Anomaloglossus saramaka, Fouquet & Jairam & Ouboter & Kok, 2020

Fouquet, Antoine, Jairam, Rawien, Ouboter, Paul & Kok, Philippe J. R., 2020, Two new species of Anomaloglossus (Anura: Aromobatidae) of the stepheni group from Suriname, Zootaxa 4820 (1), pp. 147-164 : 150-153

Anomaloglossus saramaka sp. nov.

Anomaloglossus sp. “Brownsberg” Grant et al. 2006

Anomaloglossus sp. Fouquet et al. 2007

Anomaloglossus sp. Fouquet et al. 2012

Anomaloglossus baeobatrachus Ouboter and Jairam 2012

Anomaloglossus sp. “Brownsberg” Grant et al. 2017

Anomaloglossus sp. Brownsberg Vacher et al. 2017

Holotype. MNHN _RA_2019.0016 (field n°AF3845), an adult male, collected by A. Fouquet, S. Cally and R. Jairam on 01 February 2016 at Brownsberg , Suriname (4.936527 N 55.194826 W, ~ 500 m elevation; Figs. 2‒3 ; Ap-pendix 1).

Paratypes. Fifteen specimens: MNHN _RA_2019.0018–21, 27, 28, 29 (field n°AF3840–43, 3884, 3889, 3897) and NZCS-A1206 (field n°AF3844) eight adult males and MNHN _RA_2019.0022‒26 (field n° AF3848, 3876, 3877, 3881, 3882) and NZCS-A1207 (field n° AF3847) six females collected with the holotype by A. Fouquet, S. Cally and R. Jairam, and MNHN _RA_2019.0017 (field n°AF3774) an adult male collected by A. Fouquet, S. Cally and R. Jairam on 25 January 2016 at Voltzberg , Suriname (4.68169 N 56.18568 W, ~ 100 m elevation) .

Etymology. The specific epithet is a noun in apposition and refers to the Saramaka people who live nearby the type locality and are one of the Maroon communities living in Suriname.

Definition. (1) Medium-sized Anomaloglossus (average male SVL 19.3 mm [18.6–19.9, n = 10], female SVL 20.3 mm [19.9–21.6, n = 6]) ( Table 1); (2) body robust; (3) skin on dorsum finely granular with larger scattered tubercles becoming denser on the posterior half and legs, with a larger tubercle on each eyelid; (4) ventral skin smooth except under thighs where it is finely granular; (5) inconspicuous supratympanic fold; (6) tympanum distinct anteroventrally; (7) snout long and protruding in lateral view; (8) nares oriented ventrolaterally, situated near tip of snout; (9) Finger II smaller than Finger I when fingers adpressed; (10) tip of Finger IV reaching distal edge of distal subarticular tubercle on Finger III when fingers adpressed; (11) distal subarticular tubercle distinct on Finger III and IV, not visible on the other fingers; (12) Finger III swollen dorsally and preaxially in males, extending largely towards dorsal surface of hand forming a cream-coloured gland basally; (13) fringes present on all fingers, particularly developed postaxially on Finger I and prexially on Fingers II and III, in males and females; (14) toes basally webbed, with well-developed fringes on all toes, more developed preaxially on Toes II, III and IV; (15) tarsal keel well-defined, slightly curved; (16) glandular supracarpal pad present in both sexes (larger and more glandular in males); (17) cloacal tubercles present; (18) paracloacal mark present (orangish to light brown in life, cream to grey in preservative); (19) dorsolateral stripe absent; (20) oblique lateral stripe present, solid, undulating (cream but sometimes white anteriorly, yellow at groin level in life, white in preservative), lateral band in life uniformly dark brown/black in males, brown in females, lower flank grey with white speckles, more or less extensively yellowish orange in the axillary and the groin regions; (21) ventrolateral stripe absent; (22) sexual dichromatism in throat colour pattern present, in life light grey in males with sparse minute black melanophores, evenly and entirely yellow in females; (23) sexual dichromatism in ventral colour pattern present, in life abdomen entirely or only posteriorly yellowish orange in males, uniformly bright yellowish orange in females; (24) iris with metallic pigmentation and pupil ring interrupted ventrally and dorsally by transversal black pigmentation; (25) median lingual process as long as wide, tapered, bluntly pointed, smooth (non-papillate), reclined in pit; (26) call 0.44–0.69 s in length, consisting of a train of 5–11 notes ranging 0.028–0.036 s in length and spaced by intervals of 0.024–0.030 s with a dominant frequency at 4.55–5.02 kHz (n = 7) ( Fig. 4 , Table 2); (27) type 4 tadpole ( Orton 1953), exotrophic, with a functional mouth with marginal papillae and labial teeth ( Fig. 5 , Table 3).

Morphological comparisons with other Anomaloglossus . The only other species group co-occurring with the Anomaloglossus stepheni group is the A. degranvillei group, represented by A. blanci Fouquet, Vacher, Courtois, Villette, Reizine, Gaucher, Jairam, Ouboter, and Kok, 2018 , A. degranvillei ( Lescure, 1975) , A. dewynteri Fouquet, Vacher, Courtois, Villette, Reizine, Gaucher, Jairam, Ouboter, and Kok, 2018 and A. surinamensis Ouboter and Jairam, 2012 . Anomaloglossus saramaka sp. nov. can be distinguished from species of the A. degranvillei group by its basal webbing (moderate in species of the A. degranvillei group), smaller fringes that are more developed on Toes II-IV (well-developed fringes on all toes) and the presence of a solid oblique lateral stripe (absence). Besides these two groups, all the other described Anomaloglossus species exclusively occur in Pantepui (i.e., the Guiana Shield highlands, see Kok et al. 2018) and have moderate to extensive toe webbing ( Barrio-Amorós 2006; Barrio-Amorós & Brewer-Carías 2008; Barrio-Amorós et al. 2004, 2010; Fouquet et al. 2015; Kok et al. 2010; La Marca 1997; Meinhardt & Parmalee 1996; Noble 1923; Rivero 1961) except A. meansi Kok, Nicolaï, Lathrop and MacCulloch, 2018 , A. kaiei ( Kok, Sambhu, Roopsind, Lenglet and Bourne, 2006) , A. rufulus ( Gorzula, 1990) and A. roraima ( La Marca, 1997) . However, unlike A. saramaka sp. nov., all these species lack an oblique lateral stripe.

Within the Anomaloglossus stepheni group (comparisons follow below), Anomaloglossus saramaka sp. nov. is morphologically most similar to A. baeobatrachus , A. leopardus , A. mitaraka and A. sp. “Bakhuis” (see below) and can easily be confused with these species.

Anomaloglossus saramaka sp. nov. can mainly be distinguished from A. baeobatrachus by (1) larger body size (mean = 19.3; range 18.6–19.9 mm in males [n = 10] and mean = 20.3; range 19.9–21.6 mm in females [n = 6] in A. saramaka sp. nov. vs mean = 16.2; range 14.8–17.1 mm in males [n = 16] and mean = 18.4; range 17.3–19.4 mm in females [n = 4] in A. baeobatrachus ); (2) venter mostly yellowish orange in males in A. saramaka sp. nov. (presence of a cream/white central patch in A. baeobatrachus ); (3) call with lower note rate (mean = 14.6, range 14.0–15.3 notes/s in A. saramaka sp. nov. [n = 7] vs mean = 16.2, range 15.6–16.8 notes/s in A. baeobatrachus [n = 9]) ( Table 2).

Anomaloglossus saramaka sp. nov. can mainly be distinguished from A. leopardus by (1) narrow, poorly defined dark brown bars on legs (broad and conspicuous in A. leopardus ); (2) venter mostly yellowish-orange in males in A. saramaka sp. nov. (presence of a more or less extensive cream/white central patch in A. leopardus ); (3) shorter advertisement call (mean = 0.51, range 0.38– 0.69 s in A. saramaka sp. nov. [n = 7] vs mean = 1.52, range 1.08– 2.00 s in A. leopardus [n = 4]); (4) fewer notes in calls (6–11 in A. saramaka sp. nov. [n = 7] vs 14–28 in A. leopardus [n = 4]) ( Table 2).

Anomaloglossus saramaka sp. nov. can mainly be distinguished from A. mitaraka by (1) venter mostly yellowish orange in males in A. saramaka sp. nov. (presence of a more or less extensive cream/white central patch in A. mitaraka ); (2) shorter advertisement call (mean = 0.51, range 0.38– 0.69 s in A. saramaka sp. nov. [n = 7] vs mean = 1.04, range 0.74– 1.23 s in A. mitaraka sp. nov. [n = 6]); (3) higher note rate call (mean = 14.6, range 14.0–15.3 note/s in A. saramaka sp. nov. [n = 7] vs mean = 11.43 note/s, range 10.8–12.3 in A. mitaraka [n = 6]) ( Table 2).

Anomaloglossus saramaka sp. nov. can mainly be distinguished from A. apiau by (1) solid oblique lateral stripe in A. saramaka sp. nov. (partial, only present as a series of conspicuous white dots extending from groin midway along flank in A. apiau ); (2) shorter advertisement call (mean = 0.51, range 0.38– 0.69 s in A. saramaka sp. nov. [n = 7] vs mean = 19.6, range 7.0– 39.4 s in A. apiau [n = 10]).

Anomaloglossus saramaka sp. nov. can mainly be distinguished from A. stepheni ( Figs. 2‒3 , Table 1) by (1) larger body size (mean = 19.3; range 18.6–19.9 mm in males [n = 10] and mean = 20.3; range 19.9–21.6 mm in females [n = 6] in A. saramaka sp. nov. vs mean = 17.2, range 16.5–18.0 mm in males [n = 10] and mean = 17.3, range 17.0–18.0 mm in females [n = 5] [from Martins 1989] in A. stepheni ); (2) skin on dorsum finely granular in A. saramaka sp. nov. (evenly tuberculate in A. stepheni ); (3) ventral colouration mostly yellowish orange in males in A. saramaka sp. nov. (uniformly cream or white in A. stepheni ); (4) longer advertisement call (mean = 0.51, range 0.38– 0.69 s in A. saramaka sp. nov. [n = 7] vs mean= 0.25 s, range 0.18– 0.29 s in A. stepheni [n = 4]); (5) lower note rate call (mean = 14.6, range 14.0–15.3 note/s in A. saramaka sp. nov. [n = 7] vs mean = 21.3, range 20.2–22.6 note/s in A. stepheni [n = 4]) ( Table 2).

Description of the holotype. An adult male, 18.9 mm SVL; body robust; head wider than long, HL 95 % of HW; HL 33 % of SVL; dorsal skin finely granular, one enlarged tubercle on each eyelid, snout long (SL 52 % 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 29 % of HL, 75 % of ED. Tympanum distinct anteroventrally; supratympanic fold inconspicuous; choanae small, drop shaped, located anterolaterally.

Forelimb slender, skin tuberculate; HAND 24 % of SVL; Finger I longer than Finger II when fingers adpressed; fingers large and flattened; webbing absent on fingers; lateral fringes present on all fingers, particularly developed on postaxial edge of Finger I and on preaxial edges of Finger II and III; Finger III distinctly swollen dorsally and preaxially, swelling largely extending towards dorsal surface of hand; tip of Finger IV reaching distal edge of distal subarticular tubercle on Finger III when fingers adpressed; finger discs expanded, wider than long, about 1.5 times width of digit; width of disc on Finger III 0.6 mm; discs with distinct dorsal scutes; relative lengths of adpressed fingers III> IV> II> I; palmar tubercle large, heart-shaped, 0.8 mm in diameter (larger than disc on Finger III), thenar tubercle elliptic, small (equal to disc on Finger III in maximum diameter), half the size of palmar tubercle, well separated from palmar tubercle; only basal subarticular tubercles on fingers are conspicuous; distal subarticular tubercle of Finger III and IV are almost inconspicuous, basal subarticular tubercles on Fingers I and II the largest, followed by subarticular tubercle and basal subarticular tubercle on Finger III.

Hind limb robust, skin tuberculate; TL 48 % of SVL; heels in contact when hind limbs are flexed at right angles to the sagittal plane of body; FL 43 % 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. Width of disc on Toe IV 0.7 mm. Foot basally webbed; lateral fringes present on all toes, more developed preaxially on Toes II, III and IV. Toe webbing formula I 1+ ‒ 1- II 1+ ‒ 1- III 1+ ‒ 1+ IV 0 ‒ 1+ 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 slightly curved at proximal end. Metatarsal fold strong.

Colour of holotype in life. Dorsal colour uniformly dark brown. Oblique lateral stripe solid, continuous, undulating, anteriorly brownish white, cream in the middle and yellow near groin ( Fig. 2 ). Black lateral band below oblique lateral stripe, tapering posteriorly, extending from tip of snout to groin and containing the indistinct dorsal part of tympanum. Upper lip brownish white with a few small white speckles. Lower flank (below black lateral band) grey with white speckles with yellowish orange extensions from the axillary and the groin region. Throat grey covered with minute melanophores, more densely laterally; belly anteriorly greyish white, yellowish orange laterally and posteriorly, ventral surfaces of thighs and arms yellowish orange. Iris with coper metallic pigmentation and pupil ring interrupted dorsally and ventrally by transversal pigmentation ( Fig. 2 ).

Upper and lower arm reddish brown dorsally with brown ill-defined spots and white speckles. Bright yellow spot at junction of upper arm with body, and anterior part of upper arm with a black band. Black glandular spot at junction between lower arm and hand, followed by a cream coloured part of the swollen gland extending on Finger III. Dorsal surfaces of thigh, shank and tarsus dark brown with ill-defined dark brown, almost black transverse bars, and ill-defined dark brown blotches. Paracloacal marks light brown, elongate. Toes and digits with small light blueish speckles dorsally and laterally. Palms and soles dark brown.

Colour of holotype in preservative. After four years in 70 % ethanol, colours of the specimen faded, and the dorsal colouration now varies from pale brown to grey with a brown interorbital bar; yellowish orange ventral colouration faded to white ( Fig. 3 ). Bluish speckles and orange/reddish marks turned white as well.

Variation among type specimens. Measurements (range, mean, and standard deviation) of the type series are provided in Table 1. Colouration of limbs varies from brown to reddish brown, females being more reddish. Colour of dorsum varies from light brown to dark brown and some specimens (e.g., NZCS-A1206, field n°AF3844) dis-play diffuse dark brown blotches, more frequently on the interorbital region. Colour of oblique lateral stripe varies from white to orangish. Overall dorsal and lateral colouration and tuberculation may vary with light intensity, time of the day and probably reproductive activity as males carrying tadpoles apparently display overall lighter colours, smoother skin and sharper contrasts, whereas calling males are very dark coloured and highly tuberculate. Ventral colouration of female is entirely yellowish orange while the yellowish orange parts are always limited to the posterior region of throat in males. Vocal sac, slits and minute black melanophores on throat only observed in males as well as swelling of Finger III.

Advertisement call. Seven collected specimens calling from the leaf litter were recorded from a distance of about 2 m and at temperatures ranging from 22 to 24°C. Descriptive statistics of call parameters are presented in Table 2. Anomaloglossus saramaka sp. nov. emits trains (call length mean = 0.51, range 0.38– 0.69 s) of 6–11 short notes (note length mean = 0.028 s; range 0.024 –0.031 s; inter-note interval mean = 0.05 s; range 0.04– 0.05 s). The spectral structure of the note has a developed harmonic structure and the dominant frequency is 4.84 kHz on average (range 4.55–5.02 kHz) with a slight upward modulation (ca. 0.3 kHz) ( Fig. 4 , Table 2).

Larval morphology. The following description is based on six tadpoles at stage 27, 28 and 29 ( Fig. 5 , Table 3). Tadpoles correspond to a type 4 tadpole of Orton (1953); exotrophic; body skin smooth; TL 12.95–17.19 mm; BL 4.33–5.89 mm, 33–36 % of TL, 146–165 % of BW, 191–238 % of BH; BW 123–149 % of BH ( Table 3); body ovoid, snout round in dorsal and lateral view; eyes positioned and directed laterally; ED 0.45–0.60 mm, 53–64 % of IOD; IOD larger than IND; nares frontally positioned and directed laterodorsally; narial opening circular in lateral view; END 0.45–0.56 mm. Spiracular tube sinistral, conical, projecting posterodorsally, its tip located at 60–65 % of BL posteriorly to snout. Lateral-line system inconspicuous. Caudal musculature highest at its base, tapering posteriorly, terminating at tail tip; tail tip rounded; upper fin originating at junction of body and tail, gradually increasing in height to about 3/4 of tail; UTF 40–53 % of TMH; LTF 33–47 % of TMH; MTH 13–15 % of TL ( Fig. 5 , Table 3).

Mouth ventral, oral disc strongly emarginated, width 1.40–1.50 mm. Labial teeth long, in single rows, LTRF 2(2)/3. A-2 consisting of two short rows, separated by a large and deep gap; P-1 not interrupted. Marginal papillae long, of equal size on each labium, tapered, blunt-tipped, in a single row, evenly distributed; median gap on upper labium approximately 2/3 the length of A-1; jaw sheaths large, serrated, lower jaw sheath broadly V-shaped.

In life, the entire body is dark grey with abundant golden flecks, particularly on dorsum. Golden flecks become scarce ventrally. Posteriorly, dark grey coloration fades and tail becomes translucent.

The tadpole of Anomaloglossus saramaka sp. nov. can be distinguished from those of Anomaloglossus of the stepheni group that are endotrophic ( A. stepheni and A. baeobatrachus ) by the presence of a functional mouth with marginal papillae and labial teeth. However, it virtually cannot be distinguished from the tadpole of A. mitaraka based on morphological evidence.

Distribution and natural history. Anomaloglossus saramaka sp. nov. is a diurnal species inhabiting the leaf litter in primary forest at low to mid elevations (from 100 to 500 m elevation). The species is usually found close to streams next to which it deposits its exotrophic tadpoles into puddles, but some specimens were found more than 50 m away from water bodies.

Males call all day long when the weather is rainy but calling activity is otherwise limited to sunset and sunrise. Breeding occurs during the rainy season, from December to July. The rainfall between December and April being highly variable, the reproduction seems to be concentrated in the second half (May-July) of this period. The males respond to intraspecific playbacks with shorter and more rapidly emitted note trills. Males are territorial, their small territories being spaced at least two meters apart. They usually call slightly above the leaf litter, exposed on a branch or a dead leaf. Eggs are probably deposited under or in the fold of a dead leaf. After hatching, the male carries the tadpoles (up to 9) to a small water body. We observed what appears to be shredding skin with the tadpoles being carried, which could represent food provisioning during transportation, although this remains very speculative.

Only two populations are known to date, one in Brownsberg and one in Voltzberg, both in Suriname. The species might occur between these two localities and probably in surrounding areas. However, it is unlikely that the species extends much further since other species occur nearby (A. sp. “Bakhuis”, A. mitaraka , A. leopardus ), and that other species of this group with exotrophic tadpoles display a strong allopatric pattern of distribution. Goldmining activities in northeastern Suriname have been increasing during the last decade ( Dezécache et al. 2017) and likely threaten a large part of the range of the new species even within protected areas such as Brownsberg Nature Park.

Figures

FIGURE 2. Two males (top) and one female (bottom) of the two species described herein, Anomaloglossus saramaka sp. nov. and A. vacheri sp. nov., along with one male of the three additional species of the A. stepheni group occurring in Suriname.

FIGURE 3. Views of dorsum, venter, left hand, left foot of the holotype of A. saramaka sp. nov. (left) and of the holotype of A. vacheri sp. nov. (right).

FIGURE 4. Spectrograms and oscillograms of the advertisement calls of the two species described herein, Anomaloglossus saramaka sp. nov. and A. vacheri sp. nov., along with the calls of four additional described species of the A. stepheni group; in a 2 s time window (top) and a close-up in a 0.1 s time window (bottom).

FIGURE 5. The tadpole of Anomaloglossus saramaka sp. nov. and A. vacheri sp. nov., and pictures of habitat and males in situ. Top: ventral and lateral view of AF3865_B at Gosner stage 29, a close-up of the mouth, a male (MNHN_RA_2019.0029, field n°AF3897) carrying 9 tadpoles (note the shredding skin), and habitat where males deposit tadpoles during the wet season (here dry). Bottom: ventral and lateral view of AF3422_A at Gosner stage 30, a close-up of the mouth, a picture of the specimen in situ within a small cavity in the lateritic crust indicated by an arrow, and the calling male nearby on lateritic crust.