1998) Fishery resources off Youngkwang. 1. Species composition of catch by a stow net. Korean Journal of Fisheries and Aquatic Sciences 31(5): 727–738. [In Korean]
  • Hwang SW, Hwang HB, Noh HS, Lee TW (2005) Seasonal variation in species composition of fish collected by a bag net in the Geum River estuary, Korea. Korean Journal of Fisheries and Aquatic Sciences 38(1): 39–54. https://doi.org/10.5657/kfas.2005.38.1.039 [In Korean]
  • Ishizu M, Itoh S, Tanaka K, Komatsu K (2017) Influence of the Oyashio Current and Tsugaru Warm Current on the circulation and water properties of Otsuchi Bay, Japan. Journal of Oceanography 73(1): 115–131. https://doi.org/10.1007/s10872-016-0383-z
  • Jordan DS, Tanaka S, Snyder JO (1913) A catalogue of the fishes of Japan. Journal of the College of Science, Tokyo Imperial University 33(1): 1–497, 396 figs.
  • Kawahara R, Miya M, Mabuchi K, Lavoué S, Inoue JG, Satoh TP, Kawaguchi A, Nishida M (2008) Interrelationships of the 11 gasterosteiform families (sticklebacks, pipefishes, and their relatives): a new perspective based on whole mitogenome sequences from 75 higher teleosts. Molecular Phylogenetics and Evolution 46(1): 224–236. https://doi.org/10.1016/j.ympev.2007.07.009
  • Kohno H, Kanou K, Yokoo T (2011) A photographic guide to the fishes in Tokyo bay. Heibonsha, Tokyo, 376 pp. [In Japanese]
  • Kim IS, Lee WO (1995) First record of the seahorse fish, Hippocampus trimaculatus (Pisces: Syngnathidae) from Korea. Korean Journal of Zoology 38(1): 74–77.
  • Kim YU, Myoung JG, Kim YS, Han KH, Kang CB, Kim JK, Ryu JH (2001) The marine fishes of Korea. Hanguel, Busan, 382 pp. [In Korean]
  • Kim IS, Choi Y, Lee CL, Lee YJ, Kim BJ, Kim JH (2005) Illustrated book of Korean fishes. Kyohaksa, Seoul, 615 pp. [In Korean]
  • Kim SY, Kweon SM, Choi SH (2013) First record of Hippocampus sindonis (Syngnathiformes: Syngnathidae) from Korea. Korean Journal of Ichthyology 25(1): 41–44.
  • Kim TI, Han WM, Lee GE, Lee KW (2016) Taxonomical reexamination and distribution of sea horses in the Southern Sea of South Korea. Studies on Education of Fisheries and Marine Sciences 28(4): 1159–1170. https://doi.org/10.13000/JFMSE.2016.28.4.1159
  • Kim JK, Ryu JH (2017) Distribution map of sea fishes in Korea, public edn. Mapledesign, Busan. [In Korean]
  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16(2): 111–120. https://doi.org/10.1007/BF01731581
  • Kuiter RH (2009) Seahorses and their relatives. Aquatic Photographics, Seaford, Victoria, Australia, 276 pp.
  • Lee TW, Seok KJ (1984) Seasonal fluctuations in abundance and species composition of fishes in Cheonsu Bay using trap net catches. The Journal of the Oceanological Society of Korea 19(2): 217–227. [In Korean]
  • Lourie SA, Vincent ACJ, Hall HJ (1999) Seahorses: an identification guide to the world’s species and their conservation. Project Seahorse, 214 pp.
  • Lourie SA (2003) Measuring seahorses. Project Seahorse Technical Report No. 4, Version 1.0. Project Seahorse, Fisheries Centre, University of British Columbia, 15 pp.
  • Lourie SA, Foster SJ, Cooper EWT, Vincent ACJ (2004) A guide to the identification of seahorses. Project Seahorse and TRAFFIC North America, University of British Columbia and World Wildlife Fund, Washington D. C., USA, 114 pp.
  • Lourie SA, Vincent ACJ (2004) A marine fish follows Wallace’s Line: the phylogeography of the three‐spot seahorse (Hippocampus trimaculatus, Syngnathidae, Teleostei) in Southeast Asia. Journal of Biogeography 31(12): 1975–1985. https://doi.org/10.1111/j.1365-2699.2004.01153.x
  • Lourie SA, Pollom RA, Foster SJ (2016) A global revision of the seahorses Hippocampus Rafinesque 1810 (Actinopterygii: Syngnathiformes): Taxonomy and biogeography with recommendations for further research. Zootaxa 4146(1): 1–66. https://doi.org/10.11646/zootaxa.4146.1.1
  • Matsubara K (1955) Fish morphology and hierarchy. I. Ishizaki Shoten, Tokyo, 789 pp. [289 figs] [In Japanese]
  • Mees GF (1962) A preliminary revision of the Belonidae. Zoologische Verhandelingen 54(1): 1–92.
  • Mitani F (1956) Notes on the individual variations of form and coloration of seahorses, Hippocampus coronatus T. & S.. The Zoological Society of Japan 65(2): 66–73. [In Japanese]
  • Mori T (1928) A catalogue of the fishes of Korea. Journal of the Pan-Pacific Research Institution 3(3): 2–8.
  • Mukai T, Tsuihiji T, Sato T, Morisawa M (2000) Mitochondrial DNA divergence in the seahorse, Hippocampus coronatus (Syngnathiformes: Syngnathidae), collected from Sagami Bay. Japanese Journal of Ichthyology 47(2): 139–143. [In Japanese]
  • Myoung JG, Kim BI, Lee SM, Jeon GB (2002) The sea fishes of Korea. Darakwon, Seoul, 287 pp. [In Korean]
  • Nakabo T (2009) Zoogeography and systematics of shallow water marine East Asian fishes. Korean Journal of Ichthyology 21: 38–43.
  • Nakamura S (1999a) Hanatatsu. In: Glover TA (Ed.) Glover Atlas: Fishes of Southern and Western Japan edited by T. A. Glover during 1912 to 1933. Web electronic publication. Faculty of Fisheries, Nagasaki University and Nagasaki University Library, Nagasaki, no. 124. [In Japanese] http://oldphoto.lb.nagasaki-u.ac.jp/GloverAtlas/
  • Nakamura S (1999b) Tatsunootoshigo. In: Glover TA (Ed.) Glover Atlas: Fishes of Southern and Western Japan edited by T. A. Glover during 1912 to 1933. Web electronic publication. Faculty of Fisheries, Nagasaki University and Nagasaki University Library, Nagasaki, no. 125–126. [In Japanese] http://oldphoto.lb.nagasaki-u.ac.jp/GloverAtlas/
  • Nofuji T, Ebihara A, Hammeke LE, Miyazaki K (2013) The letter from Bürger to Siebold in 1831. Bulletin of the Kyushu University Museum 11: 19–52. [In Japanese]
  • Okada Y, Matsubara K (1938) Keys to the fishes and fish-like animals of Japan. Sanseido, Tokyo, 584 pp. [In Japanese]
  • Park JM, Kwak SN (2015) Length–weight relationships and reproductive characteristics of the crowned seahorse (Hippocampus coronatus) in eelgrass beds (Zostera marina) of Dongdae Bay, Korea. Marine Biology Research 11(2): 209–213.
  • Scales H (2009) Poseidon’s steed: the story of seahorses, from myth to reality. Penguin, New York, 288 pp.
  • Senou H (1993) Syngnathidae. In: Nakabo T (Ed.) Fishes of Japan with pictorial keys to the species.Tokai University Press, Tokyo, 478–489, 1293–1295. [In Japanese]
  • Senou H (2000) Syngnathidae. In: Nakabo T (Ed.) Fishes of Japan with pictorial keys to the species, 2nd edn.Tokai University Press, Tokyo, 520–536, 1509–1515. [In Japanese]
  • Senou H (2002) Syngnathidae. In: Nakabo T (Ed.) Fishes of Japan with pictorial keys to the species, English edn.Tokai University Press, Tokyo, 520–536, 1506–1510.
  • Senou H, Kodato H, Nomura T, Yunokawa K (2006) Coastal fishes of Ie-jima Island, the Ryukyu Islands, Okinawa, Japan. Bulletin of the Kanagawa Prefectural Museum, Natural Science 35: 67–92.
  • Senou H (2013) Syngnathidae. In: Nakabo T (Ed.) Fishes of Japan with pictorial keys to the species, 3rd edn.Tokai University Press, Kanagawa, 615–635, 1909–1913. [In Japanese]
  • Sherborn CD, Jentink FA (1895) On the dates of the Parts of Siebold’s ‘Fauna Japonica’ and Giebel’s ‘Allgemeine Zoologie’ (first edition). Proceedings of the Zoological Society of London 1895: 149–150. https://doi.org/10.1016/j.gene.2014.03.040
  • Song HY, Mabuchi K, Satoh TP, Moore JA, Yamanoue Y, Miya M, Nishida M (2014) Mitogenomic circumscription of a novel percomorph fish clade mainly comprising “Syngnathoidei”(Teleostei). Gene 542(2): 146–155. https://doi.org/10.1016/j.gene.2014.03.040
  • Szabó Z, Kimokeo BK, Toonen RJ, Randall JE (2011) On the status of the Hawaiian seahorses Hippocampus hilonis, H. histrix and H. fisheri (Syngnathidae). Marine Biology Research 7(7): 701–709. https://doi.org/10.1080/17451000.2011.558096
  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30(12): 2725–2729. https://doi.org/10.1093/molbev/mst197
  • Temminck CJ, Schlegel H (1850) Pisces. In: von Siebold PF (Ed.) Fauna Japonica, sive descriptio animalium quae in itinere per Japoniam suscepto annis 1823–30 collegit, notis observationibus et adumbrationibus illustravit P.F. von Siebold. Last part. Apud A. Arnz et socios, Lugduni Batavorum (Leiden), 270–324.
  • Wang X, Zhang Y, Zhang H, Meng T, Lin Q (2016) Complete mitochondrial genome sequence of the longsnout seahorse Hippocampus reidi (Ginsburg, 1933; Gasterosteiformes: Syngnathidae). Mitochondrial DNA Part A 27(2): 1401–1402. https://doi.org/10.3109/19401736.2014.947600
  • Yoshino Y, Senou H (2008) Sea fishes of Japan. Yama-kei Publishers co. , Ltd., Tokyo, 545 pp. [In Japanese]
  • Zhang H, Zhang Y, Lin Q (2015) Complete mitochondrial genome of the pacific seahorse Hippocampus ingens Girard, 1858 (Gasterosteiformes: Syngnathidae). Mitochondrial DNA 26(5): 755–756. https://doi.org/10.3109/19401736.2013.850680
  • Zhang Z, Chen Z, Zhao L, Song N, Gao T (2017) Complete mitochondrial DNA genome of Hippocampus mohnikei (Gasterosteiformes: Syngnathidae). Mitochondrial DNA Part A 28(1): 127–128. https://doi.org/10.3109/19401736.2015.1111354
login to comment