Anomaloglossus blanci, Antoine & Vacher & Courtois & Villette & Reizine & Gaucher & Jairam & Ouboter & Kok, 2018

Antoine, Fouquet, Vacher, Jean-Pierre, Courtois, Elodie A., Villette, Benoit, Reizine, Hugo, Gaucher, Philippe, Jairam, Rawien, Ouboter, Paul & Kok, Philippe J. R., 2018, On the brink of extinction: two new species of Anomaloglossus from French Guiana and amended definitions of Anomaloglossus degranvillei and A. surinamensis (Anura: Aromobatidae), Zootaxa 4379 (1), pp. 1-23 : 5-10

Anomaloglossus blanci sp. nov.

Colostethus degranvillei — Lescure 1975 (in part): 414; Lescure & Marty 2001 (in part): 86 Anomaloglossus degranvillei — Fouquet et al. 2007 (in part): Fig. S2 ; Fouquet et al. 2012 (in part): 469 Anomaloglossus sp. “north FG” — Vacher et al. (2017)

Holotype. MNHN2017.0103 (field no. AF0953), an adult male, collected by Michel Blanc and Maël Dewynter, 10 August 2014, corridor 7 on Route Nationale 2, French Guiana, 4.0639 N 52.0416 W, ~ 100 m elevation ( Figure 2 ) . Paratypes. Ten specimens: MNHN2017.0110 (field no. AF0952), an adult male, collected with the holotype (carrying two froglets on its back). MNHN2017.0105 (field no. AF0293), an adult male collected by Antoine Fouquet, 25 May 2007, crique Diamant near Patawa Camp, French Guiana, 4.5161 N 52.1005 W, ~ 200 m elevation . MNHN2017.0106–8 (field no. AF0878, AF0932, AF0933), three adult males collected by Antoine Fouquet, 0 1 February 2013, crique Diamant near Patawa Camp, French Guiana, 4.5161 N 52.1005 W, ~ 200 m elevation . MNHN2017.0104 (field no. AF0292), an adult female collected by Antoine Fouquet, 25 May 2007, crique Diamant near Patawa Camp, French Guiana, 4.5161 N 52.1005 W, ~ 200 m elevation . MNHN2017.0109 (field no. AF1332), an adult male collected by Maël Dewynter, 16 December 2013, Saut Grand Machicou , French Guiana, 3.8974 N 52.5836 W, ~ 150 m elevation . IRSNB4198 (field no. PK3287), an adult male collected by Philippe J. R. Kok, 18 April 2010, near Patawa Camp , French Guiana, ca. 4.5161 N 52.1005 W, ~ 200 m elevation . IRSNB4199 , 4200 (field no. PK3284, 3286), two juvenile females collected by Philippe J. R. Kok, 18 April 2010, near Patawa Camp , French Guiana, ca. 4.5161 N 52.1005 W, ~ 200 m elevation.

Etymology. This species is dedicated to our friend Michel Blanc, in honour of his invaluable contribution to field herpetology in French Guiana, notably the discovery of many previously undocumented species and crucial natural history observations.

Definition and diagnosis. We assigned the new species to the genus Anomaloglossus based on previous studies (Fouquet et al. 2012; Vacher et al. 2017) and the presence of a median lingual process. The new species belongs to the A. degranvillei clade ( Vacher et al. 2017).

(1) Small-sized Anomaloglossus (average male SVL= 16.9 mm [15.9–18.8, n=8], female SVL= 17.9 mm [n=1]) ( Table 1); (2) body robust; (3) skin tuberculate on dorsum (particularly the posterior half) and legs, with a larger tubercle on each eyelid, ventral skin smooth; (4) conspicuous dark brown to black glandulous supratympanic fold anteroventrally bordered by a light stripe (orange in life, cream in preservative) extending from the ventroposterior edge of the eye onto the upper arm to the anterior cubital region; (5) tympanum indistinct; (6) snout short and protruding in lateral view; (7) nares oriented ventrolaterally, situated near tip of snout; (8) Finger II shorter than Finger I when fingers adpressed; (9) tip of Finger IV almost reaching distal subarticular tubercle on Finger III when fingers adpressed; (10) distal subarticular tubercle on Finger III and IV indistinct; (11) Finger III not distinctly swollen in males; (12) Fingers II and III with preaxial fringes particularly developed in males, inconspicuous in females; (13) toes moderately webbed, with well-developed fringes on Toes II, III and IV (sensu Grant et al. 2006; keel-like lateral folds sensu Myers & Donnelly 2008); (14) tarsal keel well-defined, curved; (15) no black arm gland in males (sensu Grant & Castro 1998, see also Grant et al. 2006); (16) cloacal tubercles present; (17) paracloacal mark ill-defined but present (reddish in life, cream speckled with melanophores in preservative); (18) dorsolateral stripe present, faint, upper part of flanks much darker than dorsum, a thin middorsal raphe going from the tip of snout to behind the head and more rarely to the vent sometimes present; (19) ventrolateral stripe absent but ventral part of flanks lighter with white or bluish flecks (in life); (20) sexual dichromatism in throat colour pattern present, throat black in reproductive males, evenly grey with small ill-defined white dots in females; (21) no sexual dichromatism in ventral colour pattern, abdomen mostly pale grey with small ill-defined white dots in both sexes, lower abdomen and ventral surface of legs yellowish in life and cream in preservative; (22) iris with metallic pigmentation and pupil ring interrupted ventrally and dorsally by transversal black pigmentation; (23) median lingual process longer than wide, tapered, bluntly pointed, smooth (non-papillate), reclined in pit; (24) single note call of 0.090– 0.103 s length and dominant frequency at 4.48–5.41 kHz (n=6) ( Figure 3 ; Table 2).

Morphological comparisons with other lowland Anomaloglossus . The only other species group cooccurring with the Anomaloglossus degranvillei group is the A. stepheni group, represented in French Guiana by A. baeobatrachus , which is readily distinguishable by conspicuous dorsolateral stripes, swollen third finger in males and absence of webbing and fringes on toes.

Within the Anomaloglossus degranvillei group, A. blanci can be distinguished from A. surinamensis ( Figure 4 ) by (1) a shorter snout, protruding in lateral view (vs. rounded in A. surinamensis ); (2) a larger body size (X¯ =16.9; range 15.9–18.8 mm in males [n=8] and one adult female measuring 17.9 mm in A. blanci vs. X¯ =14.75, range 14.0– 15.3 mm in males [n=8] and X¯ =16.5, range 16.0– 17.1 mm in females [n=4] in A. surinamensis ); (3) large fringes on fingers and toes in males (narrow in A. surinamensis ); (4) presence of a large tubercle on the top of the eyelid (inconspicuous in A. surinamensis ); (5) ventral colouration entirely grey with small ill-defined white dots (vs. grey throat and cream belly, the latter with irregular grey blotches less abundant posteriorly in A. surinamensis ); (6) yellowish ventral surface of thigh (vs. light grey and more heavily spotted with black in A. surinamensis ); (7) large MLP (> 0.5 mm vs. <0.5 mm in A. surinamensis ); (8) call characterized by longer pulsed notes (X¯ =0.094, range 0.090– 0.103 s in A. blanci [n=6] vs. tonal note X¯ =0.032, range 0.028– 0.037 s in A. surinamensis [n=20]) emitted between longer intervals (X¯ =1.414, range 1.200– 1.906 s in A. blanci [n=6] vs. X¯ =0.573, range 0.372– 0.825 s in A. surinamensis [n=20]), but both species have a similar dominant frequency (X¯ =4.75, range 4.48–5.41 kHz in A. blanci [n=6] vs. X¯ =4.89 kHZ, range 4.55–5.35 kHz in A. surinamensis [n=20]).

Anomaloglossus blanci can be distinguished from A. degranvillei ( Figure 5 ) by (1) a smaller size (X¯ =16.9; range 15.9–18.8 mm in males [n=8] and one female measuring 17.9 mm in A. blanci vs. X¯ =20.17; range 19.60–20.50 mm in males [n=3] and X¯ =23.40, range 22.4–23.9 mm in females [n=5] of A. degranvillei ); (2) belly pale grey with small ill-defined white dots (from solid black to dark grey with abundant small conspicuous white spots in A. degranvillei ); (3) ventral surface of thighs yellowish in life and cream in preservative (dark grey in A. degranvillei ); (4) call with shorter notes (0.090– 0.103 s in A. blanci [n=6] vs. 0.157– 0.160 s in A. degranvillei [n=2]) and higher dominant frequency (4.48–5.41 kHz in A. blanci [n=6] vs. 3.60– 3.62 s in A. degranvillei [n=2]).

Description of the holotype ( Figure 2 ). An adult male, 17.1 mm SVL; body robust; head wider than long, HL 89% of HW; HL 33% of SVL; dorsal skin tuberculate, one enlarged tubercle on each eyelid, snout long (SL 53% of HL), rounded to nearly truncate in dorsal view, protruding in lateral view, extending past lower jaw. Nares located anterolaterally; canthus rostralis rounded, loreal region concave; IN 42% of HW; EN 28% of HL, 70% of ED. Tympanum indistinct; supratympanic fold present extending from posteroventral corner of the eye onto the upper arm; choanae small, circular, located anterolaterally.

Forelimb slender, skin tuberculate; metacarpal ridge absent; HAND 24% of SVL; Finger I longer than Finger II when fingers adpressed; fingers large and flattened without webbing, lateral fringes present on preaxial edges of Fingers II and III; Finger III not distinctly swollen; tip of Finger IV not reaching distal subarticular tubercle on Finger III when fingers adpressed; finger discs expanded, wider than long, about 1.5X width of digit; width of disc on Finger III 0.6 mm; discs with distinct dorsal scutes. Relative lengths of adpressed fingers III> IV> I> II; palmar tubercle large, heart-shaped, 0.8 mm in diameter (larger than Finger III disc), thenar tubercle small (equal to Finger III disc), elliptic, half the size of palmar tubercle, well separated from palmar tubercle. Only basal subarticular tubercles on Fingers III and IV are conspicuous; Finger I subarticular tubercle largest followed by Finger II subarticular tubercle, basal subarticular tubercle on Finger III and IV smaller, subequal.

Hind limb robust, skin tuberculate; TL 46 % of SVL; heels not in contact when hind limbs are flexed at right angle to sagittal plane of body; FL 42% of SVL; relative length of adpressed toes IV> III> V> II> I; Toe I very short, its tip reaching the base of subarticular tubercle on Toe II when toes adpressed; toe discs larger than width of toes; disc on Toe I only slightly larger than width of digit. Width of disc on Toe IV 0.8 mm. Feet moderately webbed, webbing present between Toes I–IV, webbing without melanophores; lateral fringes present on all toes. Toe webbing formula I 1 ½-1- II 1 ½-2- III 1 - -3 IV 3 - -2+ V. One to three subarticular tubercles on toes as follows: one on Toes I and II, two on Toes III and V, three on Toe IV. Inner metatarsal tubercle protuberant elliptical, 0.5 mm in length, outer metatarsal tubercle round, protuberant, 0.3 mm in diameter. Tarsal keel well defined, tubercle-like and strongly curved at proximal end, extending distally to the fringe on preaxial edge of Toe I. Metatarsal fold strong.

Colour of holotype in life ( Figure 2 ). Dorsal colour chestnut brown, with a diffuse dark brown hourglass pattern extending from the interorbital region to middorsum immediately followed by a diffuse dark brown patch over the sacrum. Faint dorsolateral stripes. Black lateral mask extending from tip of snout to the upper part of flanks, tapering to groin and containing most of the indistinct tympanum and supratympanic fold, only interrupted by a large postocular orange stripe extending from eye onto the upper arm down to the anterior cubital region. Upper lip with 2–3 small light blue blotches. Posteroventral part of flanks pale brown with a few small white-blue and dark brown blotches. Throat solid black becoming paler posteriorly; belly grey with ill-defined light blue and white spots, lower part of belly and ventral surface of thighs and arms orange with a few ill-defined grey spots. Iris with reddish metallic pigmentation and pupil ring interrupted dorsally and ventrally by transversal pigmentation.

Upper arm pale orange dorsally, black on its anterior part (same colour as throat), and dark brown with illdefined orange marbling on its posterior part. Lower arm light brown with two ill-defined dark brown cross bands. Dorsal surfaces of thigh, shank and tarsus with diffuse combination of orange, pale brown and a wide ill-defined dark brown cross band; more cross bands on tarsus. Reddish paracloacal marks. Toes and digits with small light blue dots. Palms and soles dark grey.

Colour of holotype in preservative. After three years in preservative (70% ethanol), the specimen faded and the dorsal colouration now varies from brown to grey. The bluish freckles turned cream as did the orange and reddish marks.

Variation among type specimens. Measurements (range, mean, and standard deviation) of the type series are provided in Table 1. Intraspecific variation is high and adult dorsal colouration varies from brown to reddish brown. Most specimens have dark brown blotches on dorsum. One male ( MNHN 2017.0108/AF0933) has a middorsal raphe running from the tip of the snout to the vent; in four males ( MNHN 2017.0105–7/AF0293, 0 878, 0 932 and MNHN 2017.0109/AF1332; Figure 6 ) that raphe is inconspicuous and extends only from the tip of the snout to the interorbital region. Flanks can be dark brown to light grey rendering the lateral black band more or less conspicuous. Additionally, overall colouration and tuberculation may vary with light intensity, time of the day and probably reproductive activity as males carrying tadpole apparently display overall lighter colours, smoother skin and sharper contrasts while calling males are very dark and highly tuberculate.

Advertisement call ( Figure 3 ). Six specimens (three uncollected) calling from the leaf litter 1–3 meters away from a stream were recorded from a distance of about 1 m and at temperatures ranging from 23 to 26°C. They emitted single short pulsed notes (note length X¯ = 0.094 s; range 0.090– 0.103 s) at a regular pace (inter-note interval X¯ = 1.414 s; range 1.200– 1.906 s). The spectral structure of the note has a developed harmonic structure and the dominant frequency is 4.75 kHz on average (range 4.48–5.41 kHz) with a slight upward modulation (ca. 0.1 kHz).

Distribution and ecology. Anomaloglossus blanci inhabits small sandy or rocky streams at low elevations (from 50 to 200 m elevation) often close to larger tributaries (e.g. Crique Diamant, Approuague). Males call from stream banks during the day with peak in intensity at dawn (6–7 am) and late afternoon (4–5 pm) during the rainy season, but also during humid days of the dry season.

Eighteen populations have been documented in north-eastern French Guiana ( Figure 1 ), but despite intensive surveys of these populations in 2016, no individual could be found in three of them. No noticeable degradation of the habitat has been observed. Interestingly, this species does not co-occur with A. surinamensis , whose populations seem stable.

No tadpole before Gosner stage 41 has been observed, either in the water or carried by males. However, two observations have been made of adults carrying tadpoles at a late development stage (> stage 41) ( Figure 6 ). The tadpoles are endotrophic and lack functional mouth. If they are detached from the back of their father, they die within a few hours despite humid and ideal thermal conditions (pers. obs.). These observations suggest that the tadpoles may undergo a phase of nidicolous development after hatching and only complete their development on the back of the adult from an advanced stage.

Only 1–4 tadpoles of the same stage were observed at a time carried by adults. This reduced clutch size is likely linked to the fact that large eggs are needed to complete endotrophic development. However, adults were often observed carrying tadpoles at two different stages, demonstrating that they can keep mating while already attending a clutch. This is likely linked to the extended time needed for the tadpoles to develop until complete metamorphosis.

Figures

FIGURE 1. (A) Map of occurrences of the four species of the A. degranvillei species group. The range of A. surinamensis is depicted by a grey convex polygon. (B) Best ML tree obtained from RAxML NG using>15kb of mtDNA for six terminals (accession numbers in red) and 418 bp of 16S for 32 terminals (accession numbers in black). The tree is rooted on Anomaloglossus baeobatrachus. Bootstrap valuesare given in % foreach node (*=99 or 100%).

FIGURE 2. Holotype of Anomaloglossus blanci sp. nov MNHN2017.0103 (AF0953): (A) in life dorsolateral view; (B) in life ventral view; (C) in preservative dorsal view; (D) in preservative ventral view; (E) in preservative head lateral view; (F) right hand; (G) right foot; (H) median lingual process.

FIGURE 3. Spectrograms and oscillograms of typical call of the four species of the Anomaloglossus degranvillei clade with two time windows; 2 s and 0.3 s. For A.blanci and A. degranvillei the background noises masked the fundamental frequency.

FIGURE 4. Male specimen MNHN2017.0130 (AF2324) of Anomaloglossus surinamensis from Chutes Voltaire, French Guiana:(A) in life dorsolateral view; (B) in life ventral view; (C)in preservative dorsal view; (D) in preservative ventral view; (E)in preservative head lateral view; (F) Right hand; (G) right foot; (H) median lingual process.

FIGURE 6. Living specimens and habitats of the four species of the Anomaloglossus degranvillei clade; (A) A. blanci including two males carrying tadpoles MNHN2017.0110 (AF0952) was carrying two metamorphs but one was removed, a mark left by the missing tadpole is visible on the skin; an unvouchered male with three tadpoles at different stages probably from two different clutches); (B) A. dewynteri including one uncollected male carrying six tadpoles; (C) A. degranvillei uncollected male carrying four tadpoles; (D) A. surinamensis male from the type locality in Suriname carrying three tadpoles.

FIGURE5. Specimensof Anomaloglossus degranvillei from AtachiBakka,French Guiana:(A) unvoucheredfemale specimen in lifedorsolateral view; (B) unvoucheredfemale specimen in life ventral view; (C) MNHN2017.0120 (PG618) male specimen in preservative dorsal view; (D) in preservative ventral view; (E) in preservative head lateral view; (F) Right hand; (G) right foot; (H) median lingual process.