Anomaloglossus meansi, Kok, Philippe J. R., Nicolai, Michael P. J., Lathrop, Amy & MacCulloch, Ross D., 2018

Kok, Philippe J. R., Nicolai, Michael P. J., Lathrop, Amy & MacCulloch, Ross D., 2018, Anomaloglossusmeansi sp. n., a new Pantepui species of the Anomaloglossusbeebei group (Anura, Aromobatidae), ZooKeys 759, pp. 99-116 : 99

Anomaloglossus meansi sp. n. Figures 3, 4; Table 1

Anomaloglossus sp. Ayanganna Grant et al. 2006: 120-121, 2017: S66.

Anomaloglossus cf. praderioi Kok 2010: 66.

Anomaloglossus sp. B Kok et al. 2012: supplementary information.

Holotype.

ROM 43896, adult male from the vicinity of Camp 2 on the Wokomung Massif, Potaro-Siparuni District, Guyana (05°06.5833'N; 059°49.2667'W), 1234 m elevation, collected by A. Lathrop and R. James on 30 October 2004.

Paratypes

(n = 10). An adult male (ROM 39639) from the northeast plateau of Mount Ayanganna, Cuyuni-Mazaruni District, Guyana (05°24.1'N; 059°57.4'W), 1490 m elevation, collected by R. D. MacCulloch, A. Lathrop and C. Cox on 26 October 2000; four adult females (ROM 43320, ROM 43329, ROM 43331, ROM 43332) from the vicinity of Camp 2 on the Wokomung Massif, Potaro-Siparuni District, Guyana (05°06.5833'N; 059°49.2667'W), 1234 m elevation, collected by A. Lathrop, R. D. MacCulloch and S. Khan between 26-31 October 2004; one adult female (ROM 43323) from the vicinity of Camp 3 on the Wokomung Massif, Potaro-Siparuni District, Guyana (05°05.65'N; 059°50.5833'W), 1411 m elevation, collected by A. Lathrop, R. D. MacCulloch and S. Khan on 3 November 2004; one juvenile (ROM 43322) from the vicinity of Camp 2 on the Wokomung Massif, Potaro-Siparuni District, Guyana (05°06.5833'N; 059°49.2667'W), 1234 m elevation, collected by C. Alban on 26 October 2004; two juveniles (ROM 43324, ROM 43325) from the vicinity of Camp 2 on the Wokomung Massif, Potaro-Siparuni District, Guyana (05°06.5833'N; 059°49.2667'W), 1234 m elevation, collected by A. Lathrop, R. D. MacCulloch and S. Khan between 28-31 October 2004; and one adult male (CPI11000) from Falls Camp on the Wokomung Massif, Potaro-Siparuni District, Guyana (05°05.4333'N; 059°50.2833'W), ca. 1371 m elevation, collected by D. Bruce Means on 24 July 2003.

Diagnosis.

The following characteristics pertain to preserved specimens unless otherwise noted. A medium-sized Anomaloglossus differing from other species in the genus by the following combination of characters: (1) mean SVL in males 18.53 mm (18.15-18.86 mm, n = 3), mean SVL in females 19.15 mm (17.66-21.26, n = 5); (2) skin on dorsum shagreened, venter smooth; (3) tympanic annulus visible anteroventrally; (4) Fingers I and II subequal in length, FI = FII when fingers adpressed; (5) tip of Finger IV not surpassing the base of the distal subarticular tubercle on Finger III when fingers adpressed; (6) distal subarticular tubercle on Finger III and IV present; (7) Finger III swollen in males (conspicuous pre- and postaxial swelling in breeding males); (8) fringes on fingers absent; (9) toes basally webbed, fringes on toes absent; (10) tarsal keel well defined, slightly tubercle-like and weakly curved at proximal end; (11) black arm gland absent, glandular supracarpal pad present in both sexes (larger and more glandular in males); (12) cloacal tubercles absent; (13) pale paracloacal mark present; (14) in life, thin dorsolateral stripe present, from tip of snout to tip of urostyle (not visible, or only barely distinguishable in preservative); (15) ventrolateral stripe absent, but presence of irregular white blotches on the lower flank; (16) oblique lateral stripe absent; (17) sexual dichromatism in throat colour pattern: throat heavily pigmented with melanophores in males (dark brown to black in life), immaculate cream in females (yellowish-orange in life); (18) sexual dichromatism in ventral colour pattern: belly pigmented with melanophores in males, immaculate cream in females; (19) in life, iris metallic reddish bronze with fine dark brown reticulation; (20) large intestine extensively pigmented; (21) testes cream, unpigmented; (22) mature oocytes partly pigmented; (23) median lingual process small, longer than wide, tapered; (24) maxillary teeth present, small.

Comparisons.

Anomaloglossus meansi sp. n. can mainly be distinguished from the four described species belonging to the degranvillei group [sensu Vacher et al. 2017 and Fouquet et al. 2018, i.e. A. blanci Fouquet, Vacher, Courtois, Villette, Reizine, Gaucher, Jairam, Ouboter & Kok, 2018, A. degranvillei (Lescure, 1975), A. dewynteri Fouquet, Vacher, Courtois, Villette, Reizine, Gaucher, Jairam, Ouboter & Kok, 2018 and A. surinamensis Ouboter & Jairam, 2012; characters in parentheses] by having FI = FII when fingers adpressed (FI> FII), the tympanic annulus anteroventrally conspicuous (inconspicuous), and a conspicuous thin dorsolateral stripe from tip of snout to tip of urostyle (absent or inconspicuous).

Anomaloglossus meansi sp. n. can mainly be distinguished from the four described species belonging to the stepheni group [sensu Vacher et al. 2017, i.e. A. apiau Fouquet, Souza, Nunes, Kok, Curcio, Carvalho, Grant & Rodrigues, 2015, A. baeobatrachus (Boistel & de Massary, 1999), A. leopardus Ouboter & Jairam, 2012 and A. stepheni (Martins, 1989); characters in parentheses] in lacking an oblique lateral stripe (present, even if short and discontinuous in A. apiau ), and in having a conspicuous thin dorsolateral stripe from tip of snout to tip of urostyle (absent).

Anomaloglossus meansi sp. n. can mainly be distinguished from the three described species belonging to the megacephalus group [sensu Grant et al. 2017, i.e. A. megacephalus Kok, MacCulloch, Lathrop, Willaert & Bossuyt, 2010, A. verbeeksnyderorum Barrio-Amorós, Santos & Jovanovic, 2010, A. wothuja ( Barrio-Amorós, Fuentes-Ramos & Rivas-Fuenmayor, 2004); characters in parentheses] in having only basal toe webbing (moderate to extensive), in lacking an oblique lateral stripe (present, even if short and/or discontinuous), and in having a conspicuous thin dorsolateral stripe from tip of snout to tip of urostyle (absent).

Compared to the other five species belonging to the beebei group [sensu Grant et al. 2017, i.e. A. beebei (Noble, 1923), A. kaiei (Kok, Sambhu, Roopsind, Lenglet & Bourne, 2006), A. praderioi , A. roraima (La Marca, 1997) and A. rufulus (Gorzula, 1990)], A. meansi sp. n. can easily be distinguished from A. beebei by its larger size in males (maximum SVL 18.86 mm in A. meansi [n = 3,] versus maximum SVL 16.80 mm [n=18] in A. beebei ), smooth ventral skin (granular in A. beebei ), basal toe webbing (moderate in A. beebei ), and in having a conspicuous thin dorsolateral stripe from tip of snout to tip of urostyle (absent or originating from the posterior corner of eye); from A. kaiei in having a conspicuous thin dorsolateral stripe from tip of snout to tip of urostyle (originating from the posterior corner of eye in A. kaiei ) and a black throat in preserved males (greyish, never black in A. kaiei ); from A. roraima by its larger size in females (maximum SVL 21.26 mm in A. meansi [n = 3,] versus maximum SVL 19.30 mm [n = 18] in A. roraima ), smooth ventral skin (granular in A. roraima ), and in having a conspicuous thin dorsolateral stripe from tip of snout to tip of urostyle (when present originating from the anterior or posterior corner of eye in A. roraima ); from A. rufulus in having a conspicuous thin dorsolateral stripe from tip of snout to tip of urostyle (absent in A. rufulus ) and the posterior part of belly unmarked (heavily marbled in A. rufulus ). Anomaloglossus meansi sp. n. is most similar to A. praderioi with which it shares a conspicuous thin dorsolateral stripe from tip of snout to tip of urostyle but is immediately distinguished by its smaller size in males (maximum SVL 18.86 mm in A. meansi [n = 3,] versus maximum SVL 22.40 mm [n = 11] in A. praderioi ), the absence of fringes on toes (extensive in A. praderioi ), Finger III with pre- and postaxial swelling in breeding males (preaxial swelling only in A. praderioi ), less toe webbing (compare Figure 3 with figure 2 in Kok 2010), and the lack of black spots on chest and lower flanks in males (present in A. praderioi ).

Compared to the remainder 12 Anomaloglossus species not yet assigned to any group [ A. ayarzaguenai (La Marca, 1997), A. breweri ( Barrio-Amorós, 2006), A. guanayensis (La Marca, 1997), A. moffetti Barrio-Amorós & Brewer-Carías, 2008, A. murisipanensis (La Marca, 1997), A. parimae (La Marca, 1997), A. parkerae (Meinhardt & Parmelee, 1996), A. shrevei (Rivero, 1961), A. tamacuarensis (Myers & Donnelly, 1997), A. tepequem Fouquet, Souza, Nunes, Kok, Curcio, Carvalho, Grant & Rodrigues, 2015, A. tepuyensis (La Marca, 1997) and A. triunfo ( Barrio-Amorós, Fuentes-Ramos & Rivas-Fuenmayor, 2004); characters in parentheses], A. meansi sp. n. mainly differs in having only basal toe webbing (moderate to extensive), and in having a conspicuous thin dorsolateral stripe from tip of snout to tip of urostyle (absent).

Description of the holotype.

Adult male (ROM 43896; Figure 3), 18.58 mm SVL, in suboptimal state of preservation (extensive ventral incisions, dorsal skin locally damaged); body robust; head as wide as long, HL 99.7% of HW, HW 32% of SVL; dorsal skin shagreened; ventral skin smooth; snout moderately long, SL 47% of HL, 128% of EL, round in dorsal view, protruding in lateral view, extending past lower jaw; nares located close to tip of snout, directed posterolaterally, visible from front, barely visible in dorsal and ventral views, EN 28% of HL, 77% of ED, EN 60% of SL, TSL 49% of SL; posterior rim of naris bordered posteriorly by an inconspicuous crescent-shaped ridge; IND 40% of HW; canthus rostralis rounded; loreal region concave; IOD 104% of EL, longer than upper eyelid; postrictal tubercles low and inconspicuous; tympanic membrane inconspicuous, round, concealed posterodorsally by a diffuse supratympanic swelling; tympanic annulus visible anteroventrally, TYM 52 % of EL; choanae small, circular, located anterolaterally. Maxillary teeth present, small. Tongue longer than wide, free posteriorly, with rounded margin, small median lingual process longer than wide, tapered. Vocal slits bilateral, large, extending from edge of tongue to angle of jaw.

Forelimb swollen, robust, 94% of FAL. Ulnar fold absent, metacarpal ridge absent; swollen, glandular supracarpal pad present, heavily pigmented with melanophores; hand moderate in size, 24% of SVL, 75% of HW; relative length of fingers III>II=I=IV; pre- and postaxial swelling on third finger (i.e. Finger III swollen); fingers without fringes; tip of Finger IV not reaching distal subarticular tubercle on Finger III when fingers adpressed; finger discs expanded, wider than long, about 1.4 times width of digit; width of disc on Finger III 0.52 mm; palmar tubercle large, egg shaped, 0.72 mm (larger than Finger III disc), thenar tubercle smaller, elliptical; one or two round to ovoid subarticular tubercles (one each on Fingers I and II, two each on Fingers III and IV, with distal tubercle on Finger IV less conspicuous).

Hind limb robust, moderately long, with heel of adpressed leg reaching posterior corner of eye; skin granular with no cloacal tubercles discernible (but this could be an artefact of preservation); TL 46% of SVL, heels not in contact when hind limbs are flexed at right angle to sagittal plane of body; FL 38% of SVL; relative length of adpressed toes IV>III>V>II>I; Toe I very short, its tip barely reaching the base of subarticular tubercle of Toe II when 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 0.67 mm; toes basally webbed, lateral fringes absent; one to three round to ovoid subarticular tubercles (one each on Toes I and II, two each on Toes III and V, and three on Toe IV, with distal tubercle on Toe IV the smallest and least conspicuous). Inner metatarsal tubercle protuberant elliptical, 0.47 mm in length, outer metatarsal tubercle round, protuberant, pigmented, 0.35 mm in diameter. No medial metatarsal tubercle discernible. Tarsal keel slightly tubercle-like and weakly curved at proximal end, extending distally to preaxial edge of Toe I. Metatarsal fold not visible.

Colour of holotype in life.

Dorsal ground colour chestnut brown with a short black middorsal line between shoulders. A black line from snout tip through eye, extending dorsolaterally to groin. A narrow pale brown dorsolateral stripe above this line, blending into the chestnut dorsal ground colour. Upper surface of limbs light brown proximally, becoming dark brown distally. Flanks reddish brown with yellow spots on lower flanks. Venter pale brown with dark brown mottling, throat very dark brown to black. Underside of limbs orange-red, changing to dark reddish brown on distal forearms.

Colour of holotype in preservative.

After more than 13 years in preservative, dorsal ground colour became dark chestnut brown with a short middorsal black longitudinal line in the scapular region. No other dorsal marking present. Dorsal surface of arms varies from light brown proximally to dark brown, purplish-black towards the granular supracarpal pads. Dorsal surface of legs light brown with darker brown markings. Flanks dark brown to purplish-black with pale spots on lower flanks. Narrow pale brown dorsolateral stripes indistinguishable from dorsal ground colour, although the black dorsolateral stripe remains visible. Throat black, heavily pigmented with melanophores; belly cream, pigmented with melanophores (less densely distributed than on throat). Pale paracloacal marks are visible. Palms dark brown, soles medium brown (Figure 3).

Measurements of holotype

(in mm).SVL = 18.58; HL = 5.91; HW = 5.93; IOD = 2.26; EN = 1.68; SL = 2.77; TSL = 1.35; EL = 2.16; TYM = 1.12; IND = 2.39; HAND I = 3.06; HAND II = 3.2; HAND III = 4.44; HAND IV = 3.09; WFD = 0.52; FAL = 3.81; THL = 7.80; TIL = 8.61; TAL = 4.48; FL = 7.08; WTD = 0.67.

Sexual dimorphism and variation within the type series.

Males are usually smaller than females, 18.15-18.86 mm SVL (n = 3) versus 17.66-21.26 mm SVL (n = 5) in females, with Finger III distinctly swollen in breeding males (Figure 3). Supracarpal pads are less extended and less glandular in females and juveniles than in males. Colouration is sexually dichromatic; throat heavily pigmented black in males (immaculate yellowish-orange in females), and belly yellowish-orange pigmented with melanophores in males (immaculate yellowish-orange in females) (Figure 3). Venter immaculate in juveniles, although small pigmented areas on throat may occur (presumably in juvenile males).

Morphometric variation is summarized in Table 1, illustrations of a male and a female paratype in life are in Figure 4. Snout in dorsal and ventral views varies from round to truncate (the latter more particularly in females, see Figure 3).

There is substantial variation in colour among preserved individuals, obviously due to preservation artefact (CPI11000 for instance is much lighter than all other individuals). Lower lip pigmented in all male and juvenile individuals, but only in three out of five females. The interorbital region is usually darker than the dorsal ground colour. A short middorsal dark brown/black longitudinal line usually present in the scapular region. One female (ROM 43329) has a diffuse diamond shape marking on the anterior dorsum. Upper surface of arms and legs is cream to dark brown, with darker markings on legs. Palms and soles are light to dark brown. Flanks vary from cream to very dark purplish brown.

Distribution and natural history.

The only localities documented for the new species are depicted in Figure 2. Specimens were collected in cloud forest (Figure 5), on the ground or low vegetation. Most were collected after nightfall, although one adult and one juvenile were collected during daylight. Specimens were collected on mountain flanks, not summits; at 1490 m on Ayanganna, and at 1234 m, 1371 m and 1411 m on Wokomung. The majority of specimens (eight) were collected at 1234 m on Wokomung. Fewer were collected at higher elevations; only one each at 1490 m on Ayanganna, 1371 m and 1411 m on Wokomung. This may have been because of habitat differences; high-canopy open forest at lower elevation and dense, low-canopy vegetation at higher elevations (see Discussion).

Etymology.

It is a great pleasure to name this new species after our friend and colleague D. Bruce Means, indefatigable explorer of the "islands in the sky", and who collected one specimen of the new species and contributed with photographs and data. Thanks to his extensive fieldwork, Bruce Means greatly contributed to our understanding of the distribution, ecology, and taxonomy of Pantepui amphibians and reptiles. The specific epithet should be treated as a noun in the genitive case.

Phylogenetic relationships.

The new species was recovered sister to Anomaloglossus praderioi by Grant et al. (2006, 2017) and Kok et al. (2012) (see Figure 1). Uncorrected p distance in the “barcoding” fragment of the 16S rRNA gene [ Vences et al. (2005); based on the sequences used in Grant et al. (2017) and calculated in PAUP 4.0a161 ( Swofford 2002)] is 4.3-4.8% between Anomaloglossus praderioi and A. meansi sp. n. Genetic divergence between populations of A. praderioi from the slopes of Roraima-tepui and Maringma-tepui is 0.2%, whereas divergence between populations of A. meansi sp. n. from Mount Ayanganna and the Wokomung Massif is 0.9-1.0%.

Conservation status.

Anomaloglossus meansi sp. n. is only known from four localities and the 11 specimens used in the description. Virtually nothing is known about its ecology, breeding behaviour and population density. Given the uncertainty on its population status we suggest Anomaloglossus meansi sp. n. to be listed as Data Deficient according to the IUCN Red List category guidelines (2014).

Discussion.

Although Ayanganna and Wokomung are close neighbours, the habitats on their slopes are not exactly similar. The slopes of Ayanganna are a series of relatively flat poorly drained plateaus alternating with steeper slopes. Collecting activities were concentrated on the plateaus, where the vegetation consists of dense, low-canopy high-tepui forest, with a dense understory of woody shrubs and large terrestrial bromeliads ( MacCulloch and Lathrop 2009).

The slopes of Wokomung have no large flat plateaus. Habitat at the collecting sites consists of well-drained slopes covered in lower montane cloud forest with some epiphytes and medium density understory, including scattered terrestrial bromeliads. Streams were common on the slopes ( MacCulloch et al. 2006). The majority of specimens were found in this habitat, and this may indicate that Anomaloglossus meansi sp. n. prefers this to other habitat types; or is a reflection of collecting effort in these habitats.

Species in the Anomaloglossus beebei group are currently only known from east of the Rio Caroní, in the Eastern Pantepui District. Anomaloglossus rufulus is restricted to the highlands of the eastern part of the Chimantá Massif in Venezuela, whereas A. kaiei has a rather large distribution in the uplands of the Pakaraima Mountains of Guyana (Figure 2). The sister species A. roraima and A. beebei are allopatric, A. roraima being restricted to the highlands of the eastern tip of the Eastern Tepui Chain, whereas A. beebei is reported further to the east in the uplands of Kaieteur National Park, the Wokomung Massif and Mount Ayanganna (Figure 2). A similar spatial distribution is detected in the sister species A. praderioi and A. meansi sp. n., which are also allopatric, with A. praderioi reported from the uplands of the Eastern Tepui Chain, whereas A. meansi sp. n. is only known further to the east in the uplands of Mount Wokomung and Mount Ayanganna.

As mentioned above, virtually nothing is known about the ecology of A. meansi sp. n. Based on its phylogenetic position it is likely this species has an exotrophic, lentic tadpole (Figure 1). Comprehensive ecological data are crucial for the assessment of species conservation status, but these assessments are known for a few species only in the Pantepui region and there is a high risk that population declines remain unnoticed in such remote areas.

Two additional phylogenetically distinct species of Anomaloglossus remain to be described in the megacephalus group (see Grant et al. 2017; the authors, in progress), but several locally restricted Anomaloglossus species probably await discovery ( Vacher et al. 2017).