A unique species of the flappy-snake eel genus, Phyllophichthus diandrus sp. nov., is described based on a single specimen (270 mm in total length) collected from Dong-gang, southwestern Taiwan. The new species possesses several characters that are distinct from the only other species in the genus, Phyllophichthus xenodontus. Phyllophichthus diandrus sp. nov. can be easily distinguished from P. xenodontus by having two papillae inside of nasal tube (vs three in P. xenodontus), 25 branchiostegal rays (vs 29), the dorsal-fin origin positioned behind the tip of the pectoral fin (vs not behind, usually above mid-pectoral fin), and the absence of the maxillary teeth (vs present). The relationship between Phyllophichthus and Leiuranus is discussed based on generic and morphological features.

Biodiversity, fish fauna, ichthyology, marine species, nasal tube, snake eel, taxonomy

The family Ophichthidae (snake eels or worm eels) is the most abundant group of the order Anguilliformes, comprising 365 species in 62 genera. While many species are recognized, most of them are belonging to several major genera, i.e. Apterichtus Duméril, 1805 (20 spp.), Bascanichthys Jordan & Davis, 1891 (19 spp.), Ophichthus Ahl, 1789 (97 spp.), and Scolecenchelys Ogilby, 1897 (20 spp.) (Y. Hibino pers. data). In contrast, several specialized monotypic genera have been discovered, such as Glenoglossa McCosker, 1982, which has an elongate tongue with a shrimp-like tip, and Chauligenion McCosker & Okamoto, 2016, which has a protruding lower jaw.

The genus Phyllophichthus Gosline, 1951 is one of the unique monotypic genera, established for Phyllophichthus xenodontus Gosline, 1951. Gosline’s (1951) work, which included an osteological study, was based on various groups of Ophichthidae. He found specialization of the shape of the anterior nasal tube that has a leaf- or flower-like shaped, posterior extension in Phyllophichthus (Gosline 1951; Hibino and Kimura 2016; Hibino 2020). In addition, Phyllophichthus has an acute, straight snout, as well as relatively simple sensory canals on the head.

During a survey in recent decades by our team of the snake-eel fauna of Taiwan, one particular specimen was collected that was initially identified as Phyllophichthus sp. by Hibino (2019), who suggested the possibility of it being an undescribed species but also noted a potential abnormality in the lower jaw. After careful re-examination, we have determined it to be the second species within the genus.

All methods for morphological measurements follow Hibino et al. (2019). Measurements for total and tail lengths are taken by 300 or 600 mm rulers and others by a digital caliper to the nearest 0.1 mm. Osteological observation including counts of vertebrae and branchiostegal rays are based on the radiographs taken by a digital x-ray machine (Dexela CMOS X-ray detector, Model 2315, Dexeal Co. Ltd, UK) in the National Museum of Marine Biology and Aquarium, Pingtung, Taiwan. Total length (TL) and head length (HL) are used throughout for expressing the body proportions.

DNA extraction, polymerase chain reaction (PCR), and sequencing methods followed Weigt et al. (2012). The total DNA was extracted from muscle tissue of samples and amplified partial regions of mitochondrial genes of 16S ribosome RNA (16S) and cytochrome c oxidase subunit I (COI). The primers for PCR and sequence were primer A (5′-GGTCCWRCCTGCCCAGTGA-3′), B (5′-CCGGTCTGRACYAGATCACGT-3′) for 16S (Kurogi 2008) and FISH-BCL (5′-TCAACYAATCAYAAAGATATYGGCAC-3′), FISH-BCH (5′-ACTTCYGGGTGRCCRAARAATCA-3′) for COI (Baldwin et al. 2009). Amplification of the target region was confirmed by gel electrophoresis, DNA was purified by ExoSAP-IT (Applied Biosystems) and sequenced using 3730×l DNA Analyzer (Applied Biosystems). All sequences have been deposited in the DNA Data Bank of Japan (DDBJ) (Table 1).

Partial sequences of 16S (537 bp) and COI (612 bp) obtained present study and retrieved GenBank (Table 1) were aligned by MAFFT v. 7 (Katoh and Standley 2013) and a maximum-likelihood (ML) tree (16S + COI) was constructed by RAxML v. 8 (Stamatakis 2014). The evolutionary model was used GTR+G+I following the best model computing by MEGA 11 (Tamura et al. 2021). The confidence of each branch was evaluated by 1000 bootstrap replications. Scolecenchelys aoki (Jordan & Snyder, 1901) and Muraenichthys hattae Jordan & Snyder, 1901 were used as outgroups.

Specimens examined in this study are deposited in the Kitakyushu Museum of Natural History and Human History, Kitakyushu, Fukuoka, Japan (KMNH VR), National Museum of Marine Biology and Aquarium, Pingtung, Taiwan (NMMB-P), and Museum Support Center of the Smithsonian Institution, Suitland, Maryland, USA (USNM).

 Phyllophichthus diandrus sp. nov.

https://zoobank.org/7134B3C8-04EB-4E43-9761-1AC65F70A8BE

Figs 1, 2A, 3, 4

English name: Bi-stamened Flappy Snake Eel

Chinese name: 雙蕊葉吻蛇鰻

Phyllophichthus sp.: Hibino 2019: 149 (Dong-gang, Taiwan).

Type material

Holotype : NMMB-P28224, 270 mm TL, ca 22°26'N, 120°24'E, Dong-gang, Pingtung, southwestern Taiwan, northern South China Sea, mid-water trawl, 6 Jan. 2017, collected by H.-C. Ho.

Diagnosis

Inside of anterior-nostril tube with two papillae; dorsal-fin origin well behind tip of pectoral fin, distance from the tip to the origin of dorsal fin 0.6 times of the fin; no teeth on maxilla and vomer; 25 branchial aches; vertebral formula 12-69-160.

Description

Measurements in mm (% of TL in parenthesis): HL 22.4 (8.3%); preanal length 128.1 (47.5%); tail length 141.7 (52.5%); predorsal length 29.8 (11.0%); body depth at gill opening 4.7 (1.7%); body depth at mid anus 6.2 (2.3%). Measurements in mm (% of HL) in parenthesis: snout length 5.2 (23.2%); eye diameter 1.8 (8.0%); mouth gape 5.4 (24.1%); interorbital width 1.6 (7.1%); gill opening 1.9 (8.5%); isthmus 2.7 (12.1%); pectoral-fin length 3.2 (14.3%); pectoral-fin base 1.5 (6.7%). Body elongate, slender, trunk cylindrical, compressed toward tip of tail; tip of tail hard and pointed; anus anterior to mid-body, tail 1.9 in total length (Fig. 1).

Figure 1. 

Phyllophichthus diandrus sp. nov., NMMB-P28224, holotype, 270 mm TL, Dong-gang, Taiwan A dorsal view B ventral view C enlarged view of lateral head. Arrows indicate origin of dorsal fin (above) and anus (below).

Head relatively short, 5.7 in preanal length and 12.0 in TL; contour of head smooth, slightly convex in post-temporal; snout acute and relatively pointed in lateral view, narrow from dorsal side; snout long, prominently projected anteriorly; a distinct groove ventrally of snout; mouth inferior, lower jaw short and tip below middle of base of nostril tube, distance between tips of snout and lower jaw more than eye diameter; anterior nostril tubular, towards ventrally, base of both side closed: posterior rim of tube extending posteriorly, forming a broad flap; inside of tube with two papillae (Fig. 2A); posterior nostril a slit opening inside of mouth, concealed by wide dermal flap rolling into mouth completely; eye developed, large, its diameter 2.9 times in snout length; lips smooth without cirri or protrusions, upper lip extending to inner mouth, a curved fold along lower margin of eye; mouth moderate, rictus slightly behind a vertical through posterior margin of eye; interorbital region slightly convex without groove; branchial basket convex; gill opening positioned just anterior to base of pectoral fin.

Figure 2. 

Closed illustration of tubular anterior nostril from ventral view A Phyllophichthus diandrus sp. nov., NMMB-P28224, holotype, 270 mm TL B P. xenodontus, NMMB-P5264 (one of two), 373 mm TL, Taiwan. BF broad flap. Arrows indicate papillae inside of nasal tube.

Teeth small, conical, pointed; no teeth on maxilla and vomer, maxillary region completely covered by an extending upper labial flap (Fig. 3); 6 intermaxillary teeth arranged in two rows but concealed by a dermal structure and not visible; dentary teeth uniserial posteriorly, 17 on left side and 15 on right side.

Figure 3. 

Ventrolateral view of palatal area of Phyllophichthus diandrus sp. nov., NMMB-P28224, holotype, 270 mm TL. DF dermal flap on posterior nostril LF edge of upper labial flap MR maxillary region VR vomerine region.

Sensory pores on head obvious (Fig. 4); supraorbital pores 1 + 3, 1 ethmoid and 3 pores slightly before a level of center of eye; infraorbital pores 3 + 3, first between anterior and posterior nostrils and second anteroventro-corner of eye, third behind center of eye, and remaining on postorbital; preoperculo-mandibular pores 4 + 2; 3 on supratemporal; 1 interorbital pore present; lateral-line pore slightly obscure, nearly completed except tip of tail equal to one third of HL.

Figure 4. 

Lateral view of anterior head of Phyllophichthus diandrus sp. nov., NMMB-P28224, holotype, 270 mm TL. AN anterior-nostril tube IO infraorbital pores M mandibular pores PO preopercular pores SO supraorbital pores ST supratemporal pore. Arrows indicate interorbital (left) and mid-temporal pores (right).

Neurocranium narrow dorsally; dentary stout and recurved; branchiostegal rays developed and deeply overlapped ventrally, 25 in total. Predorsal vertebrae 12, preanal 69, and total 160.

Pectoral fin moderate, shape round, its length 1.6 in snout and 7.0 in HL; medial fins low in height, origin of dorsal fin behind tip of pectoral fin, distance from pectoral fin-tip to dorsal-fin origin 0.6 times of the fin, distance from gill opening to dorsal-fin origin 3.0 in HL; caudal fin absent.

Color in preservation light yellowish brown; abdomen slightly paler but not bicolored distinctly; all fins pale white.

Distribution

Known only by a single specimen from Dong-gang, southwestern Taiwan. Depth range estimated as more than 100 m.

Etymology

The specific name diandrus is the Latin compound adjective “bi-stamened”, referring to the flower-like shaped tubular nostril with two papillae inside.

Based on careful examination of the radiograph images of the holotype, we found no osteological damage on its lower jaw, despite the suspicion of an abnormal condition raised by Hibino (2019). As stated above, Phyllophichthus was known previously only from a single species, P. xenodontus which is widespread in the tropical and subtropical regions in the Indo-Pacific Ocean.

Our species represents the second species in the genus. Phyllophichthus diandrus sp. nov. can be easily distinguished from P. xenodontus by having two papillae inside of nasal tube (vs three in P. xenodontus), 25 branchiostegal rays (vs 29), the dorsal-fin origin behind the tip of the pectoral fin (vs usually above mid-pectoral fin), and an absence of the maxillary teeth (vs present) (McCosker 1977; Smith et al. 2014; this study). Another nominal species, Phyllophichthus macrurus McKay, 1970, described from Western Australia, has been regarded as a junior synonym of P. xenodontus by several authors (McCosker et al. 2006; Smith et al. 2014; McCosker 2022). The dorsal-fin origin of P. macrurus is positioned above posterior two-thirds of the pectoral fin, not behind the fin tip (McKay 1970; this study) and is clearly within the range of P. xenodontus. Thus, we retain this name in the synonymy of P. xenodontus.

Smith et al. (2014) noted that because of the wide range in the vertebral counts there might be several populations present in P. xenodontus. However, due to the small number of specimens, they did not separate them into different taxa. Smith et al. (2014) examined 11 specimens collected from Hawaii (type locality of P. xenodontus), Seychelles, the Red Sea, Taiwan, Solomon Islands, Vanuatu, and the Marquesas Islands. In their description, they clearly stated that P. xenodontus has three papillae inside the nasal tube, the same as the illustration of the holotype provided by Gosline (1951). Five of 11 specimens examined by Smith et al. (2014) were also checked and this character was confirmed by YH. Furthermore, our additional specimens of P. xenodontus from Taiwan (n = 3) and Japan (n = 2) also have characters identical to the holotype.

The genetic distance between P. diandrus sp. nov. and P. xenodontus is high, more than 5% based on a combination of mitochondrial COI and 16S sequences (Fig. 5). Furthermore, P. diandrus sp. nov. exhibits a distinctive characteristic of lacking teeth on the maxilla, a trait that may warrant consideration for the establishment of a new genus in Ophichthidae. However, further investigation with additional specimens and more comprehensive studies are necessary to explore this hypothesis.

Figure 5. 

Maximum likelihood tree of selected genera in subfamily Ophichthinae based on partial COI and 16S sequences, including two Phyllophichthus species.

The genus Phyllophichthus was established by Gosline (1951). While mentioning that its dentition is similar to Leiuranus Bleeker, 1852 (i.e. both genera lack vomerine teeth), he also noted that the condition of the mandibular teeth in Phyllophichthus is unique. McCosker (1977) confirmed Phyllophichthus as a valid genus and suggested that Phyllophichthus is closely related to Leiuranus and Elapsopis Kaup, 1856 in the tribe Ophichthini. McCosker et al. (1989) treated Elapsopis versicolor Richardson, 1848, the only species of Elapsopis, as a member of Leiuranus without further explanation. Leiuranus versicolor has vomerine teeth, free branchial rays, secondary ossification of the fifth ceratobranchial, and the presence of actinosts (McCosker 1977), but other osteological features, including fusion of the upper pharyngeal dermal tooth plates, are consistent with those of Leiuranus semicinctus (Lay & Bennett, 1839).

Based on COI and 16S sequences, Phyllophichthus forms a sister group with Leiuranus, supported by a high bootstrap value. This result supports the hypothesis proposed by McCosker (1977), which was primarily based on osteological analysis. While the shape of the neurocranium (subtruncate) of Phyllophichthus is similar to that of Leiuranus, the expanded appendage of the nasal tube, modified suspensorium, jaws, dentition, and neurocranium (McCosker 1977; this study) are distinct from the former. Consequently, we recognize both Phyllophichthus and Leiuranus as valid genera, each comprising two species.

Fricke et al. (2015) established a new genus and species, Suculentophichthus nasus Fricke, Golani & Appelbaum-Golani, 2015 from a single specimen collected at Eilat, Gulf of Aqaba in the Red Sea. Because of its large tubular nostril they considered the genus to be closely related to Phyllophichthus, distinguishing the two genera by a number of differences, including the shape of the tubular nostril, caudal vertebral counts, the position of the dorsal fin origin, and the presence of supraorbital canal/pores. However, the first three characters are within species-level variation, and there is no difference in the fourth character. It is notable that Phyllophichthus has no protrusions along the upper lip, whereas S. nasus has at least one protrusion (one in the text, but two shown in the illustration). Further work is needed to determine whether Phyllophichthus and Suculentophichthus Fricke, Golani & Appelbaum-Golani, 2015 should be regarded as separatable genera or not.

Phyllophichthus diandrus sp. nov. is unique in having no teeth on the maxilla, which is completely covered by an extending upper labial flap. It is speculated that this species specializes in feeding on soft organisms due to the presence of dentary and intermaxillary teeth.

We appreciate Yo Su (National Kaohsiung University of Science and Technology), Po-Na Lee, Ming-Hua Chiang (NMMB-P), Keita Koeda (University of Ryukyus), Jeffery T. Williams, David G. Smith, Jeffery Clayton, Sandra Raredon, Diane Pitassy, and Chad Walter (USNM) and You Sakurai (Okinawa Environmental Research Co., Ltd.) for providing opportunity to use specimens for this study, and to John Pogonoski (CSIRO) providing the important literature and photo.