Introduction

Dragonets of the family Callionymidae (Pisces: Teleostei) are a group of benthic living fishes occurring in the upper 900 metres of all temperate, subtropical and tropical oceans of the world, with a few species found in estuarine and freshwater habitats. They are characterised by a depressed body, a triangular head when seen from above, large eyes situated dorsally on the head, the presence of a preopercular spine bearing additional points and/or serrae, gill opening reduced to a small pore, swimbladder absent, two dorsal fins, the first with thin, flexible spines, the second with soft rays, and jugular pelvic fins which are separated from each other but each connected with the pectoral-fin base by a membrane.

The Indo-Pacific species of the family were revised by Fricke (1983a), who distinguished 126 valid species from the area. Fricke (2002), in a checklist of the callionymid fishes of the world, listed a total of 182 valid species in 10 genera. Subsequently, 16 additional species and one new genus were described [Callionymus kanakorum Fricke, 2006 and Protogrammus antipodum Fricke, 2006 from New Caledonia (Fricke 2006), the genus Tonlesapia with Tonlesapia tsukawakii Motomura & Mukai, 2006 from Cambodia (Motomura & Mukai 2006), T. amnica Ng & Rainboth, 2011 from Vietnam (Ng & Rainboth 2011), Synchiropus tudorjonesi Allen & Erdmann, 2012 from Papua, Indonesia (Allen & Erdmann 2012), Callionymus profundus Fricke & Golani, 2013 from the northern Red Sea (Fricke & GOLANI 2013), Callionymus madangensis Fricke, 2014 from Papua New Guinea (Fricke 2014), Diplogrammus paucispinis Fricke & Bogorodsky in Fricke, Bogorodsky & Mal, 2014 from the eastern Red Sea (Fricke et al. 2014a), Callionymus omanensis Fricke, Jawad & Al-Mamry, 2014 from the northwestern Indian Ocean (Fricke et al. 2014b), Protogrammus alboranensis Fricke, Ordines, Farias & García-Ruiz, 2016 from the southwestern Mediterranean Sea (Farias et al. 2016), Callionymus alisae Fricke, 2016 from New Ireland (Fricke 2016a), Callionymus petersi Fricke, 2016 from New Ireland (Fricke 2016b), Synchiropus novaehiberniensis Fricke, 2016 from New Ireland (Fricke 2016c), Synchiropus sycorax Tea & Gill, 2016 from the Philippines (Tea & Gill 2016), Callionymus boucheti Fricke, 2017 from New Ireland (Fricke 2017), Callionymus vietnamensis Fricke & Vo, 2018 from Vietnam (Fricke & VO 2018)]; Synchiropus apricus (McCulloch, 1926) was removed from the synonymy of Synchiropus phasis (Günther, 1880) by Gomon & Yearsley (2008), and Eleutherochir mccaddeni Fowler, 1941 was removed from the synonymy of E. opercularis (Valenciennes in Cuvier & Valenciennes, 1837) by Yoshigou et al. (2006), bringing the worldwide total to 201 species in the family (Fricke et al. 2022a).

The genus Yerutius Whitley, 1931 was originally described by Whitley (1931: 115) based on Callionymus apricus McCulloch, 1926 as the type species (by original designation). The type species was synonymised with Synchiropus phasis (Günther, 1880) by Fricke (1983a: 572; 2002: 63), but removed from synonymy and resurrected by Gomon & Yearsley (2008) (see above). Species of Yerutius were classified by Nakabo (1982) in the genus Foetorepus Whitley, 1931.

Fricke (1981: 26) defined the subgenus Synchiropus (Yerutius) within the genus Synchiropus Gill, 1859, which equalled part of the genus Foetorepus (not Whitley, 1931) of Nakabo (1982), and included two species, S. phasis (Günther, 1880) (Fricke 1981) from southern Australia and New Zealand and S. atrilabiatus (Garman, 1899) from the eastern Pacific. Fricke (2002: 102) distinguished seven species in this subgenus, also including Synchiropus agassizii (Goode & Bean, 1888) from the western Atlantic, S. dagmarae Fricke, 1985 from the southwestern Atlantic, S. goodenbeani (Nakabo & Hartel, 1999) from the northwestern Atlantic, S. phaeton (Günther, 1861) from the northeastern Atlantic and Mediterranean and S. valdiviae (Trunov, 1981) from Walvis Ridge, southeastern Atlantic.

Species of the complex live on deep soft bottoms; they usually do not bury in the substrate but are well camouflaged due to their cryptic colouration. Callionymid fishes typically occur in harem groups, with one male controlling a larger home range and living together with several females. Spawning usually takes place around dusk; the courting pair ascends and releases the eggs well above the ground, following a complex courtship behaviour where the spreading of the first dorsal fin or flashing blue ‘lights’ (iridescent blue spots) are frequent motor patterns. The eggs and larvae are pelagic; during transition into juveniles they shift to a benthic lifestyle (Fricke et al. 2014b).

In a revision of the Synchiropus agassizii species complex, Fricke (1985: 247) noted that the tropical West African form of S. phaeton seemed different and might be based on a different taxon, but that its formal recognition and description would have needed more material. During the cruise Bissau 2019 in November/December 2019, several specimens of this new species were collected, as well as two additional specimens collected in Angola by Research Vessel “Dr. Fridtjof Nansen” in 2003; the new species is described, and the subgeneric complex reviewed, in the present paper.

Material and methods

The data of the holotype are given first, followed by those of the paratypes in brackets. Methods follow Fricke (1983a); fin-ray counts follow Fricke (1983b); osteological nomenclature follows Nakabo (1983). The starting point for length measurements is the middle of the upper lip. The standard length (measured from the tip of the upper lip to the middle of the urohyal/caudal fin base) is abbreviated SL. The predorsal (1) length is measured from the middle of the upper lip to the base of the first spine of the first dorsal fin; the predorsal (2) length correspondingly to the base of the first ray of the second dorsal fin. The last ray of the second dorsal and anal fins is always divided at its base; counts in the key include this divided ray as one. In identification keys, males and females are keyed out separately only if there are significant differences between male and female morphology and colouration, and if females of two different species are more similar to each other than to the males of the same species. In callionymid fishes, sexes are easily externally distinguished by the presence of an enlarged urogenital papilla in the male (small or absent in the female).

Species classification is based on Fricke (2002). Nomenclature follows Fricke et al. (2022b). References and journals follow Fricke (2022) and Fricke & Eschmeyer (2022a), respectively.

Molecular analyses: A piece of the right pectoral fin was removed from fresh specimens and preserved in 96% ethanol. A total of three samples of Synchiropus flavistrigatus sp. n. were used for molecular analyses. In addition, three samples of S. phaeton were also analysed, which were collected from bottom trawl sampling carried out at a mean depth of 357 m during the MEDITS_ES05_20 survey around the Balearic Islands (39°17′0.6″N 2°25′47.2″E), western Mediterranean, in June 2020.

DNA was extracted from this tissue using the DNeasy Blood and Tissue Extraction kit (Qiagen, West Sussex, UK). Polymerase chain reaction (PCR) was used to amplify two partial mitochondrial genes: cytochrome c Oxidase subunit I (COI; DNA barcode) with primers FF2d/FR1d (Ivanova et al. 2007) and the 12s rRNA with primers 12SL1091/12SH1478 (Kocher et al. 1989). PCR was performed in a 25 µl volume: 17.7µl ddH2, 2.5µl Mangobuffer (Bioline), 1 µl DNTPs, 1.75 µl MgCl2, 0.5 µl of each primer (each 10 pmol), 0.05 µl TAQ (Bioline) and 1 µl DNA. The PCR thermal profile used for both mitochondrial genes was: initial stage at 96 °C for 5 min; then 35 cycles at 94 °C for 60 seconds, 50/54 °C for 60 seconds and 72 °C for 60 seconds, followed by a final extension at 72 °C for 10 min. PCR products were purified using the QIAquickR PCR Purification Kit (QIAGEN). Both heavy and light strands were sequenced on an ABI 3130 sequencer (Applied Biosystems).

Sequences were imported into BioEdit 7.0.5.2. (Hall 1999) and checked for quality and accuracy with nucleotide base assignment. Multiple sequence alignments (MSA) were obtained with ClustalW (Thompson et al. 1994). The DNA sequences obtained were deposited in the GenBank database ( http://www.ncbi.nlm.nih.gov/genbank/) under the following numbers: ON391145-0N391150 for COI and ON398520-ON398525 for 12s rRNA.

Additionally, GenBank was searched for all species belonging to the genus Synchiropus, considering at least the same resulting length of the two sequenced mitochondrial fragments.

The genetic distance (p-distance) and number of base differences between pairs of sequences of each mitochondrial fragment were calculated with MEGA v.7.1 (Tamura et al. 2013). The sequences were also used to reconstruct the phylogenetic relationships of the new species with the rest of the species included here. To do so, phylogenetic trees based on Maximum Likelihood (ML) were reconstructed. The optimal substitution model of molecular evolution for COI was the Hasegawa-Kishino-Yano model with invariable sites and gamma distribution (HKY+G+I; Hasegawa et al. 1985), while for the 12s rRNA fragment Kimura 2-parameter was used (Kimura 1980). These models were selected following the Akaike Information Criterion (AIC) using MEGA. ML trees were also performed with MEGA and assessed by non-parametric bootstrapping (1000 replicates). The species Callionymus enneactis Bleeker, 1879 (GenBank ID for complete mitochondrial genome AP012316; Song et al. 2014) was included as an outgroup for both phylogenetic trees.

Materials: Materials of the new species and comparative materials are listed below. Abbreviations of museum collections (see below) follow Fricke & Eschmeyer (2022b). Type specimens are deposited in the Colección de Fauna Marina, Instituto Español de Oceanografía, Centro Oceanográfico de Málaga, Málaga, Spain (CFM-IEOMA), the Hebrew University of Jerusalem, Israel (HUJ), and Staatliches Museum für Naturkunde Stuttgart, Germany (SMNS).

Comparative material [subgenus Synchiropus (Yerutius): Synchiropus agassizii: MCZ 86660 (holotype of Callionymus agassizii Goode & Bean, 1888 and Callionymus himantophorus Goode & Bean, 1896), Barbados; ROM 36864 (1), Barbados; ROM 36865 (1), Barbados; ROM 3686 (1), Barbados; USNM 188529 (8), Honduras. Synchiropus atrilabiatus: CAS-SU 25249 (1 syntype of Callionymus atrilabiatus Garman, 1899), Panama, Panama Bay; CAS-SU 5746 (holotype of Callionymus garthi Seale, 1940), Colombia, Port Utria; USNM 144258 (holotype of Synchiropus talarae Hildebrand & Barton, 1949), Peru, Talara; CAS 44015 (1), Costa Rica, Golfo de Nicoya; CAS 44026 (1), Costa Rica, Golfo de Nicoya; CAS 44114 (32), Costa Rica, Quepos; CAS 44124 (46), Costa Rica, Quepos; CAS 44136 (2), Costa Rica, Golfo de Nicoya; CAS 46429 1), Panama, Hannibal Bank; CAS 46947 (2), Costa Rica, Cabo Blanco; CAS-SU 19393 (32), Mexico, Baja California Sur, Gorda Banks; CAS-SU 25249 (1), Panama; CAS-SU 46428 (21), Mexico, Baja California Sur, Gorda Banks; CAS-SU 46430 (1), Mexico, Baja California Sur, Gorda Banks; CAS-SU 46431 (2), Mexico, Baja California Sur, Gorda Banks; GCRL 10682-1329 (1), Panama; LACM 20681-1 (1), Ecuador, Galapagos Islands; LACM 32269-4 (2), Costa Rica, Cocos Island; LACM 32556-1 (7) Costa Rica, Isla de Cano; SIO 68-55 (3), Mexico, Baja California Sur; ZMUC P64158 (2), Panama, Gulf of Panama. Synchiropus dagmarae: USNM 188521 (holotype), Venezuela, off mouth of Orinoco River; USNM 256454 (10 paratypes), Venezuela, off mouth of Orinoco River; ISH 1088/6 (1), Uruguay, off east coast; ISH 1775/68 (1), Brazil, off Rio Grande do Sul; ISH 1983/68 (3), Brazil, off Rio de Janeiro; NSMT-P 22380 (2), Suriname; NSMT-P 22381 (1), Suriname; NSMT-P 22382 (3), Suriname; NSMT-P 22383 (2), Suriname; NSMT-P 22384 (1), Suriname; NSMT-P 22385 (2), Suriname; NSMT-P 22386 (1), Suriname; NSMT-P 22387 (30), Suriname; NSMT-P 22391 (13), Suriname; SMNS 9068 (3), Suriname; SMNS 9069 (1), Suriname. Synchiropus goodenbeani: MCZ 95955 (holotype of Synchiropus goodenbeani), USA, New York, Long Island; BMNH 1933.10.12.85 (1 paratype of Synchiropus goodenbeani, USA, Florida, Dry Tortugas); MCZ 38492 (1 paratype of Synchiropus goodenbeani), USA, mid-Atlantic Bight; USNM 44607 (1 paratype of Callionymus himantophorus Goode & Bean, 1896), USA, off Florida, Gulf of Mexico; SMNS 8465 (1), USA, New York. Synchiropus phaeton: NMW 58817 (1 syntype of Callionymus phaeton Günther, 1861), Italy, Rome; BMNH 1952.5.26.11 (1), Italy, Elba; BMNH 1972.1.10.66-71 (6), Morocco, off Casablanca; BMNH 1978.1.17.62 (1), Tunisia; HUJ 8036 (1), Israel; HUJ 8075 (1), Italy, Lampedusa; HUJ 8077 (3), Israel, Hadera; HUJ 8078 (2), Israel; HUJ 8079 (11), Cyprus; HUJ 8087 (1), Israel; HUJ 8092 (5), Israel; HUJ 8095 (1), Malta; HUJ 8387 (1), Cyprus; HUJ 9134 (5), Malta; HUJ 15041 (4), Israel; HUJ 16432 (1), Israel; HUJ 17110 (1), Israel; HUJ 17607 (1), Israel; HUJ 18650 (1), Israel; HUJ 20683 (1), Spain, Balearic Islands; HUJ 20698 (1), Spain, Balearic Islands, Mallorca; HUJ 20813 (2), Spain, Balearic Islands, Menorca; MSNG 43609 (4), Italy, San Remo; NMW 77229 (1), Italy, Gulf of Genoa; NMW 77230 (1), France, Nice; SMNS 15282 (1), France, Banyulssur-Mer. Synchiropus phasis: BMNH 1879.5.14.564 (holotype of Callionymus phasis Günther, 1880), Australia, New South Wales, Eden; AMS E.5714 (2), Australia, Victoria, Gippsland; AMS I.18794-001 (10), Australia, New South Wales, Wollongong; AMS I.18795-007 (2), Australia, New South Wales, Wollongong; BMNH 1937.9.21.28 (1), Australia, Tasmania; LACM 11516-5 (1), Australia, Victoria, off Bairnsdale; NMW 58774 (1), Australia, South Australia; Gulf of Saint Vincent. Synchiropus valdiviae: ZISP 45303 (1 paratype of Callionymus valdiviae Trunov, 1981), southeastern Atlantic, Valdivia Bank.

Taxonomy

Fig. 1.

Synchiropus flavistrigatus sp. n., SMNS 27157, holotype, 111.7 mm SL, male, eastern Atlantic Ocean, Guinea-Bissau, 230 km southwest of Bissau. A. Lateral view, left side (scale indicates 5 mm). B. Left preopercular spine (scale indicates 1 mm). CFM-IEOMA 7442, paratype, specimen 2, female (88.5 mm SL), eastern Atlantic Ocean, Guinea-Bissau, 213 km southwest of Bissau. C. Lateral view, left side (scale indicates 5 mm); D. Left preopercular spine (scale indicates 1 mm).

Table 1.

Synchiropus flavistrigatus sp. n., SMNS 27157, holotype, male, 111.7 mm SL (= standard length), eastern Atlantic Ocean, Guinea-Bissau, 230 km southwest of Bissau. Meristic data and proportions.

Table 2.

Synchiropus flavistrigatus sp. n., paratypes, eastern Atlantic Ocean, Guinea-Bissau. Proportions. SL = standard length.

Fig. 2.

Synchiropus flavistrigatus sp. n., female specimen, eastern Atlantic Ocean, Guinea-Bissau, 230 km southwest of Bissau. Live colouration. Lateral view. (Photograph: F. ORDINES)

Fig. 3.

Geographical distribution of the genus Synchiropus in the Atlantic Ocean. A. Synchiropus flavistrigatus sp. n., type locality. B. Synchiropus flavistrigatus sp. n., other localities. C. S. agassizii. D. S. dagmarae. E. S. goodenbeani. F. S. phaeton. G. S. valdiviae.

Table 3.

Synchiropus phaeton, proportions (as percentage of standard length). Examined males: HUJ 8077 (1), HUJ 8092 (2), HUJ 8099 (6), HUJ 8387 (1), HUJ 9134 (3), HUJ 18650 (1), HUJ 20683 (1), HUJ 20813 (1), SMNS 15282 (1). Examined females: HUJ 8077 (2), HUJ 8078 (2), HUJ 8092 (1), HUJ 8099 (5), HUJ 9134 (2), HUJ 17110 (1), HUJ 20698 (1), HUJ 20813 (1).

Fig. 4.

Synchiropus phaeton, female specimen, western Mediterranean Sea, Balearic Islands, Menorca Channel, 40°03.52′N 3°12.35′E–40°03.73′N 3°18.44′E, 155–214 m depth. Live colouration. Lateral view. (Photograph: M. FORTEZA SALOM)

Table 4.

Comparison of the Atlantic species of Synchiropus, with values different from those of S. flavistrigatus sp. n. in bold font. Abbreviations: A = anal fin; D1 = first dorsal fin; D2 = second dorsal fin; P1 = pectoral fin; SL = standard length.

Table 5.

Comparison of Synchiropus flavistrigatus sp. n. with the Indo-Pacific species of Synchiropus (Yerutius), with values different from those of the new species in bold font. Abbreviations: A = anal fin; D1 = first dorsal fin; D2 = second dorsal fin; P1 = pectoral fin; SL = standard length.

Table 6.

Mean genetic distances (%) and numbers of bp differences for COI barcode fragment of Synchiropus spp., respectively below and above the diagonal.

Discussion

The presence of this new species in the eastern Atlantic of West Africa was already suggested by Fricke (1985), but it took several decades to acquire sufficient material from the area to describe it and separate it from the similar species S. phaeton. This is in part due to the fact that deep-water habitats in that region are rarely sampled, and also to the loss of the examination sheets for eastern Atlantic Synchiropus in a car accident in 1984 (so the work had to be done again, and the material had to be re-examined).

The new species was previously confused with S. phaeton, which is now restricted to the waters off Northwest Africa and the Mediterranean Sea. It lives in similar habitats as S. phaeton, on deep sand or mud bottoms. of the lower continental shelf and upper continental slope. During the BISSAU1219 Survey, a total of 86 bottom trawl samples were obtained from 25 to 900 m depth. In this range, S. flavistrigatus sp. n. was only detected in hauls from 104 to 386 m depth. While in the past, the western Atlantic was thought to harbour a greater diversity of Synchiropus with a total of three species (S. agassizii, S. dagmarae, S. goodenbeani), now we also know three species of the genus from the eastern Atlantic (S. phaeton, S. valdiviae, S. flavistrigatus sp. n.). In contrast, there is just a single species of callionymid known from continental waters of the eastern Pacific (S. atrilabiatus).

Fig. 5.

Phylogenetic relationships based on Maximum Likelihood for COI (A) and 12s rRNA (B) fragments for Synchiropus species. Bootstrap values (%) and GenBank accession numbers are indicated near the nodes and the after species name, respectively. The samples of Synchiropus flavistrigatus sp. n. sequenced here are indicated in bold, while the samples of Synchiropus phaeton are represented by asterisks.

The molecular analyses based on COI and 12s rRNA fragments strongly support the morphological results confirming that S. flavistrigatus sp. n. corresponds to a new species, distinct from S. phaeton. Interspecific divergences between S. flavistrigatus sp. n. and S. phaeton were high for COI (3%) but low for the 12s rRNA fragment (0.5%). The values for the COI fragment exceed the standard threshold for the delimitation of marine fish species, which is around 2% for COI fragments (Hubert et al. 2008). On the other hand, 12s rRNA is a relatively conserved mitochondrial gene evolving more slowly than the mitochondrial genome as a whole (Palumbi 1996). Although there is no clear consensus on the percentage of differences to separate marine fishes, Cawthorn et al. (2012) found that the maximum genetic distance for the species level is 0.5%, which clearly coincides with the interspecific distance for 12s rRNA obtained here.

The phylogenetic analyses of both fragments showed two clearly divergent and close lineages between S. flavistrigatus sp. n. and S. phaeton, which might indicate a recent divergence event, as recorded in other fish genera from the eastern Atlantic and Mediterranean, such as Symphodus tinca (Linnaeus, 1758) vs. remaining species of Symphodus Rafinesque, 1810 (Hanel et al. 2002), Pagellus acarne (Risso, 1827) vs. P. bogaraveo (Brünnich, 1768) (Meynard et al. 2012), or Coris julis (Linnaeus, 1758) vs. C. melanura (Lowe, 1839) (Ramírez-Amaro et al. 2021), but more molecular studies are needed to confirm this.

While Indo-Pacific species of Synchiropus are distributed at all depths between the shallows and 900 m, in the Atlantic only the deep-water subgenus Yerutius mainly occurs at depths below 100 m. In shallow waters, Synchiropus is here replaced by members of the genus Callionymus Linnaeus, 1758.