Gephyromantis (Phylacomantis) kintana, Cocca & Andreone & Belluardo & Rosa & Randrianirina & Glaw & Crottini, 2020

Cocca, Walter, Andreone, Franco, Belluardo, Francesco, Rosa, Goncalo M., Randrianirina, Jasmin E., Glaw, Frank & Crottini, Angelica, 2020, Resolving a taxonomic and nomenclatural puzzle in mantellid frogs: synonymization of Gephyromantis azzurrae with G. corvus, and description of Gephyromantis kintana sp. nov. from the Isalo Massif, western Madagascar, ZooKeys 951, pp. 133-157 : 133

Gephyromantis (Phylacomantis) kintana sp. nov. Figures 3D , 4D

Etymology.

Mercurio and Andreone (2007) dedicated G. azzurrae to F. Andreone’s second daughter, Kintana Azzurra Andreone. Since this name turned out to be a junior synonym of G. corvus , F. Andreone and the other authors of this paper wish to dedicate the new species to honour her with the new name. The Malagasy word " kintana " means "star" and is used as a noun in apposition.

Remarks.

DNA sequences of this species have been wrongly referred to as Gephyromantis corvus by Vences (2000; AF215320), Vieites et al. (2009; AF215320), Crottini et al. (2011a; HQ640422-HQ640425), Kaffenberger et al. (2012; JN664348), Cocca et al. (2018; KX066608-KX066637) and all other studies where these accession numbers have been used.

Holotype.

ZSM 163/2019 (ACZCV_0291; Figs 3D , 4D ; tissue sample taken for genetic analysis: MT043942), adult male from Zahavola (Isalo, Ihorombe region, Ranohira Fivondronona, southwestern Madagascar), - 22.6215361S, 45.358667E, ca. 881 m a.s.l., canyon with a narrow gallery forest laying on the edge of the border of Isalo National Park, collected on 26 November 2014 by F. Andreone, A. Crottini, and G. M. Rosa.

Paratypes.

ZSM 164/2019 (ACZCV_0292; tissue sample taken for genetical analysis: KX066612), adult female, collected at the same locality and date and by the same collectors of the holotype; MRSN A5324 (FAZC 12758; tissue sample taken for genetical analysis: KX066613 and HQ640424), adult male collected at the same locality as the holotype on 17 November 2004 by F. Andreone; ZSM 1553/2009, adult male collected in an imprecise locality within Isalo National Park (original collection data: "Isalo, zwischen Canyons und Piscine" probably referring to a locality close to Piscine Naturelle; Isalo, Ihorombe region, Ranohira Fivondronona, southwestern Madagascar), - 22.559667S, 45.371833E, ca. 890 m a.s.l., on 5 June 2003 by N. Lutzmann; ZSM 165/2019 (FAZC 14355; tissue sample taken for genetical analysis: KX066633), adult male, collected at Malaso (Isalo, Ihorombe region, Ranohira Fivondronona, southwestern Madagascar), - 22.5885S, 45.35533333E, ca. 966 m a.s.l., a shallow canyon with almost no gallery forest and included within Isalo National Park, on 30 November 2009 by F. Andreone, A. Crottini and G. M. Rosa; MRSN A5322 (FAZC 12627), adult male, collected at Malaso (Isalo, Ihorombe region, Ranohira Fivondronona, southwestern Madagascar), - 22.5885S, 45.35533333E, ca. 966 m a.s.l., on 22 November 2004 by F. Andreone; MRSN A5323 (FAZC 12661; tissue sample taken for genetical analysis: KX066635, HQ640422), adult female collected at Malaso (Isalo, Ihorombe region, Ranohira Fivondronona, southwestern Madagascar), - 22.5885S, 45.35533333E, ca. 966 m a.s.l., on 24 November 2004 by F. Andreone; MRSN A5373 (FAZC 12859; tissue sample taken for genetical analysis: KX066632, HQ640423), adult male collected at Tsiombivositra (Isalo, Ihorombe region, Ranohira Fivondronona, southwestern Madagascar), - 22.3025000S, 45.3583330E, ca. 900 m a.s.l., a locality close to the border but included within Isalo National Park, on 11 December 2004 by F. Andreone; MRSN A5325 (FAZC 13000; tissue sample taken for genetical analysis: KX066631) and MRSN A5326 (FAZC 13001), adult females collected at Ambovo (Isalo, Ihorombe region, Ranohira Fivondronona, southwestern Madagascar), - 22.508S, 45.3525E, ca. 999 m a.s.l., within the borders of Isalo National Park, on 18 December 2004 by F. Andreone; MRSN A2786 (FAZC 11964; tissue sample taken for genetical analysis: HQ640425), adult female collected at Andranomena (Isalo, Ihorombe region, Ranohira Fivondronona, southwestern Madagascar), - 22.740167S, 45.275E, ca. 740 m a.s.l.), a locality close to Ilakaka and situated outside of the borders of Isalo National Park, on 25 January 2004 by V. Mercurio and J. E. Randrianirina.

Diagnosis.

A species assigned to the genus Gephyromantis (sensu Glaw and Vences 2006), subgenus Phylacomantis , based on genetic and morphological similarities to the other known species ( G. atsingy , G. corvus , and G. pseudoasper ), and recognisable by the presence of the following morphological characters and natural history traits: (1) medium size (adult male SVL 36-44 mm), (2) webbing between toes present, (3) lateral metatarsalia partly connected, (4) inner and outer metatarsal tubercles present, (5) presence of femoral glands of "Type 2" (sensu Glaw et al. 2000), (6) presence of a paired subgular vocal sac, (7) tongue bifid, (8) enlarged triangular finger tips; (9) dirty white throat, belly and thighs, (10) males with white vocal sacs; (11) brownish to olive-grey dorsal colouration with multiple and irregular brown-olive patches, (12) occurrence in young (shallow) canyons with limited (to almost no) vegetation, (13) mostly crepuscular/nocturnal activity, (14) advertisement call (see Mercurio and Andreone 2007 for the description of the advertisement call of specimen MRSN A5313 (ZSM 0047/2011), now genetically assigned to G. kintana sp. nov.).

The new species differs from the three other species of Phylacomantis by high genetic differentiation (pairwise 16S distance ranging from 9.9% to 13.4%), as well as from a combination of morphological and natural history traits.

Gephyromantis kintana sp. nov. is overall similar to the other three species of the subgenus Phylacomantis . Distinguished from G. pseudoasper by: (a) dirty white throat (vs. darker colouration); (b) ventrally dirty white thighs (vs. orange colouration); (c) presence of white vocal sacs (vs. blackish vocal sacs); (d) less granular dorsal skin; (e) larger size (maximum SVL in males 43.6 vs. 37.4 mm), (f) higher maximum number of granules in the femoral glands (96 vs. 43), (g) occurrence in young (shallow) canyons with limited vegetation (vs. mostly rainforest), (h) advertisement call (15-21 vs. 3 notes per call and lower dominant frequency, 3,000-3,200 Hz vs. 3,400-5,000 Hz).

Distinguished from the sympatric G. corvus by: (a) brownish to olive grey dorsal colouration with multiple and irregular brown-olive patches (vs. darker brown dorsal colouration, often with a broad vertebral stripe), (b) dirty white throat (vs. dark brown throat), (c) dirty white belly (vs. brown belly), (d) dirty white thighs (vs. brown thighs); (e) presence of white vocal sacs (vs. brown-blackish vocal sacs), (f) higher maximum number of granules in the femoral glands (96 vs. 58), (g) occurrence in young (shallow) canyons with limited vegetation (vs. dry deciduous gallery forest in deep canyons), (g) advertisement call (15-21 vs. 10-14 notes per call and higher dominant frequency, 3,000-3,200 Hz vs. 2,400-2,700 Hz).

Distinguished from G. atsingy by: (a) brownish to olive grey dorsal colouration with multiple and irregular brown-olive patches (vs. light brown-beige with a greenish shading), (b) less granular dorsal skin; (c) larger size (maximum SVL in males 43.6 vs. 36.6 mm), (d) higher maximum number of granules in the femoral glands (96 vs. 70), e) occurrence in young (shallow) canyons with limited/missing vegetation (vs. “tsingy” geological formations).

Description of the holotype

(Figs 3D , 4D ). Adult male in good state of preservation, distal phalanx of the 5th toe of the left foot removed as tissue sample and part of the ventral surface of thighs cut and opened to count the number of the granules of the femoral gland. SVL 38.2 mm; for other measurements see Table 2 . Body slender; head slightly wider than long; snout slightly pointed in dorsal view, rather rounded in lateral view; nostrils directed laterally much nearer to tip of snout than to eye; canthus rostralis moderately defined; tympanum distinct, rounded, its horizontal diameter 0.8 of eye diameter; supratympanic fold well distinct, regularly curved; tongue distinctly bifid posteriorly. Arms slender; subarticular tubercles single; outer metacarpal tubercle poorly developed, inner metacarpal tubercle relatively well developed; fingers without webbing; finger disks triangular and distinctly enlarged; nuptial pads absent. Hind limbs slender; tibiotarsal articulation reaching beyond the snout tip when hindlimbs are depressed along body; lateral metatarsalia partly connected; inner metatarsal tubercle distinct, outer metatarsal tubercle small but recognisable; webbing of foot 1(1), 2i(1.75), 2e(0.75), 3i(2), 3e(1), 4i(2), 4e(2), 5(0.5). Skin slightly granular on dorsum and belly, ventral skin smooth on throat and chest. Femoral glands are distinctly recognisable from external view and are arranged in a typical glandular cluster ("Type 2", according to Glaw et al. 2000), including 71 single whitish granular glands of ca. 0.3 mm diameter. The vocal sacs in the male holotype are white and distinct.

Colouration of the holotype

(Fig. 3D ). After almost six years in 70% ethanol the holotype conserves the original colour patterns, although it showed a slightly faded dorsal colour (Fig. 3D ). Overall grey-brown colouration with distinct darker brown markings. Forelimbs dorsally grey-brown with one distinct darker brown cross-band on upper arm and three brown cross-bands on lower arm and hand, hands speckled. Finger and toe tips are grey-cream and first and second toes are lighter in colour than the other toes. Flanks with the same colour of the dorsum but with less distinct darker patches. Overall the darker dorsal colour fades into the whitish ventral colour. Nostril distinctly surrounded by a cream thin line; lateral head same colour as dorsum. Ventral colouration in the preserved specimen is more contrasted than in the living specimen. Throat, belly and thighs dirty white, ventral shanks slightly darker than thighs, chest flecked with a few distinct and scattered grey-brownish markings; sole of foot brown. Colouration of limbs is overall similar to the dorsum, although it has less defined markings. Hindlimbs with five dark brown cross-bands on femur, four on tibia, four on tarsus and foot; dorsal foot grey-brown with four slightly defined perpendicular darker brown crossbands.

Colouration of the holotype in life

(Fig. 4D ). The live dorsal colouration, based upon photographs, is olive grey with multiple and irregular brown-olive patches with some greenish and orangish shades in dorsal surface. These markings are more contrasted than in the preserved specimen (Figs 3D vs. 4D). The tympanum is cream with multiple small light brown markings. Slightly defined interocular bar. Flanks with multiple brown-olive flecks that become increasingly smaller ventrally. Brown-olive irregular markings present also in lateral head. Hindlimbs dorsally olive grey with brown-olive crossbands and markings and some greenish and orangish shades. Ventral skin colouration in life unknown. The iris of the holotype is golden with a thin black vertical line in the lower portion of the eye, and a mid-horizontal metallic reddish brown broad band.

Variations.

Individuals of G. kintana sp. nov. have small variations in colouration if compared with the holotype (see Fig. 4B, C, E-G ). In life, dorsal colouration can have a very variable number of irregular brown-olive patches. The female paratype ZSM 164/2019 has a lighter dorsum and the dark spots are more contrasted and more visible than in the holotype. The female paratype MRSN A5326 has darker markings on the chest. Two juveniles of G. kintana (specimens not collected) showed multiple copper markings on dorsum and on forelimbs and hindlimbs (Fig. 4B, E ).

The number of granules composing the femoral glands varies among the analysed specimens. The holotype has 71 granules while specimens MRSN A5322, ZSM 1553/2009, ZSM 0047/2011 (former MRSN A5313) and ZSM 165/2019 have respectively 24, 35, 29 and 75 granules. Paratype MRSN A5373 has the highest number of granules (96; Table 2 ).

We observed minor variation in the webbing formula in two paratypes, with specimen ZSM 164/2019 with 1(1), 2i(1.75), 2e(0.5), 3i(2), 3e(1), 4i(2), 4e(2.25), 5(0.5); and ZSM 165/2019 with 1(1), 2i(1.5), 2e(0.5), 3i(2), 3e(0.75), 4i(2), 4e(2.25), 5(0.5).

Distribution.

Gephyromantis kintana sp. nov. is currently known from localities inside (Piscine Naturelle, Zahavola, Sakamalio, Malaso, Tsiombivositra, and Ambovo) and outside (Andranomena, Andranombilahy, Andohasahenina, and possibly Ilakaka) the borders of Isalo National Park (Fig. 1 ). However, this known distributional area remains restricted to the southern and western portion of the Isalo Massif. Now that we provided a straightforward way to distinguish this species from its sympatric sister species G. corvus more field surveys should be conducted to characterise its distribution in detail. The range encompasses elevations from 726-999 m a.s.l. The population densities are not known but it can be locally abundant, with several individuals grouping together close to remaining water bodies forming ponds in shallow (young) canyons (see Fig. 5C ).

Natural history.

Gephyromantis kintana can be found in relatively undisturbed areas in shallow (young) canyons in the Isalo Massif (Fig. 5A-C ). Different from the individuals of G. corvus in Isalo, that are generally found calling from low vegetation on the lower branches of the trees laying over canyon streams (Fig. 5D ), males of G. kintana generally call from rocks within the canyon (see Figs 4G , 5C ). Most of the sampled individuals were found on the walls of the canyons, and most of the times far from the trees. Different from old (deeper) canyons, which are characterised by the occurrence of a dense gallery forest (Fig. 5D ), younger canyons are generally surrounded by sparse vegetation (Fig. 5A ). In Malaso, G. kintana was often observed sitting on the walls, approximately 1 m above the water (Fig. 5C ), while in Zahavola the species was observed using holes on the sandstone walls as shelters (Figs 4G , 5B ). Active individuals were found during the day and at dusk, when males start calling quite loudly, but also at night.. The tadpoles of G. kintana found at Malaso have a dark fin (Fig. 4A ). Phylacomantis tadpoles with a reddish fin are also known, but there is no molecular taxonomic identification for this material, and it is therefore not yet possible to conclude if this colour variation (black vs. red) is a diagnostic character between the two Phylacomantis species inhabiting the Isalo Massif. Acoustic communication in tadpoles of G. kintana has yet to be recorded, which would not be surprising considering the sound repertoire described in G. corvus larvae (see Reeve et al. 2011).

Conservation status.

If suitable habitat is considered to encompass all areas within the polygon drawn among the known localities (likely an over-estimate), then the EOO (extent of occurrence) totals 563 km2. If plots with a scale of 2 km2 are used to estimate AOO (area of occupancy), then this species occurs within 36 km2 of habitat. Based on IUCN Red List guidelines (IUCN Standards and Petitions Subcommittee 2019) we propose that G. kintana should be considered as Endangered (under criterium B1ab(iii)+2ab(iii)). This suggestion considers the species’ narrow distribution and apparent restriction to inhabit young canyons as well as the fact that the area of the Isalo Massif not included in the borders of the National Park is under severe exploitation by various anthropogenic activities ( Mercurio et al. 2008). In these areas the main threats are: 1) the use of periodic, and often uncontrolled fires to maintain the savannahs ( Mercurio et al. 2008); 2) excavations for sapphire mines ( Duffy 2006); and 3) unsustainable logging of remaining gallery forests ( Mercurio et al. 2008). Despite very limited information on this species, the ongoing pressure on the extent and quality of the habitat is expected to impact the populations likely leading to their declines. Rakotondravony and Goodman (2011) listed G. corvus for the Makay Massif region (also discussed in Cocca et al. 2018). We do not consider this record here because we did not have access to any voucher material from this area at this time, and from the available photographs it was not possible to unequivocally assign this geographic record to either G. corvus or G. kintana .

Figures

Figure 1. Distribution of Gephyromantis corvus and G. kintana sp. nov. Note that in Sakamalio the two species are found in syntopy.

Figure 3. Images of preserved specimens of Gephyromantis corvus and G. kintana sp. nov. Comparison of dorsal and ventral views of preserved specimens of the two sister species G. corvus and G. kintana sp. nov. from Isalo, with particular emphasis on the diagnostic ventral colouration. A holotype of G. corvus (ZFMK 57430), adult male from Namazaha Valley; B holotype of G. azzurrae (MRSN A 5310), adult male from Andriamanero; C adult male (ZFMK 70494) used as genetic reference (AF 215320) for G. corvus in Vences (2000), from an unknown locality of the Isalo Massif (photographs made available by Dennis Roedder and Morris Flecks); D holotype of G. kintana sp. nov. (ZSM 163 / 2019, ACZCV _ 0291), adult male from Zahavola.

Figure 4. Images of living individuals of Gephyromantis kintana sp. nov. Living individuals of G. kintana sp. nov. showing the main developmental stages of the newly described species and its natural environment. A UADBA-A uncatalogued (ACZCV _ 0297), tadpole from Malaso, dorsal view; B ACZC 6920 (individual not collected), juvenile from Zahavola, dorsolateral view; C ACZC 6919 (individual not collected), adult female from Zahavola, dorsolateral view; D ZSM 163 / 2019 (ACZCV _ 0291), adult male holotype from Zahavola, dorsolateral view; E ACZC 6921 (individual not collected), juvenile from Zahavola found on rocks, dorsolateral view; F ACZC 6919 (individual not collected), adult female from Zahavola on rocky substrate, dorsolateral view; G ACZC 1853 (individual not collected), adult from Malaso hiding in a hole in the wall of the canyon. Photographs by Angelica Crottini.

Figure 5. Habitats of Gephyromantis corvus and G. kintana sp. nov. A vegetation within Zahavola Canyon, type locality of G. kintana sp. nov.; B vertical walls at Zahavola with multiple holes, which are used as shelters by G. kintana; C lentic water at Malaso Canyon. Multiple G. kintana sp. nov. individuals are sitting on the wall of the canyon ca. 1 m above the water (arrows point to the three specimens); D Canyon des Rats with its typical dry deciduous gallery forest, habitat of G. corvus. Photographs by Angelica Crottini.