New Species of Gephyromantis from Marojejy National Park, Northeast Madagascar
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1 New Species of Gephyromantis from Marojejy National Park, Northeast Madagascar Author(s): Frank Glaw, Jörn Köhler, and Miguel Vences Source: Journal of Herpetology, 45(2): Published By: The Society for the Study of Amphibians and Reptiles DOI: / URL: BioOne ( is an electronic aggregator of bioscience research content, and the online home to over 160 journals and books published by not-for-profit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
2 Journal of Herpetology, Vol. 45, No. 2, pp , 2011 Copyright 2011 Society for the Study of Amphibians and Reptiles New Species of Gephyromantis from Marojejy National Park, Northeast Madagascar FRANK GLAW, 1,2 JÖRN KÖHLER, 3 AND MIGUEL VENCES 4 1 Zoologische Staatssammlung München, Münchhausenstr. 21, München, Germany 3 Department of Natural History, Hessisches Landesmuseum Darmstadt, Friedensplatz 1, Darmstadt, Germany 4 Zoological Institute, Technical University of Braunschweig, Mendelssohnstr. 4, Braunschweig, Germany ABSTRACT. We describe a new species of semiarboreal frog in the genus Gephyromantis from midelevation rain forests of the Marojejy Massif in northeastern Madagascar, which, according to previously published molecular data, forms a clade with Gephyromantis ambohitra, Gephyromantis asper, and Gephyromantis spinifer. The new species is morphologically most similar to G. ambohitra but differs by its advertisement call and a high genetic distance in mitochondrial DNA. Considering intensive recent logging activity in Marojejy National Park, we propose an IUCN status of Vulnerable for this new species. In the Malagasy-Comoroan family Mantellidae, the genus Gephyromantis comprises 35 nominal species of mostly semiarboreal frogs, most of which are restricted to rain-forest habitat in eastern and northern Madagascar (Glaw and Vences, 2006, 2007). One lineage in Gephyromantis (the subgenus Phylacomantis) has free-swimming carnivorous tadpoles, but in general Gephyromantis are remarkable because they contain species characterized by endotrophic development. Their developmental mode has been described as being direct (Blommers- Schlösser, 1979; Blommers-Schlösser and Blanc, 1991; Glaw and Vences, 2007) but instead may rather consist of nonfeeding tadpoles developing in terrestrial nests (unpubl. data) and, thus, follow a nidicolous developmental mode (sensu McDiarmid and Altig, 1999). However, precise observations are available for only very few species. Surprisingly, during a recent program of identifying Malagasy tadpoles through DNA bar coding, evidence was collected that Gephyromantis asper, a species for which direct development had been reported (Blommers-Schlösser, 1979) instead is characterized by free-swimming exotrophic tadpoles (Vences et al., 2008), similar to Gephyromantis ambohitra from northern Madagascar (Randrianiaina et al., 2007) which is part of the same Gephyromantis subclade (Vieites et al., 2009). These two species, together with Gephyromantis spinifer, form an isolated evolutionary lineage within Gephyromantis. Although they have been assigned to the subgenus Duboimantis (Glaw and Vences, 2006), they might not form a clade with other species of this subgenus (tree in Vieites et al., 2009). Thus, a better understanding of the taxonomy, evolutionary relationships, and distribution of these frogs is crucial to understand the evolution of reproductive and developmental modes in Gephyromantis and other mantellids. Despite intensive taxonomic revisions and descriptions of new species (Andreone et al., 2003; Glaw and Vences, 2000, 2001, 2002a,b; Vences and De la Riva, 2007; Vences and Glaw, 2001; Vences et al., 1997, 2003), the diversity of Gephyromantis is far from being fully understood, and numerous undescribed candidate species have been identified (Vieites et al., 2009). One of these, phylogenetically related to G. ambohitra, G. asper, and G. spinifer (Vieites et al., 2009), is described herein as a new species based on combined evidence from morphology, bioacoustics, and mitochondrial DNA sequences. MATERIALS AND METHODS Frog specimens were collected at night by opportunistic searching and by localizing calling males, using torches and head lamps. Specimens were euthanized in a chlorobutanol solution, fixed in 95% ethanol, and preserved in 70% ethanol. Locality information was recorded with GPS receivers. 2 Corresponding Author. frank.glaw@zsm.mwn.de Specimens studied in this paper are deposited in the collections of the Université d Antananarivo, Département de Biologie Animale, Antananarivo (UADBA) and Zoologische Staatssammlung München (ZSM). FGZC refers to field numbers of one of the authors (FG). Morphological measurements (in millimeters) were all taken by one author (MV) with digital calipers (precision 0.01 mm) to the nearest 0.1 mm. Abbreviations are as follows: SVL (snout vent length), HW (greatest head width), HL (head length), ED (horizontal eye diameter), END (eye nostril distance), NSD (nostril snout tip distance), NND (nostril nostril distance), TD (horizontal tympanum diameter), TL (tibia length, actually referring not to the tibia bone but to the shank), HAL (hand length), HIL (hind limb length), FOL (foot length), FOTL (foot length including tarsus), FORL (forelimb length), RHL (relative hind limb length), FGL (femoral gland length), and FGW (femoral gland width). Terminology, especially of dermal structure such as tubercles, spines and ridges, and description scheme follow Vences and Glaw (2001). Webbing formula follows Savage and Heyer (1967) as modified by Myers and Duellman (1982) and Savage and Heyer (1997). To facilitate comparisons, we also give the formula used by Blommers- Schlösser (1979) and most subsequent authors who published accounts on Madagascan anurans. Calls were recorded in the field using a Sony WM-D6C tape recorder with an external microphone (Vivanco EM 239). Recordings were sampled at khz and 16-bit resolution and computer-analyzed using the software Adobe Audition version 1.5. Frequency information was obtained through Fast Fourier Transformation (FFT; width 1,024 points). Spectrograms were obtained at Hanning window function with 256 bands resolution. Temporal measurements are given as range, with mean 6 standard deviation in parentheses. Terminology in call descriptions follows Köhler (2000). TAXONOMY Gephyromantis tahotra sp. nov. Figure 1 Remark. This species has been considered before as confirmed candidate species Gephyromantis sp. 1 by Vieites et al. (2009), and as Gephyromantis sp. aff. ambohitra Marojejy by Glaw and Vences (2007). Holotype. ZSM 193/2005 (FGZC 2882), adult male, collected at Marojejy National Park, at a campsite locally called Camp Simpona, 14u S, 49u E, 1,326 m above sea level, northeastern Madagascar, on 16 February 2005 by two of the authors (FG and MV) and R. D. Randrianiaina. Paratypes. ZSM 191/2005 (FGZC 2815), and ZSM 192/2005 (FGZC 2848), two females, with same data as holotype, except the collection date of ZSM 192/2005 (17 February 2005).
3 156 F. GLAW ET AL. FIG. 1. Gephyromantis tahotra sp. nov. in life. Male holotype (ZSM 193/2005) in (A) dorsolateral and (B) ventral views, and female paratype (ZSM 191/2005) in (C) dorsolateral and (D) ventral views. Color reproduction supported by the Thomas Beauvais Fund. Etymology. The species name is derived from the Malagasy word tahotra, which means fear, and is used as a noun in apposition. It makes reference to the intensive illegal wood exploitation within Marojejy National Park that followed the 2009 political crisis of Madagascar, and that causes fear of extinction of rain-forest restricted species such as G. tahotra. Diagnosis. Assigned to the genus Gephyromantis based on (1) presence of intercalary elements between ultimate and penultimate phalanges of fingers and toes (as verified externally), (2) presence of femoral glands of type 2 sensu Glaw et al. (2000) in males and their absence in females, (3) presence of distinct inner and outer dorsolateral ridges, (4) blackish paired subgular vocal sacs in males, and (4) molecular phylogenetic relationships to other Gephyromantis (see Vieites et al., 2009; G. sp. 1). Within Gephyromantis, assigned to the subgenus Duboimantis as defined by Glaw and Vences (2006) by (1) medium size (SVL. 32 mm), (2) presence of distinct and continuous dorsolateral ridges and superocular dermal spines (5 conical tubercles), (3) blackish paired subgular vocal sacs in males, and (4) nocturnal calling behavior. Among species of the subgenus Duboimantis, G. tahotra can be distinguished from Gephyromantis granulatus, Gephyromantis leucomaculatus, Gephyromantis redimitus, Gephyromantis schilfi, and Gephyromantis zavona by the presence of distinct superocular dermal spines and inner dorsolateral ridges starting behind the eyes and converging centripetally before they run centrally on middorsum (vs. absence of such dermal spines and ridges); from Gephyromantis cornutus, Gephyromantis moseri, Gephyromantis tandroka, and Gephyromantis tschenki by the absence of distinct interocular tubercles (vs. presence) and blackish paired subgular vocal sacs (vs. grayish single or bilobate sacs); from Gephyromantis salegy by smaller size (male SVL 34 mm vs mm) and much more strongly elevated dorsolateral ridges; from Gephyromantis luteus, Gephyromantis plicifer, and Gephyromantis sculpturatus by smaller size (male SVL 34 mm vs mm) and less expressed webbing (not reaching terminal disks of toe 5 vs. usually reaching terminal disk). Furthermore also clearly distinguished by smaller size (male SVL 34 mm) from G. granulatus (40 45 mm), G. redimitus (47 53 mm), and G. tandroka (39 mm). The new species is morphologically most similar and according to molecular data closely related to G. ambohitra, G. asper, and G. spinifer (see Vieites et al., 2009). It is distinguished from G. asper by larger size (male SVL 34 mm vs mm) and smoother dorsal skin (only few tubercles and ridges external to inner dorsolateral ridges, vs. strong expression of
4 NEW GEPHYROMANTIS FROM MADAGASCAR 157 TABLE 1. Morphometric measurements (in mm) of holotype (HT) and paratypes (PT) of Gephyromantis tahotra sp. nov. from the type locality Marojejy National Park and of newly collected specimens of Gephyromantis ambohitra from the type locality Montagne d Ambre National Park, and from Manongarivo Special Reserve. Relative hind limb length (RHL) is coded as follows: when adpressed along body, tibiotarsal articulation reaches (1) the nostril, (2) the snout tip, (3) beyond the snout tip, or (4) far beyond the snout tip. Abbreviations: M, male; F, female; n.r., not recognizable. For other abbreviations, see Materials and Methods. Voucher number Sex SVL HW HL TD ED END NSD NND FORL HAL HIL FOTL FOL TIBL FGL FGW RHL Gephyromantis tahotra sp. nov. (Marojejy) ZSM 191/2005 (PT) F ZSM 192/2005 (PT) F ZSM 193/2005 (HT) M Gephyromantis ambohitra (Montagne d Ambre) ZSM 871/2003 M ZSM 872/2003 M n.r. n.r. 4 ZSM 2069/2007 M n.r. n.r. 4 ZSM 873/2003 F ZSM 875/2003 F ZSM 204/2004 F ZSM 205/2004 F ZSM 2068/2007 F Gephyromantis ambohitra (Manongarivo) ZSM 838/2003 M ZSM 848/2003 M ZSM 849/2003 M ZSM 850/2003 M ZSM 851/2003 F these structures), and by advertisement call (moderately long notes of ms duration vs. short notes of 5 13 ms duration); from G. spinifer by a much smoother dorsal skin (only few tubercles and ridges lateral to inner dorsolateral ridges, vs. very strong expression of these structures), and by a weakly expressed black-white pattern on the belly and throat (vs. a very strong such pattern especially in females); from G. ambohitra mainly by advertisement call (internote interval, ms vs ms; see below) and a strong molecular differentiation (11 12% pairwise divergence in the 16S rrna gene; Vieites et al., 2009). Morphological differences to G. ambohitra need to be verified by a larger sampling of specimens and populations but probably include (Table 1) a slightly smaller body size (male SVL 34 mm vs mm) and smaller femoral glands (their length 5 mm vs. 6 8 mm). Description of the Holotype. Adult male, in good state of preservation, muscles from right thigh removed as tissue sample. SVL 34.0 mm. For measurements, see Table 1. Body slender; head slightly longer than wide, distinctly wider than body; snout acuminated in dorsal view, truncate in lateral view; nostrils directed laterally, slightly protuberant, much nearer to tip of snout than to eye; canthus rostralis distinct, concave; loreal region concave; tympanum distinct, elliptical (slightly higher than wide), its diameter 59% of eye diameter; supratympanic fold very distinct, straight; tongue ovoid, distinctly bifid posteriorly; vomerine teeth indistinct, in two small rounded aggregations, positioned posterolateral to choanae; choanae rounded. A dark dermal fold (the inflatable parts of the vocal sacs) running along each lower jaw from the commissure of the mouth to the middle of the lower jaw. Arms slender, subarticular tubercles single; a very poorly developed outer and a poorly developed inner metacarpal tubercle; fingers without webbing; relative length of fingers 1, 2, 4, 3, second finger distinctly shorter than fourth finger; finger disks distinctly enlarged; nuptial pads absent. Hind limbs slender; tibiotarsal articulation reaching far beyond snout tip when hind limb is adpressed along body; lateral metatarsalia separated by webbing; inner metatarsal tubercle distinct, outer metatarsal tubercle very small but recognizable; webbing formula of foot I 2 2 II 2 3 III IV V; webbing formula according to the notation of Blommers-Schlösser (1979) 1(1), 2i(1), 2e(1), 3i(2), 3e(1), 4i(2.25), 4e(2), 5(0.5); relative toe length 1, 2, 3 # 5, 4. Toe disks distinctly enlarged. Skin on dorsal surfaces generally smooth; outer dorsolateral folds present only in traces; inner dorsolateral folds distinct, elevated, starting approximately 1 mm behind the eyes and gradually vanishing on the posterior back; outer dorsolateral folds running from middorsum posterior to the inguinal region. Two distinct, blackish interocular ridges, bordering the beige vertebral stripe; superocular tubercles present, few of them enlarged to small dermal spines; a short and indistinct (dermal) tarsal spine. Ventral skin smooth on throat and limbs, slightly granular on posterior belly. Femoral glands poorly delimited and barely detectable externally. Dorsal coloration after five years in preservative brown with a broad beige vertebral band from snout tip to vent, which is intermittent for about 2 mm on the posterior back. Inner dorsolateral folds bordered by black. Each hind limb with one distinct broad dark brown cross-band extending on thighs and shank, and three narrower and less distinct brown cross-bands. Dorsal color of forelimbs dark brown with two distinct crossbands on lower arm and several additional indistinct crossbands on the hand. Tympanic region and area between eye and upper jaw dark brown. Lips with alternating brown and whitish flecks. On the flanks, the dark dorsal color fading gradually into the light ventral color. Ground color of ventral surfaces cream-white with fine brown pigment on the median part of the throat and chest, some indistinct and weakly symmetrical brown markings on chest, and a largely uniformly gray posterior belly. Dermal folds of vocal sacs dark gray. Ventral sides cream-white on thigh, with a brown and cream band on shank; ventral surfaces of tarsus and feet black. In life (see also Glaw and Vences, 2007:221), color was very similar to that in preservative. Throat and blackish folds of the vocal sacs were slightly darker, the iris was golden. Variation. The two female paratypes are in excellent state of preservation and resemble the holotype in morphology and coloration but are larger (for measurements, see Table 1). The light vertebral stripe is similarly shaped as in the holotype but continuous and distinctly broadened in front of the eyes. The tarsal spines are larger than in the holotype. Coloration of ZSM 191/2005 is very similar to the holotype but with more homogenous dark cross-bands on limbs. ZSM 192/2005 is darker dorsally with beige mottling between the forelegs.
5 158 F. GLAW ET AL. FIG. 3. Spectrogram and corresponding oscillogram of the advertisement call of Gephyromantis tahotra sp. nov. from Marojejy, recorded on 16 February 2005 at 21uC air temperature. FIG. 2. Schematic map of Madagascar showing the known distributions of Gephyromantis ambohitra, Gephyromantis asper, Gephyromantis tahotra, and Gephyromantis spinifer, which together form a clade within the genus Gephyromantis (Vieites et al., 2009). For locality records and respective voucher specimens see Vences and Glaw (2001) and Glaw and Vences (2007). Localities discussed in the text are noted. Ventrally, both paratypes have a more contrasting ventral coloration, with distinct brown and cream mottling on the throat, chest, and anterior belly. The thighs of ZSM 191/2005 are largely cream with brown flecks only close to the knee joint, whereas the thighs of ZSM 192/2005 are mottled brown. Additional specimens from northeastern Madagascar, stored in the MNHN most likely referable to G. tahotra were studied by Vences and Glaw (2001) and have been assigned to this species (under the name Gephyromantis sp. aff. ambohitra Marojejy ) by Glaw and Vences (2007). Natural History. Specimens were calling at Marojejy along a small rain-forest stream, perched on leaves about 50 cm high (Vences et al., 2006). The species is not known from any other locality (Fig. 2). Advertisement Call. The advertisement call of G. tahotra recorded at Camp Simpona, Marojejy National Park, on 16 February 2005 at 21uC (Vences et al., 2006, CD 2, track 2) consists of a series of moderately long pulsed notes, repeated at regular intervals (Fig. 3). Numerical parameters are as follows: note duration, ms ( ; N 5 11); internote interval, ms ( ; N 5 10); pulse rate in notes, app. 310 pulses/sec; dominant frequency, 1,535 1,562 Hz (1, ; N 5 11). Overall frequency is distributed in a broad band from approximately 1,400 5,800 Hz, with numerous narrow frequency bands recognizable; a second energy peak in addition to the dominant frequency is recognizable at 3,400 Hz. Notes exhibit some overall amplitude modulation, with energy continuously decreasing throughout the note. Comparative Call Data. Advertisement calls of G. ambohitra recorded at Montagne d Ambre (type locality) on 17 February 2003 at 21uC (Vences et al., 2006, CD 2, track 1, cut 2) consist of series of moderately long notes repeated at regular intervals (Fig. 4). Structure and duration of notes is very similar to those of G. tahotra, but internote intervals are much longer and the pulse rate is considerably lower. Numerical parameters are as follows: note duration, ms ( ; N 5 14); internote interval, ms ( ; N 5 12); pulse rate in notes, approximately 150 pulses/sec; dominant frequency, 3,180 3,366 Hz (3, ; N 5 10). Overall frequency is distributed at approximately 2,800 4,400 Hz. Calls of another population of G. ambohitra recorded at Manongarivo on 3 February 2003 at 23uC (Vences et al., 2006, CD 2, track 1, cut 1) generally agree in characters with those from the type locality and had following numerical parameters: note duration, ms ( ; N 5 19); internote interval, ms ( ; N 5 17); pulse rate in notes, approximately 160 pulses/sec; dominant frequency, 3,044 3,115 Hz (3, ; N 5 8). Call energy at 1,390 1,560 Hz is almost as high as that of the dominant frequency. In conclusion, the two species G. ambohitra and G. tahotra are well differentiated by their advertisement calls. The calls of the FIG. 4. Spectrogram and corresponding oscillogram of the advertisement call of Gephyromantis ambohitra from Montagne d Ambre, recorded on 17 February 2003 at 21uC air temperature.
6 NEW GEPHYROMANTIS FROM MADAGASCAR 159 two species differ as follows: at comparable temperatures, calls of G. ambohitra show distinctly longer internote intervals ( vs ms), lower pulse rate within notes ( vs. 310 pulses/sec), and higher dominant frequency (3,044 3,366 vs. 1,535 1,562 Hz). Calls of G. asper mainly differ from those of G. tahotra (and G. ambohitra) by very short note duration of only 5 13 ms (Vences and Glaw, 2001). Molecular Differentiation. A DNA sequence of the mitochondrial 16S rrna gene of the new species (from Vieites et al., 2009) is available from Genbank under the accession number FJ A comparison of DNA sequences of the mitochondrial 16S rrna gene as available from the works of Vences and Glaw (2001), Vieites et al. (2009), and Randrianiaina et al. (2007) yielded very high genetic divergences of all species in the G. asper group. Gephyromantis tahotra was genetically closest to G. asper and G. spinifer (7.1% and 8.2% uncorrected pairwise divergence) and was strongly differentiated from G. ambohitra from Manongarivo (11.4%) and Montagne d Ambre ( %). Gephyromantis spinifer and G. ambohitra, respectively, differed by 7.0% and % from G. asper, and the two populations assigned to G. ambohitra (Manongarivo and Montagne d Ambre) differed by %, a value much above the threshold of 3% proposed by Fouquet et al. (2007) and Vieites et al. (2009) for a preliminary identification of candidate species. DISCUSSION The systematics of mantellid frogs have undergone a period of rapid change and progress, mainly based on the integrative analysis of morphology, bioacoustics, and molecular genetics of materials collected during recent fieldwork. Vences and Glaw (2001), in their revision of G. asper and morphologically similar species, had only a limited amount of bioacoustic and molecular information available and assigned material from the Paris museum collected at the Tsaratanana Massif (just north of Manongarivo) and Marojejy to G. asper, whereas at the same time describing the morphologically distinct population from Montagne d Ambre in the far north as new species, G. ambohitra. Data presented here demonstrate the bioacoustic distinctness of G. ambohitra and the bioacoustic uniformity of two geographically distant populations assigned to this species by morphology and molecular phylogeny (i.e., from Manongarivo and Montagne d Ambre). Our new data from Marojejy furthermore reveal the existence of a new species of this clade, described here as G. tahotra. However, the situation might be more complex, and additional studies are needed to fully clarify the taxonomy and distribution of this clade of frogs. First, preliminary molecular data from tadpoles collected in Marojejy (R. D. Randrianiaina, unpubl. data) indicate the possible existence of both G. tahotra and G. ambohitra on this massif, but so far, no reliable records of adults of the latter species are available. This indicates that in-depth studies on the basis of additional field data are needed in this region, and therefore, we refrain from assigning historical museum voucher specimens from Marojejy and Tsaratanana to either G. ambohitra or G. tahotra, considering the morphological similarity and possible sympatric occurrence of both species. The identity of two frogs collected recently from Tsaratanana, tentatively assigned to G. ambohitra, is therefore in need of confirmation as well (Andreone et al., 2009). The analysis of additional reliably identified specimens also is an essential prerequisite to understand whether diagnostic morphological characters exist to distinguish G. tahotra from G. ambohitra. Second, the strong molecular differentiation among populations of G. asper from the southern central east and northern central east of Madagascar indicates that these might represent different species as well. However, Vieites et al. (2009) considered them as deep conspecific lineages and called for fieldwork to fill the apparent gaps in the distribution of the various species in this complex and to identify their precise contact zones and areas of possible sympatry. The primary habitats of the Marojejy Massif are protected as Marojejy National Park, which was declared a World Heritage Site in These habitats harbor remarkable biotic diversity and endemism (Raselimanana et al., 2000; Garreau and Manantsara, 2003), as do the adjacent forests and massifs (Andreone et al., 2000). The distribution of amphibian species in northern Madagascar is poorly understood (Glaw and Vences, 2007; Vieites et al., 2009). However, there are numerous amphibians of which reliable records are known exclusively from this massif: the mantellids G. tandroka and G. schilfi, and the microhylids Rhombophryne minuta, Stumpffia grandis, Stumpffia roseifemoralis, and Stumpffia tridactyla, as well as several undescribed candidate species of the genera Gephyromantis, Platypelis, Rhombophryne, and Stumpffia. Almost all of these potential local endemics, similar to G. tahotra, are known from higher elevations at Marojejy (.1,100 m), whereas at lower elevations, fewer putative endemics are known (three candidate species belonging to Stumpffia and Platypelis) and one species thought to be a lowelevation endemic of Marojejy, Mantella manery, has recently been discovered in other areas (Edmonds, 2009). In contrast, this trend is not clearly recognizable in reptiles. Putative highaltitude endemics include the chameleons Calumma peyrierasi and Calumma jejy (Brygoo, 1978; Raxworthy and Nussbaum, 2006) and an undescribed species of gecko of the genus Uroplatus (Glaw and Vences, 2007), whereas the fossorial skink Pseudoacontias angelorum, known from just a single specimen (Nussbaum and Raxworthy, 1995), and the leaf chameleon Brookesia karchei, are putative midaltitude endemics. Despite remarkable efforts of establishing Marojejy National Park as an ecotourist destination (Bradt, 2007) (www. marojejy. com; accessed 2010), illegal logging of rosewood has been a permanent threat to its forests (Patel, 2007) and has risen to a dramatic extent in 2009 as a result of political turmoil (Schuurman and Lowry, 2009), requiring the temporary closure of the park. According to Andreone et al. (2005, 2008), at present no Gephyromantis species is classified in the IUCN Red List category of Critically Endangered, six species are classified as Endangered (Gephyromantis azzurrae, Gephyromantis corvus, Gephyromantis horridus, Gephyromantis runewsweeki, Gephyromantis silvanus, Gephyromantis webbi), and seven species as Vulnerable (G. ambohitra, Gephyromantis klemmeri, Gephyromantis rivicola, G. salegy, G. schilfi, Gephyromantis striatus, G. tandroka). In line with the arguments used in these conservation assessments, we propose for G. tahotra a conservation status of Vulnerable based on IUCN (2001) criteria B1ab(iii) (i.e., because it is known from less than 10 locations and because there is continuing decline in the extent and quality of its habitat). This is the same category assigned and criteria applied as to other Marojejy endemic Gephyromantis that occur syntopically at Marojejy, namely G. tandroka and G. schilfi. Acknowledgments. We are grateful to R.-D. Randrianiaina for his tireless help in the field. This work has been carried out in the framework of collaboration agreements of the authors institutions with UADBA. The Malagasy authorities kindly granted research and export permits. Specimens were obtained during expeditions supported by the Volkswagen Foundation and Deutsche Forschungsgemeinschaft. LITERATURE CITED ANDREONE, F., J. E. RANDRIANIRINA, P. D. JENKINS, AND G. APREA Species diversity of Amphibia, Reptilia and Lipotyphla (Mammalia) at Ambolokopatrika, a rainforest between the Anjanaharibe-Sud and Marojejy massifs, NE Madagascar. Biodiversity and Conservation 9:
7 160 F. GLAW ET AL. ANDREONE, F., G. APREA, M.VENCES, AND G. ODIERNA A new frog of the genus Mantidactylus from the rainforests of north-eastern Madagascar, and its karyological affinities. Amphibia-Reptilia 24: ANDREONE, F., J. E. CADLE, N. COX, F. GLAW, R. A. NUSSBAUM, C. J. RAXWORTHY, S. N. STUART, D. VALLAN, AND M. VENCES Species review of amphibian extinction risks in Madagascar: conclusions from the Global Amphibian Assessment. Conservation Biology 19: ANDREONE, F., N. A. COX, F. GLAW, J. KÖHLER, N. H. C. RABIBISOA, H. RANDRIAMAHAZO,H.RANDRIANASOLO,C.J.RAXWORTHY,S.N.STUART,D. VALLAN, AND M. VENCES Update of the Global Amphibian Assessment for Madagascar in light of new species discoveries, nomenclature changes, and new field information. In F. Andreone (ed.), A Conservation Strategy for the Amphibians of Madagascar. Monografie del Museo Regionale di Scienze Naturali di Torino 45: ANDREONE, F., F. GLAW, F. MATTIOLI, R. JESU, G. SCHIMMENTI, J. E. RANDRIANIRINA, AND M. VENCES The peculiar herpetofauna of some Tsaratanana rainforests and its affinities with Manongarivo and other massifs and forests of northern Madagascar. Italian Journal of Zoology 76: BLOMMERS-SCHLÖSSER, R. M. A Biosystematics of the Malagasy frogs. I. Mantellinae (Ranidae). Beaufortia 352:1 77. BLOMMERS-SCHLÖSSER, R. M. A., AND C. P. BLANC Amphibiens (première partie). Faune de Madagascar 75 (part 1): BRADT, H Madagascar. Bradt Travel Guide, Chalfont St. Peter, U.K. BRYGOO, E. R Reptiles Sauriens Chamaeleonidae Genre Brookesia et complément pour le genre Chamaeleo. Faune de Madagascar 47: EDMONDS, D Extended distribution of two frogs from Madagascar: Mantella crocea and Mantella manery (Anura: Mantellidae). Herpetology Notes 2: FOUQUET, A., A. GILLES, M. VENCES, C. MARTY, M. BLANC, AND N. J. GEMMELL Underestimation of species richness in Neotropical frogs revealed by mtdna analyses. PLoS ONE 2 (10):e1109. GARREAU, J.-M., AND A. MANANTSARA The protected-area complex of the Parc National de Marojejy and the Réserve Spéciale d Anjanaharibe-Sud. In S. M. Goodman and J. P. Benstead (eds.), The Natural History of Madagascar, pp University of Chicago Press, Chicago. GLAW, F., AND M. VENCES A new species of Mantidactylus from northeastern Madagascar (Amphibia, Anura, Ranidae) with resurrection of Mantidactylus blanci (Guibé, 1974). Spixiana 23: Two new sibling species of Mantidactylus cornutus from Madagascar. Spixiana 24: a. A new species of Mantidactylus (Anura: Mantellidae) from Andasibe in Eastern Madagascar. Journal of Herpetology 36: b. A new cryptic frog species of the Mantidactylus boulengeri group with a divergent vocal sac structure. Amphibia-Reptilia 23: Phylogeny and genus-level classification of mantellid frogs. Organisms Diversity and Evolution 6: A Field Guide to the Amphibians and Reptiles of Madagascar. 3rd ed. Vences and Glaw Verlag, Köln, Germany. GLAW, F., M. VENCES, AND V. GOSSMANN A new species of Mantidactylus from Madagascar, with a comparative survey of internal femoral gland structure in the genus (Amphibia: Ranidae: Mantellinae). Journal of Natural History 34: IUCN (WORLD CONSERVATION UNION) IUCN red list categories. Vers Species Survival Commission, IUCN, Gland, Switzerland. KÖHLER, J Amphibian diversity in Bolivia: a study with special reference to montane forest regions. Bonner zoologische Monographien 48: MCDIARMID, R. W., AND R. ALTIG Tadpoles. The Biology of Anuran Larvae. University of Chicago Press, Chicago. MYERS, C. W., AND W. E. DUELLMAN A new species of Hyla from Cerro Colorado, and other tree frog records and geographical notes from western Panama. American Museum Novitates 2752:1 32. NUSSBAUM, R. A., AND C. J. RAXWORTHY Review of the scincine genus Pseudoacontias Barboza Du Bocage (Reptilia: Squamata: Scincidae) of Madagascar. Herpetologica 51: PATEL, E. R Logging of rare rosewood and palisandre (Dalbergia spp.) within Marojejy National Park, Madagascar. Madagascar Conservation and Development 2: RANDRIANIAINA, R.-D., F. GLAW, M. THOMAS, J. GLOS, N. RAMINOSOA, AND M. VENCES Descriptions of the tadpoles of two species of Gephyromantis, with a discussion of the phylogenetic origin of direct development in mantellid frogs. Zootaxa 1401: RASELIMANANA, A. P., C. J. RAXWORTHY, AND R. A. NUSSBAUM Herpetofaunal species diversity and elevational distribution within the Parc National de Marojejy, Madagascar. In S. M. Goodman (ed.), A Floral and Faunal Inventory of the Parc National de Marojejy: With Reference to Elevational Variation. Fieldiana Zoology (N.S.) 92: RAXWORTHY, C. J., AND R. A. NUSSBAUM Six new species of occipitallobed Calumma chameleons (Squamata: Chamaeleonidae) from montane regions of Madagascar, with a new description and revision of Calumma brevicorne. Copeia 2006 (4): SAVAGE, J. M., AND W. R. HEYER Variation and distribution in the tree frog genus Phyllomedusa in Costa Rica, Central America. Beiträge zur neotropischen Fauna 5: Digital webbing formulae for anurans: a refinement. Herpetological Review 28:131. SCHUURMAN, D., AND P. P. LOWRY II The Madagascar rosewood massacre. Madagascar Conservation and Development 4: VENCES, M., AND I. DE LARIVA A new species of Gephyromantis from Ranomafana National Park, south-eastern Madagascar (Amphibia, Anura, Mantellidae). Spixiana 30: VENCES, M., AND F. GLAW Systematic review and molecular phylogenetic relationships of the direct developing Malagasy anurans of the Mantidactylus asper group (Amphibia, Mantellidae). Alytes 19: VENCES, M., F. GLAW, AND F. ANDREONE Description of two new frogs of the genus Mantidactylus from Madagascar, with notes on Mantidactylus klemmeri (Guibé, 1974) and Mantidactylus webbi (Grandison, 1953) (Amphibia, Ranidae, Mantellinae). Alytes 14: VENCES, M., F. ANDREONE, F. GLAW, AND J. E. RANDRIANIRINA Molecular and bioacoustic divergence in Mantidactylus granulatus and M. zavona sp. n. (Anura: Mantellidae): bearings for the biogeography of northern Madagascar. African Zoology 38: VENCES, M., F. GLAW, and R. MARQUEZ (EDS.) The Calls of the Frogs of Madagascar. 3 audio CDs and booklet. Alosa, Barcelona, Spain. VENCES, M., Y. CHIARI, M. TESCHKE, R.-D. RANDRIANIAINA, L. RAHARIVOLO- LONIAINA, P. BORA, D. R. VIEITES, AND F. GLAW Which frogs are out there? A preliminary evaluation of survey techniques and identification reliability of Malagasy amphibians. In F. Andreone (ed.), A Conservation Strategy for the Amphibians of Madagascar. Monografie del Museo Regionale di Scienze Naturali di Torino 45: VIEITES, D. R., K. C. WOLLENBERG, F. ANDREONE, J. KÖHLER, F. GLAW, AND M. VENCES Vast underestimation of Madagascar s biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences of the USA 106: Accepted: 29 September 2010.
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