Research Article |
Corresponding author: Philippe J.R. Kok ( philippe.kok@vub.ac.be ) Academic editor: Angelica Crottini
© 2018 Philippe J.R. Kok, Michaël P.J. Nicolaï, Amy Lathrop, Ross D. MacCulloch.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Kok PJR, Nicolaï MPJ, Lathrop A, MacCulloch RD (2018) Anomaloglossus meansi sp. n., a new Pantepui species of the Anomaloglossus beebei group (Anura, Aromobatidae). ZooKeys 759: 99-116. https://doi.org/10.3897/zookeys.759.24742
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Recent extinctions and drastic population declines have been documented in the Guiana Shield endemic frog genus Anomaloglossus, hence the importance to resolve its alpha-taxonomy. Based on molecular phylogenies, the literature has long reported the occurrence of an undescribed species in the Pakaraima Mountains of Guyana in the Pantepui region. We here describe this new taxon and demonstrate that in addition to divergence at the molecular level the new species differs from congeners by a unique combination of morphological characters, notably a small size (maximum SVL in males 18.86 mm, maximum SVL in females 21.26 mm), Finger I = Finger II when fingers adpressed, Finger III swollen in breeding males, fringes on fingers absent, toes basally webbed but lacking fringes, in life presence of a thin dorsolateral stripe from tip of snout to tip of urostyle, and a black throat in preserved males (immaculate cream in females). Virtually nothing is known about the ecology of the new species. We suggest the new species to be considered as Data Deficient according to IUCN standards.
Aromobatidae , diversity, Guiana Shield, Guyana, Pakaraima Mountains
In their influential work about bird diversification in the Venezuelan highlands,
Vertical isolation makes tepui ecosystems particularly sensitive to global warming (see
Taxonomy and terminology follow
Collecting activities took place on Mount Ayanganna and the Wokomung Massif, west-central Guyana (Figure
Occurrence map of the Anomaloglossus species belonging to the beebei group (coloured convex polygons); distribution of A. meansi sp. n. is depicted by yellow dots. A map of the Eastern Pantepui District; black rectangle is enlarged in B. B localities of occurrence of Anomaloglossus meansi sp. n. based on museum specimens.
Specimens were collected by hand and euthanized by immersion in a solution of MS 222 (
All morphometric data were taken from the preserved specimens by the same person (MPJN), to the nearest 0.01 mm, under a Leica stereo dissecting microscope using an electronic digital caliper. Colour pattern in life was taken from field notes and colour photographs. Sex and maturity were determined by the presence/absence of vocal slit(s) and by dissection. Comparisons of external character states are based both on original descriptions and examination of museum specimens (see Appendix for comparative material examined). Abbreviations for measurements are as follows:
SVL snout-vent length
HW head width, at level of angle of jaws
HL head length, from angle of jaw to tip of snout
IOD inter orbital distance
EN eye to naris distance, from anterior edge of eye to centre of naris
SL snout length, from anterior edge of eye to tip of snout
TSL tip of snout length, from centre of naris to tip of snout
IND internarial distance, the distance between the centres of nares
EL eye horizontal length
TYM tympanum horizontal length
HAND I–IV relative lengths of fingers, from the proximal edge of the palmar tubercle to the tip of each finger
WFD width of disc on Finger III
FAL forearm length, from elbow joint to proximal edge of metacarpal tubercle
THL thigh length, from vent opening to flexed knee
TIL tibia length, from knee to heel
TAL tarsus length, from heel to proximal edge of outer metatarsal tubercle
FL foot length, from proximal edge of inner metatarsal tubercle to tip of Toe IV
WTD width of disc on Toe IV
Anomaloglossus
sp. Ayanganna
Anomaloglossus
cf.
praderioi
Anomaloglossus
sp. B
(n = 10). An adult male (
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.
Anomaloglossus meansi sp. n. can mainly be distinguished from the four described species belonging to the degranvillei group [sensu
Anomaloglossus meansi sp. n. can mainly be distinguished from the four described species belonging to the stepheni group [sensu
Anomaloglossus meansi sp. n. can mainly be distinguished from the three described species belonging to the megacephalus group [sensu
Compared to the other five species belonging to the beebei group [sensu
Anomaloglossus meansi sp. n. in preservative. A male holotype
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).
Adult male (
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.
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.
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
(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.
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
Morphometric variation is summarized in Table
Morphometric measurements (in mm) of the type series of Anomaloglossus meansi sp. n. Abbreviations are defined in the text. Means ± SD are followed by the range in parentheses.
Character | Male (n = 3) | Female (n = 5) | Juvenile (n = 3) |
---|---|---|---|
SVL | 18.53±0.35 (18.15–18.86) | 19.15±1.48 (17.66–21.26) | 12.72±2.13 (10.69–14.94) |
HW | 5.89±0.09 (2.19–2.73) | 6.11±0.24 (5.81–6.31) | 4.28±0.60 (1.48–1.78) |
IOD | 2.39±0.30 (2.19–2.73) | 2.41±0.20 (2.17–2.72) | 1.61±0.15 (1.48–1.78) |
HL | 5.56±0.31 (5.32–5.91) | 5.48±0.28 (5.13–5.81) | 3.79±0.60 (3.13–4.29) |
EN | 1.63±0.04 (1.60–1.68) | 1.68±0.11 (1.48–1.75) | 1.17±0.26 (0.96–1.41) |
SL | 2.79±0.02 (2.77–2.82) | 2.81±0.17 (2.56–3.00) | 2.05±0.30 (1.76–2.36) |
EL | 2.37±0.17 (2.17–2.48) | 2.36±0.13 (2.22–2.51) | 1.83±0.13 (1.73–1.89) |
TYM | 1.08±0.04 (1.03–1.12) | 1.06±0.14 (0.86–1.24) | 0.69±0.15 (0.58–0.86) |
IND | 2.44±0.05 (2.39–2.48) | 2.60±0.16 (2.37–2.82) | 1.83±0.24 (1.59–2.07) |
TSL | 1.24±0.10 (1.15–1.35) | 1.41±0.10 (1.29–1.53) | 0.87±0.17 (0.74–1.06) |
HAND I | 3.12±0.20 (2.96–3.35) | 3.25±0.13 (3.10–3.45) | 1.89±0.70 (3.10–2.69) |
HAND II | 3.13±0.06 (3.07–3.2) | 3.30±0.14 (3.07–3.45) | 2.34±0.39 (2.06–2.78) |
HANDIII | 4.68±0.10 (4.26–4.44) | 4.84±0.19 (4.17–4.66) | 3.04±0.46 (2.76–3.57) |
HAND IV | 3.10±0.10 (3.00–3.2) | 3.14±0.12 (2.93–3.22) | 2.15±0.31 (1.84–2.46) |
WFD | 0.57±0.07 (0.52–0.65) | 0.55±0.06 (0.52–0.65) | 0.43±0.06 (0.37–0.47) |
FAL | 4.27±0.40 (3.81–4.56 | 4.41±0.41 (3.97–5.04) | 2.54±0.84 (1.94–3.51) |
THL | 8.29±0.42 (7.80–8.54) | 8.85±0.28 (8.52–9.18) | 5.37±1.07 (4.61–6.60) |
TIL | 8.45±0.33 (8.07–8.66) | 9.09±0.35 (8.61–9.48) | 6.13±1.13 (5.12–7.35) |
TAL | 4.47±0.21 (4.26–4.68) | 4.56±0.38 (4.05–5.02) | 3.04±0.73 (2.50–3.86) |
FL | 7.2±0.38 (7.07–7.45) | 7.86±0.38 (7.53–8.48) | 4.89±1.27 (3.82–6.29) |
WTD | 0.72±0.06 (0.67–0.78) | 0.68±0.06 (0.61–0.76) | 0.43±0.03 (0.42–0.46) |
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 (
The only localities documented for the new species are depicted in Figure
Habitat of Anomaloglossus meansi sp. n. on the Wokomung Massif A photograph (looking NE) of the highest part of the massif; the plateau in the centre of the photo is the tallest part of the entire Wokomung Massif B cloud forest at about 1385 m elevation, habitat of Anomaloglossus meansi sp. n. Photographs courtesy D. Bruce Means.
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.
The new species was recovered sister to Anomaloglossus praderioi by
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).
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 (
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 (
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
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
Two additional phylogenetically distinct species of Anomaloglossus remain to be described in the megacephalus group (see
PJRK is supported by a postdoctoral fellowship from the Fonds voor Wetenschappelijk Onderzoek Vlaanderen (FWO12A7617N). AL and RDM were supported by grants from the Royal Ontario Museum Governors and Department of Natural History. Permission to conduct this study in indigenous lands in the Pakaraima Mountains of Guyana was granted by the Guyanese Ministry of Amerindian Affairs. Research and export permits were issued by the Guyana Environmental Protection Agency. We thank the following curators and collection managers for their assistance and access to collections under their care: F.J. Bisbal, E. Camargo, R. Rivero, J. Sánchez (Museo de la Estación Biología de Rancho Grande, Maracay, Venezuela; EBRG), E. La Marca (Universidad de los Andes, Departamento de Geografía, Mérida, Venezuela; ULABG), M. Salazar (Universidad Central de Venezuela, Museo de Biología, Caracas, Venezuela; MBUCV), and J.C. Señaris (Museo de Historia Natural La Salle, Caracas, Venezuela; MHNLS). K. Roelants (Vrije Universiteit Brussel, Belgium) kindly drew the figures used in Figure
Comparative material examined
Anomaloglossus ayarzaguenai: Venezuela, Estado Bolívar, Cerro Jaua, MHNLS 12949 (holotype), MHNLS 12950–51 (2 paratypes).
Anomaloglossus beebei: Guyana, Potaro‐Siparuni District, Kaieteur National Park, IRSNB 13721–26, 13728–53, ULABG 6817 (ex IRSNB 13727).
Anomaloglossus breweri: Venezuela, Estado Bolívar, Aprada-tepui, Cueva del Fantasma, MHNLS 17044 (holotype), MHNLS 17045–46 (2 paratypes).
Anomaloglossus guanayensis: Venezuela, Estado Bolívar, Serranía de Guanay, MHNLS 10708 (holotype), MHNLS 10712–10714 (3 paratypes), 10716–10717 (2 paratypes), 10724–10725 (2 paratypes).
Anomaloglossus kaiei: Guyana, Potaro‐Siparuni District, Kaieteur National Park, IRSNB 1938 (holotype), IRSNB 1939–64 (26 paratypes), IRSNB 14420–57,
Anomaloglossus megacephalus: Guyana, Cuyuni‐Mazaruni District, Maringma-tepui, IRSNB 1986 (holotype), Mount Ayanganna,
Anomaloglossus moffetti: Venezuela, Estado Bolívar, Sarisariñama-tepui, EBRG 4645 (holotype), EBRG 4646–51 (6 paratypes).
Anomaloglossus murisipanensis: Venezuela, Estado Bolívar, Murisipán‐tepui, MHNLS 11385 (holotype).
Anomaloglossus parimae: Venezuela, Estado Amazonas, Cerro Delgado Chalbaud, ULABG 4221 (holotype), ULABG 4212–20 (9 paratypes), ULABG 4222–26 (5 paratypes).
Anomaloglossus parkerae: Venezuela, Estado Bolívar, Sierra de Lema, Salto El Danto, MHNLS 2901, MHNLS 11088–89.
Anomaloglossus praderioi: Guyana, Cuyuni‐Mazaruni District, Maringma-tepui, IRSNB 11403–13; Venezuela, Estado Bolívar, Mount Roraima ULABG 4196 (holotype), MHNLS 11272 (paratype), Sierra de Lema, EBRG 5569.
Anomaloglossus roraima: Guyana, Cuyuni-Mazaruni District, Wei-Assipu-tepui, IRSNB 15851, IRSNB 15865, IRSNB 15904–11, Maringma-tepui, IRSNB 15864, IRSNB 15883–901; Venezuela, Estado Bolívar, Mount Roraima, ULABG 4197 (holotype).
Anomaloglossus rufulus: Venezuela, Estado Bolívar, Amari‐tepui, Chimantá Massif, MHNLS 10361 (holotype).
Anomaloglossus tamacuarensis: Venezuela, Estado Amazonas, Sierra Tapirapecó, north base of Pico Tamacuari, MBUCV 6430–33 (4 paratypes).
Anomaloglossus tepuyensis: Venezuela, Estado Bolívar, Auyán-tepui, ULABG 2557 (holotype).
Anomaloglossus triunfo: Venezuela, Estado Bolívar, Cerro Santa Rosa, Serranía del Supamo, EBRG 4756 (holotype), EBRG 4757–59 (3 paratypes).
Anomaloglossus verbeeksnyderorum: Venezuela, Estado Amazonas, Tobogán de la Selva, Municipio Atures, MHNLS 19649 (holotype).
Anomaloglossus wothuja: Venezuela, Estado Amazonas, base of Cerro Sipapo, Tobogán del Cuao, EBRG 6689 (holotype).