Cryptic Species of a Cascade Frog from Southeast Asia: Taxonomic Revisions and Descriptions of Six New Species Author BAIN, RAOUL H. Author LATHROP, AMY Author MURPHY, ROBERT W. Author ORLOV, NIKOLAI L. Author CUC, HO THU text American Museum Novitates 2003 2003-10-29 3417 1 60 http://www.bioone.org/doi/abs/10.1206/0003-0082%282003%29417%3C0001%3ACSOACF%3E2.0.CO%3B2 journal article 3413 10.1206/0003-0082(2003)417<0001:CSOACF>2.0.CO;2 0464179d-9549-4885-9ddd-32ffef32942e 0003-0082 4734880 Rana bacboensis , new species (Previously referred to as species 2, ‘‘Black Egg’’) Figures 11D , 12E, F , 13B HOLOTYPE : (ROM field no. 13171) ROM 29534 an adult female from the Khe Moi River, approximately 24 km west of Con Cuong village , Con Cuong District , Nghe An Province , Vietnam (18°56̍30̎N, 104°48̍35̎E) collected 24 October 1994 by I.S. Darevsky , L.A. Lowcock , R.W. Murphy , and N.L. Orlov. The holotype had leg and liver tissue removed shortly after it was euthanised. Fig. 11. Members of the Rana chloronota complex. ( A ) Male and female and ( B ) male R. chloronota , Nghe An Province, Vietnam. C. R. graminea , male, Hainan Island, China, (NLO field series 26375). D. R. bacboensis , new species , holotype, a female from Nghe An Province, Vietnam. ( E ) Female holotype and male paratype in amplexus, and ( F ) juvenile paratype of R. daorum , new species , Lao Cai Province, Vietnam. Fig. 12. Heads of members of the Rana chloronota complex in lateral and dorsal views: ( A, B ) Rana chloronota , male (ROM 26402), and ( C, D ) female (ROM 26406); paratypes of ( E, F ) Rana bacboensis , new species (ROM 29529); ( G, H ) Rana daorum , new species (ROM 38538); ( I, J ) Rana hmongorum , new species (ROM 39891); ( K, L ) Rana morafkai , new species (ROM 39906); ( M, N ) Rana banaorum , new species (ROM39941); and ( O, P ) Rana megatympanum , new species (ROM 26398). Fig. 13. Hands and feet of members of the Rana chloronota complex: ( A ) Rana chloronota (ROM 26402); paratypes of ( B ) Rana bacboensis , new species (ROM 29529); ( C ) Rana daorum , new species (ROM 38538); ( D ) Rana hmongorum , new species (ROM 26379); ( E ) Rana morafkai , new species (ROM 39906); ( F ) Rana banaorum , new species (ROM 39941); and ( G ) Rana megatympanum , new species (ROM 26398). Scale equals 5 mm. PARATYPES : ROM 29531–29533, all females, collected with holotype on 24 October 1994 by I.S. Darevsky, L.A. Lowcock, R.W. Murphy, and N.L. Orlov; ROM 26404, a female collected at the type locality by A. Lathrop , R.W. Murphy , and N. Orlov on 5 June 1995 ; ROM 26357–26358, adult females collected from the type locality on 5 June 1995 by A. Lathrop, R.W. Murphy, and N.L. Orlov; ROM 29359, a female, from Ba Be Lake , Ba Be Lake National Park , Bac Kan Province (formerly Cao Bang Province ), Vietnam (22°25̍05̎N, 105°38̍05̎E), collected by R.H. Bain on 24 May 1995 at the outflow on the south side of Ba Be Lake ; ROM 29526–29530, all females, from Na Hang Nature Reserve , Tuyen Quang Province , Vietnam (22°21̍54̎N, 105°25̍40̎E) approximately 15 km from Pac Ban village collected by R.W. Murphy and A. Lathrop between 25 and 30 May 1996 ; AMNH A­161248, a female, from Hieng Stream , Chau Khe Commune , Con Cuong District , Nghe An Province , Vietnam (19°02̍17̎N, 104°42̍06̎E, elevation 300 m ) collected on 29 April 1998 by N.Q. Truong ; FMNH 255611 (adult female), 255612 (adult male) along the Khe Chat Stream , Pu Mat Nature Reserve , Con Cuong District , Nghe An Province , Vietnam (18°56̍N, 104°45̍E, elevation 300 m ) on 8 September 1998 by Bryan L. Stuart. DIAGNOSIS: Rana bacboensis , a member of the subgenus Odorrana (sensu Fei et al., 1990 ), is characterized by a combination of the following attributes: (1) body dorsoventrally compressed; (2) SVL of males 54.9 mm , means of females 96 mm ( 82–105 mm ); (3) vomerine teeth present in rows oblique to choanae; (4) vertical black stripes on upper lip (especially under eye), light colored glandule above insertion of arm; (5) head broad, bluntly rounded in profile; (6) tympanum circular, distinct, TMP:EYE 0.43 in females, 0.66 in the male; (7) supratympanic fold weak; (8) dorsal skin shagreened, becoming granular laterally, dorsolateral fold absent; venter smooth; (9) dorsum brown with black blotches; forelimbs and hindlimbs with transverse bands of distinct blotches to tips of digits; (10) median callous pad on base of fingers II and III to proximal tubercle; (11) disks on fingers and toes enlarged (<2× base of phalanges); (12) feet fully webbed to disks, but as a fringe from distal subarticular tubercle of IV, slight lateral fringes on toes I and V to terminal phalanges, webbing marbled brown on white; (13) subarticular tubercles distinct, conical; inner metatarsal tubercle distinct, ovoid; (14) terminal phalanges T­ shaped; (15) xiphisternum large, deeply notched posteriorly; (16) male with velvety nuptial pad on thumb, paired gular pouches, no pectoral spines; (17) eggs black. COMPARISONS: Rana bacboensis is one of the larger species of cascade ranids (SVL female 81–105 mm ). It can be distinguished from all other cascade ranids of Southeast Asia by its dark, pigmented eggs (immaculate white or white with melanic pole in other species) (table 12). Its black vertical lip­bars distinguish it from R. archotaphus , R. chalconota , R. chloronota , R. grahami , R. graminea , R. hejiangensis , R. hosii , R. jingdongensis , R. kwangwuensis , R. leporipes , R. livida , R. schmackeri , R. sinica , and Huia nasica . The brown dorsum with dark spots distinguishes it from R. archotaphus , R. chalconota , R. chloronota , R. grahami , R. graminea , R. hejiangensis , R. hosii , R. jingdongensis , R. junlianensis , R. kwangwuensis , R. leporipes , R. margaretae , R. schmackeri , and R. sinica , all of which have a predominantly green dorsum. The presence of gular pouches in males differentiates R. bacboensis from R. andersonii , R. chalconota , R. grahami , R. hainanensis , R. hosii , R. jingdongensis , R. junlianensis , R. kwangwuensis , and R. margaretae . Huia nasica has a smooth, olive­brown dorsum with lighter flanks ( R. bacboensis is shagreened and uniformly brown with black spots both on the dorsum and flanks), and adult females are smaller than those of R. bacboensis ( 67 mm vs.> 80 mm ). The absence of an outer metatarsal tubercle and the large female SVL also distinguishes R. bacboensis from R. archotaphus and R. chalconota (female SVL 81– 105 mm for R. bacboensis , 59–62 mm and 46–59 mm for R. archotaphus and R. chalconota , respectively). The absence of dorsolateral folds distinguishes R. bacboensis from R. chalconota , R. graminea , R. hosii , and R. leporipes (pustules on the dorsum of R. grahami sometimes form a dorsolateral fold). Rana bacboensis has webbing to the base of the toe pad distinguishing it from R. leporipes (webbing to distal phalanx). Rana sinica can further be distinguished from Rana bacboensis by its indistinct, skin­covered tympanum, and different finger formula (I <II <IV for R. sinica , II <I <IV for R. bacboensis ). Rana bacboensis shares a superficial resemblance to R. tiannensis , another large brown cascade ranid, but differs in having shagreened dorsal skin with small lateral granulations (dorsum of R. tiannensis is rough with large, prominent lateral granulations) and smaller toe disk than finger disk (the opposite condition of R. tiannensis ). Rana bacboensis most closely resembles R. hainanensis , R. jingdongensis , and R. andersonii . Rana bacboensis further differs from R. hainanensis in its relative lengths of fingers (II <IV <I <III for R. hainanensis ) and by its shagreened skin (smooth for R. hainanensis ). Rana bacboensis also differs from R. jingdongensis in profile of its snout shape (rounded or obtusely pointed in R. jingdongensis versus rounded in R. bacboensis ) and texture of skin ( R. jingdongensis dorsum scattered with tubercles and large warts, lips and sides of heads with white spines, all absent in R. bacboensis ). Rana bacboensis also differs from R. andersonii in its head shape (obtusely pointed in R. andersonii ) and absence of ventral spines in the males. DESCRIPTION OF HOLOTYPE : A gravid female (ROM 29534), head length greater than width (127%), head width 34% of SVL, length 43% of SVL; snout short, protruding beyond margin of lower jaw, rounded in dorsal view, bluntly rounded in profile; eye large, prominent, 81% of snout length; eyelid broader than interorbital distance. Top of head flat; canthus rostralis rounded; loreal region concave; lip flared just anterior to orbit; nostril about three­fourths distance from eye to tip of snout; supratympanic fold barely evident, curving posteroventrally from posterior corner of eye to a level above insertion of arm; tympanum round, distinctly visible, separated from eye by distance equal to TMP:EYE 0.62. Choanae ovoid; vomerine dentigerous processes prominent, slightly oblique, posteromedial to choanae, each bearing numerous teeth. Tongue cordiform, distinctly notched posteriorly, free for approximately one­half its length. Forearms moderately robust; fingers moderately short, slender; hands 27% of SVL, relative lengths of fingers II <I <IV <III; ventromedial callous ridge on fingers II and III prominent, extending to proximal tubercle; disks expanded (<2× base of phalanges), relative pad size II <I <IV <III, pad length (III) 75% of pad width; ventral circummarginal grooves present; terminal phalanges T­ shaped; subarticular tubercles conical. Hindlimbs moderately robust; tibia length 60% of SVL; foot length 62% of SVL; relative toe lengths I <II <III <V <IV; inner tarsal fold absent; feet fully webbed to disks, but as a fringe from distal subarticular tubercle of IV, lateral fringes on toes I and V to terminal phalanges; toes long, slender, with large, rounded triangular disks, relative pad size I = II = III> IV k V, pad width (IV) 85% of pad length, circummarginal grooves present; subarticular tubercles prominent, conical; inner metatarsal tubercle ovoid, long; outer metatarsal tubercle absent. Xiphisternum large, deeply notched posteriorly. Skin on dorsum shagreened with heavy granulations, leathery in alcohol preservation; dorsolateral folds absent; small tubercles anterior and posterior to tympanum; flanks with small granulations and large pustules; distinct granules on posterior thighs and around cloaca; cloacal opening unmodified, directed posteriorly, at upper level of thighs. COLOR IN LIFE (in preservative): Dorsum, flanks, and loreal region brown (brownish gray) with small black spots, becoming larger on the flanks; upper and lower lips creamy yellow with vertical black bars; dorsal limbs and digits brown with black transverse bands; webbing on feet marbled white and dark brown (black); venter creamy white, sometimes with light spotting on belly, chest, and chin; iris golden, margin of pupil outlined in a striking yellow and red border. SECONDARY SEXUAL CHARACTERS: The holotype possesses large, black eggs ( 2 mm in diameter). The lone male paratype has gular pouches, thickened forearms, and thick white nuptial pads. MEASUREMENTS OF HOLOTYPE (in mm): SVL 95.1; SNT 12.0; HDL 41.0; HDW 32.2; EYE 9.7; IOD 6.4; TMP 6.0; TEY 5.0; HND 25.6; FGR 21.8; FPL 2.8; FPW 3.7; TIB 56.8; FTL 59.6; TPL 2.4; TPW 2.0. VARIATION OF PARATYPES : Variation in all type material is given in table 15. MEASUREMENTS OF FEMALE PARATYPES (in mm, n = 6, ROM 29359, 29526–29530): SVL 95.8 mm ± 6.4 (81.8–105.1); SNT 13.8 ± 1.4 (10.8–15.6); HDL 46.4 ± 3.5 (43.5– 51.2); HDW 35.4 ± 2.9 (34.1–39.6); EYE 9.8 ± 0.5 (9.4–10.8); IOD 7.9 ± 1.7 (5.8– 11.0); TMP 5.3 ± 0.6 (4.0–6.0); TEY 4.9 ± 0.7 (3.6–6.0); HND 25.5 ± 2.8 (18.6–30.3); FGR 20.8 ± 2.3 (14.0–24.1); FPL 3.0 ± 0.3 (2.4–3.6); FPW 3.5 ± 0.6 (2.6–4.3); TIB 58.6 ± 3.7 (50.5–66.2); FTL 70.2 ± 7.8 (55.8–79.1). MEASUREMENTS OF MALE PARATYPE (in mm, FMNH 255611): SVL 54.9, SNT 8.8, HDL 28.0, HDW 18.1, EYE 6.6, IOD 6.1, TMP 4.4, TEY 1.8, HND 16.5, FPL 2.4, FPW 1.8, TIB 32.4, FTL 45.4, TPL 2.4, TPW 1.6. ETYMOLOGY: The specific name, derived from Bac Bo, the Vietnamese name for northern Vietnam (often referred to as Tonkin ), reflects this species’ distribution. DISTRIBUTION AND ECOLOGY: Rana bacboensis occurs in forested montane river systems across northern Vietnam . These rivers vary from shallow and slow moving to torrential and deep. Specimens may be found on boulders and logs, both in and around the water and in the adjacent forest. Radiographs revealed that females feed on large invertebrates, including small freshwater crabs. Females were collected in April–May and October. The holotype , collected in October , has fully developed ova, and two females (ROM 26358, 29529) collected in the spring have undeveloped ova suggesting a fall breeding season. No calls are associated with this species. The tadpoles are unknown . REMARKS: Cascade ranids bearing white eggs lay them under rocks, sheltered from the sunlight ( Pope, 1931 ; ROM field notes, 1996). In contrast, the black eggs of R. bacboensis might be found where they are exposed to sunlight to promote development, a requirement for some species with melanic eggs ( Duellman and Trueb, 1986 ).