Pseudocrangonyx joolaei, Lee & Tomikawa & Nakano & Min, 2020

Lee, Chi-Woo, Tomikawa, Ko, Nakano, Takafumi & Min, Gi-Sik, 2020, A new species of the genus Pseudocrangonyx (Crustacea: Amphipoda Pseudocrangonyctidae) from Simbok Cave, Korea, Zootaxa 4731 (3), pp. 321-334 : 323-333

Pseudocrangonyx joolaei sp. nov.

[New Korean name: sim-bok-dong-gul-yeop-sae-u]

( Figs 2–9 )

urn:lsid:zoobank.org:act:750E9CE7-F762-4C8E-BC76-A0C988F6EAD4

Pseudocrangonyx asiaticus . — Uéno, 1966: 506–518 (in part), fig. 8L, M. — Holsinger, 1989: 954–956 (in part), fig. 4.

Material examined. Holotype: NNIBRIV21629, female ( Fig. 2 ), BL 10.6 mm, collected from Simbok Cave (36°47.13′N, 127°57.76′E), Galgeum-ri, Goesan-gun, Chungcheongbuk-do, Korea, on 24 March 2018, by C.-W. Lee.

Paratypes: NNIBRIV21630, NNIBRIV21631, 1 male, BL 6.0 mm, and 1 female, BL 8.3 mm; collection data same as for holotype .

Type locality. Simbok Cave (36°47.13′N, 127°57.76′E), Galgeum-ri, Goesan-gun, Chungcheongbuk-do, Korea

Diagnosis. Antennal sinus shallow with rounded angle; eyes absent; pereonites 1–6 with short dorsal setae; dorsal margin of urosomite 3 lacking setae; pereonites 2–4 each with sternal gill; antenna 1 being 0.47–0.48 times as long as body length; antenna 2 with calceoli in both sexes; mandible palp article 3 almost as long as article 2; maxilla 1 inner plate with 6 plumose setae; maxilla 2 inner plate with oblique inner row of 6 setae; gnathopods 1 and 2, carpi with serrate setae on posterodistal corners in both sexes; palmar margins of propodi of gnathopods 1 and 2 with 14–18 and 13–20 robust setae, respectively; pleopod peduncles lacking marginal setae, inner margin of inner rami with bifid setae; uropod 1 inner ramus 1.4 times as long as outer ramus, inner and outer margins of inner ramus with 3–4 and 1–3 robust setae, respectively, basal part of inner ramus with 3 slender setae, outer ramus with 2 marginal robust setae; uropod 2 inner ramus 1.2–1.4 times as long as outer ramus, inner and outer margins of inner ramus with 3 and 1–2 robust setae, respectively, outer ramus with 1–2 marginal robust setae; uropod 3 terminal article 0.1 time as long as length of proximal article; telson length 1.2–1.24 time as long as width, cleft for 38.3–45.2%.

Description. Female holotype (NNIBRIV21629): Head ( Fig. 3A ) with short dorsal seta; rostrum short; lateral cephalic lobe rounded; antennal sinus shallow with rounded angle; eyes absent. Pereonites 1–6 with short dorsal setae; dorsal margin of pereonite 7 with long setae. Dorsal margins of pleonites 1–3 with long setae ( Fig. 3B ). Posterior margin of epimeral plate 1 with 7 setae, posteroventral corner with seta; ventral and posterior margins of plate 2 with 3 and 9 setae, respectively, posteroventral corner with seta; ventral and posterior margins of plate 3 with 4 and 7 setae, respectively, posteroventral corner subquadrate with seta ( Fig. 3B ). Dorsal margin of urosomites 1–2 with setae, urosomite 3 lacking dorsal setae. Anteroventral corner of urosomite 1 with seta ( Fig. 3B ).

Antenna 1 ( Fig. 3C ) 0.47 times as long as body length, peduncular articles 1–3 in length ratio of 1.0: 0.6: 0.3; accessory flagellum ( Fig. 3D ) 2-articulate, almost reaching distal part of primary flagellar article 1, terminal article with 4 setae and 2 aesthetascs; primary flagellum 16-articulate, 1 aesthetasc on some articles.

Antenna 2 ( Fig. 3E, F ) 0.74 times as long as antenna 1; peduncular article 5 with 4 calceoli; flagellum 0.70 times as long as peduncular articles 4 and 5 combined, consisting of 9 articles, first 6 each with calceolus.

Mouthparts. Upper lip ( Fig. 3G ) with rounded anterior margin, with fine setae. Mandibles ( Fig. 3 H–J) with left and right incisors with 7- and 5-dentate, respectively; left lacinia mobilis 5-dentate, right lacinia bifid, with many teeth; molar process triturative; accessory setal rows of left and right mandibles each with 7-pectinate setae; palp 3-articulate, article 3 with 5 A-, 17 D-, and 5 E-setae. Lower lip ( Fig. 3K ) with broad outer lobes with fine setae, mandibular process of outer lobe rounded apically; inner lobes indistinct. Maxilla 1 ( Fig. 3 L–N) with inner and outer plates, and palp; inner plate subquadrate with 6 plumose setae; outer plate subrectangular with 7 serrate teeth apically; palp 2-articulate, longer than outer plate, article 2 with weakly plumose robust seta apically, and 4 apical and 4 subapical robust setae. Maxilla 2 ( Fig. 4A ) with oblique inner row of 6 setae on inner plate. Maxilliped ( Fig. 4B, C ) with inner and outer plates, and palp; inner plate subrequtangular with 5 apical robust setae; outer plate suboval with 8 apical plumose setae, 2 subapical robust setae, and some medial setae; palp 4-articulate, medial margin of article 2 lined with setae, article 4 with nail.

Gnathopod 1 ( Fig. 4D ) with subquadrate coxal plate, bearing setae on anterior margin and anterodistal corner, width 1.5 times as long as depth; basis thick and short, anterior margin bare, posterior margin with 16 setae; posterodistal corner of carpus with 3 serrate robust setae; propodus stout, subtriangular, palmar margin with 18 robust setae in 2 rows, some distally notched; posterior margin of dactylus dentate ( Fig. 4E ).

Gnathopod 2 ( Fig. 4F ) with rounded coxal plate, with setae on its anterior to ventral margins, width 1.3 times as long as depth; basis slender with short setae on anterior margin and submargin, posterior margin with long setae; posterodistal corner of carpus with 2 serrate robust setae; propodus slender than that of gnathopod 1, palmar margin with 20 robust setae in 2 rows, some distally notched; posterior margin of dactylus dentate ( Fig. 4G ).

Pereopod 3 ( Fig. 5A ) with subquadrate coxal plate bearing setae on anterior to ventral margins, width 1.4 times as long as depth; anterior and posterior margins of basis with setae; merus, carpus, and propodus in length ratio of 1.0: 0.8: 0.8; posterior margin of dactylus with 3 setae ( Fig. 5B ).

Pereopod 4 ( Fig. 5C ) with subquadrate coxal plate bearing setae on anterior margin and anterodistal corner, width 1.6 times as long as depth; anterior and posterior margins of basis with setae; merus, carpus, and propodus in length ratio of 1.0: 0.8: 0.8.

Pereopod 5 ( Fig. 5D ) with bilobed coxal plate bearing setae on anterior and posterior lobes; anterior and posterior margins of basis with setae; merus, carpus, and propodus in length ratio of 1.0: 0.8: 0.8; anterior margin of dactylus with 2 setae ( Fig. 5E ).

Pereopod 6 ( Fig. 6A ) with weakly bilobed coxal plate bearing setae on anterior and posterior lobes; anterior and posterior margins of basis with setae; merus, carpus, and propodus in length ratio of 1.0: 0.9: 0.9; anterior margin of dactylus with 2 setae ( Fig. 6B ).

Pereopod 7 ( Fig. 6C ) with subtriangular coxal plate, ventral margin weakly concave, with seta on anterodistal and 2 setae on posterodistal corners; anterior and posterior margins of basis with setae; merus, carpus, and propodus in length ratio of 1.0: 1.0: 1.1; anterior margin of dactylus with 3 setae ( Fig. 6D ).

Sternal gill ( Fig. 6E ) simple, 1 sternal gill on each ventral surface of pereonites 2–4. Coxal gills ( Figs. 4F , 5A, C, D , 6A ) slender, on gnathopod 2 and pereopods 3–6. Brood plates ( Figs. 4F , 5A, C, D , 6F ) slender with numerous setae, on gnathopod 2 and pereopods 3–5.

Pleopods. Peduncles of pleopods 1–3 ( Fig. 7A, C, E ) lacking marginal setae, outerdistal corners with 2, 3 and 3 setae, respectively. Pleopods 1–3 with paired retinacula ( Fig. 7B, D, F ), bifid seta (clothes-pin seta) on inner basal margin of inner ramus; pleopods 1–3 inner ramus 12-, 11-, and 11-articulate, respectively; pleopods 1–3 outer ramus 12-, 12-, and 11-articulate, respectively.

Uropods. Uropod 1 ( Fig. 7G ) with basofacial seta on peduncle; inner ramus 0.7 times as long as peduncle, inner and outer margins with 4 and 3 robust setae, respectively, basal part with 3 slender setae; outer ramus 0.7 times as long as inner, with 2 inner and 2 outer marginal robust setae, respectively, basal part with seta. Uropod 2 ( Fig. 7H ) with inner ramus 1.2 times as long as peduncle, inner and outer margins with 3 and 2 robust setae, respectively; outer ramus 0.7 times as long as inner ramus, inner and outer margins with 1 and 2 robust setae, respectively. Uropod 3 ( Fig. 7I, J ) with peduncle 0.35 times as long as outer ramus; inner ramus absent; outer ramus 2-articulate, proximal article with robust setae, terminal article 0.1 times as long as proximal article, with 7 distal setae.

Telson ( Fig. 7K ) length 1.24 times as long as width, cleft for 45.2% of length, each telson lobe with 2 lateral penicillate setae and 4 apical robust setae.

Male paratype (NNIBRIV21631): Antenna 1 ( Fig. 8A, B ) 0.48 times as long as body length, primary flagellum 15-articulate, 1 aesthetasc on some articles. Antenna 2 ( Fig. 8C, D ) 0.65 times as long as antenna 1; flagellum 0.54 times as long as peduncular articles 4 and 5 combined, consisting of 7 articles, articles 1–3 with calceolus.

Gnathopod 1 ( Fig. 8E, F ) carpus with 3 serrate setae on posterodistal corner; palmar margin of propodus with 14 robust setae in 2 rows, some distally notched ( Fig. 8G ). Gnathopod 2 ( Fig. 8H, I ) carpus with 3 serrate setae on posterodistal corner; palmar margin of propodus with 13 robust setae in 2 rows, some distally notched ( Fig. 8J ).

Uropods. Uropod 1 ( Fig. 9A ) with inner ramus 0.7 times as long as peduncle; inner and outer margins with 3 and 1 robust setae, respectively, basal part with 3 slender setae; outer ramus with 2 marginal robust setae. Uropod 2 ( Fig. 9B ) with peduncle 0.8 times as long as inner ramus; inner ramus 1.2 times as long as outer ramus, distal part with 4 serrate, 3 simple robust setae and penicillate seta. Uropod 3 ( Fig. 9C ) with outer ramus terminal article 0.1 times as long as proximal article.

Telson ( Fig. 9D ) length 1.2 times as long as width, cleft for 38.3% of length.

Variation. Paratype female (NNIBRIV21630): Antenna 1, 2 primary flagellum 14-, 7-articulate, respectively. Maxilla 1 inner plate with 4 plumose setae. Maxilla 2 with oblique inner row of 5 setae on inner plate. Pleopods 1 with 2 bifid setae (clothes-pin seta) on inner basal margin of inner ramus; pleopods 1–3 inner ramus 9-, 9-, and 8- articulate, respectively; pleopods outer ramus 1–3 10-, 10-, and 8-articulate, respectively.

Distribution. Known only from the type locality.

Etymology. The new specific name is dedicated to Dr. Joo-Lae Cho, who has significantly contributed to our knowledge of freshwater crustaceans in South Korea.

DNA sequences. In total, seven sequences were determined: holotype (NNIBRIV21629), four sequences—28S ( LC467007 ; 1301 bp), H3 ( LC467005 ; 328 bp), COI ( LC467001 ; 658 bp), and 16S ( LC467003 ; 420 bp); and paratype (NNIBRIV21630), three sequences—H3 ( LC467006 ; 328 bp), COI ( LC467002 ; 658 bp), and 16S ( LC467004 ; 420 bp). The holotype and paratype shared identical 16S and H3 sequences. Their partial COI sequences were exceptional in occurring at a single variable site between them (1/658).

Phylogenetic position and genetic distances. The BI tree (mean ln L = −15673.962; Fig. 10 ) for estimating the phylogenetic position of the new species had an almost identical topology to that of the ML tree (ln L = −16227.759; not shown). Pseudocrangonyx joolaei sp. nov. formed a well-supported clade (BS = 78%, PP = 0.99) with P. akatsukai Tomikawa & Nakano, 2018 , which is indigenous to the western part of Japan. However, the precise phylogenetic position of this clade within the genera Pseudocrangonyx and Procrangonyx was not resolved by the present phylogenetic analyses.

The pairwise uncorrected p -distance between the 28S sequences of P. joolaei sp. nov. ( LC467007 ) and P. akatsukai ( LC171506 , LC171510 , LC171525 , LC334151 ) was 1.0–1.2% (mean = 1.1%); this divergence was calculated based on the 1301 aligned positions after eliminating gap positions from the dataset. The uncorrected COI p -distance between the present new species ( LC467001 , LC467002 ) and P. akatsukai ( LC171507 , LC171511 , LC171526 , LC334152 ) was 14.0–16.1% (mean = 15.3%).

Remarks. Although Uéno (1966) reported local variations of morphological characteristics among the Korean populations of P. asiaticus , he did not mention about a variation of sternal gills. In this study, we confirmed that the number of sternal gills of P. joolaei sp. nov. is different from the original description of P. asiaticus (three pairs of sternal gills on pereonites 2 to 4 in the former versus four pairs on pereonites 2 to 5 in the latter). The number of sternal gills is used as a diagnostic character to distinguish species in some amphipod taxa, e.g. the pontogeneiid genus Awacaris ( Kuribayashi et al. 1996) . Thus, we concluded that P. joolaei sp. nov. is distinguishable from the true P. asiaticus as a distinct new species. In addition, the present new species can be distinguished from the topotypic P. asiaticus by the combination of the following features that have been considered as diagnostic characters in the previous taxonomic papers of Pseudocrangonyx (features of P. asiaticus in parentheses; Uéno 1934): 1) head with moderately (shallow) concave antennal sinus, 2) accessory flagellum of antenna 1 not exceeding (fully exceeding) first article of primary flagellum, and 3) terminal article of uropod 3 shorter (longer) than robust setae on distal part of proximal article.

It is still not known whether all the Korean sternal-gill possessors of Pseudocrangonyx belong to the present P. joolaei sp. nov. As Uéno (1966) stated that the Korean “ P. asiaticus ” possessed the sternal gills on pereonites 2–4, the sternal gills may be a synmorphy between the Korean “ P. asiaticus ” sensu Uéno (1966) including P. joolaei sp. nov. from Simbok Cave. However, Uéno (1966) also described that specimens of the several populations had a terminal article of uropod 3 that was longer than robust setae on the distal part of the proximal article of the same uropod. The taxonomic status of the remaining populations identified as “ P. asiaticus ” by Uéno (1966) should be investigated by future systematic studies.

The present phylogenetic analyses showed that P. joolaei sp. nov. formed a monophyletic clade with the Japanese P. akatsukai . The following morphological characteristics observed in these two species also imply the close relationships between them: 1) anteroventral corner of urosomite 1 with seta, 2) antenna 2 with calceoli in both sexes, 3) carpi of gnathopods 1 and 2 with serrate robust setae on posterodistal corners, 4) number of pleopodal rami more than 10-articulate, and 5) inner margin of pleopodal inner rami with bifid setae. In addition to the presence of the sternal gills in P. joolaei sp. nov., the present new species can be clearly discriminated from P. akatsukai by the following features (features of P. akatsukai in parentheses; Tomikawa & Nakano 2018): 1) antenna 1 shorter (longer) than half of body length, 2) palp article 3 of mandible shorter (longer) than article 2, and 3) telson cleft for 45.2% (9.2%) of length.

The obtained phylogenies revealed that P. joolaei sp. nov. is a close congener of the Japanese P. akatsukai and is nested within the phylogroup consisting of the Japanese P. akatsukai and P. yezonis Akatsuka & Komai, 1922 , Chinese P. elegantulus Hou in Zhao & Hou, 2017 , and Russian P. korkishkoorum Sidorov, 2006 and P. tiunovi Sidorov & Gontcharov, 2013 . The phylogenetic position of P. joolaei sp. nov. thus suggested that the sternal gill is a derived character within the pseudocrangonyctid amphipods. For our further understanding of the evolutionary history of sternalgill possessors in the genus Pseudocrangonyx , the phylogenetic position of the “true” P. asiaticus should be assessed by further study. As P. joolaei sp. nov. and P. akatsukai share characteristics in the anteroventral corner of urosomite 1 and serrate robust setae on the posterodistal corners of carpi of each of the gnathopods 1 and 2 with P. asiaticus , it is possible that the three species would form a monophyletic group within the family Pseudocrangonyctidae .

Figures

FIGURE 2. Pseudocrangonyx joolaei sp. nov., holotype female, NNIBRIV21629. Habitus, lateral view, without scale.

FIGURE 3. Pseudocrangonyx joolaei sp. nov., holotype female, NNIBRIV21629. (A) Head, lateral view. (B) Epimeral plates 1–3 and urosomites 1–3, lateral view. (C) Antenna 1, medial view. (D) Accessory flagellum of antenna 1, medial view. (E) Antenna 2, medial view. (F) Calceolus of antenna 2, medial view. (G) Upper lip, posterior view. (H) Right mandible, medial view. (I) Incisor, lacinia mobilis, and molar process of right mandible, medial view. (J) Incisor and lacinia mobilis of left mandible, medial view. (K) Lower lip, dorsal view. (L) Maxilla 1, dorsal view. (M) Apical robust setae on outer plate of maxilla 1, dorsal view. (N) Apical plumose robust seta and robust setae on palp article 2 of maxilla 1, dorsal view.

FIGURE 4. Pseudocrangonyx joolaei sp. nov., holotype female, NNIBRIV21629. (A) Maxilla 2, dorsal view. (B) Maxilliped, dorsal view. (C) Apical setae on inner plate of maxilliped, dorsal view. (D) Gnathopod 1, medial view. (E) Palmar margin of propodus and dactylus of gnathopod 1, medial view. (F) Gnathopod 2, medial view. (G) Palmar margin of propodus and dactylus of gnathopod 2, medial view.

FIGURE 5. Pseudocrangonyx joolaei sp. nov., holotype female, NNIBRIV21629. (A) Pereopod 3, medial view. (B) Dactylus of pereopod 3, medial view. (C) Pereopod 4, medial view. (D) Pereopod 5, medial view. (E) Dactylus of pereopod 5, medial view.

FIGURE 6. Pseudocrangonyx joolaei sp. nov., holotype female, NNIBRIV21629. (A) Pereopod 6, medial view. (B) Dactylus of pereopod 6, medial view. (C) Pereopod 7, medial view. (D) Dactylus of pereopod 7, medial view. (E) Sternal gills on pereonites 2–4, lateral view. (F) Brood plate of pereopod 3, medial view.

FIGURE 7. Pseudocrangonyx joolaei sp. nov., holotype female, NNIBRIV21629. (A) Pleopod 1, anterior view. (B) Retinacula on peduncle of pleopod 1, anterior view. (C) Pleopod 2, anterior view. (D) Retinacula on peduncle of pleopod 2, anterior view. (E) Pleopod 3, anterior view. (F) Retinacula on peduncle of pleopod 3, anterior view. (G) Uropod 1, dorsal view. (H) Uropod 2, ventral view. (I) Uropod 3, dorsal view. (J) Terminal article of uropod 3, dorsal view. (K) Telson, dorsal view.

FIGURE 8. Pseudocrangonyx joolaei sp. nov., paratype male, NNIBRIV21631. (A) Antenna 1, lateral view. (B) Accessory flagellum of antenna 1, lateral view. (C) Antenna 2, medial view. (D) Calceolus of antenna 2, medial view. (E) Gnathopod 1, medial view. (F) Serrate setae on posterodistal corner of carpus of gnathopod 1, lateral view. (G) Palmar margin of propodus and dactylus of gnathopod 1, medial view. (H) Gnathopod 2, medial view. (I) Serrate setae on posterodistal corner of carpus of gnathopod 2, lateral view. (J) Palmar margin of propodus and dactylus of gnathopod 2, medial view.

FIGURE 9. Pseudocrangonyx joolaei sp. nov., paratype male, NNIBRIV21631. (A) Uropod 1, dorsal view. (B) Uropod 2, ventral view. (C) Uropod 3, dorsal view. (D) Telson, dorsal view.

FIGURE 10. Bayesian inference tree for 2,778 bp of nuclear 28S rRNA and histone H3, and mitochondrial COI and 16S rRNA markers. Numbers on nodes represent bootstrap values for maximum likelihood and Bayesian posterior probabilities. Taxonomically confused clades are highlighted in a gray box. The genus-group name Pseudocrangonyx is abbreviated to P.