A new fossorial frog, genus Rhombophryne, from Nosy Mangabe Special Reserve, Madagascar

Zoosyst. Evol. 86 (2) 2010, 235 –243 / DOI 10.1002/zoos.201000006

A new fossorial frog, genus Rhombophryne, from Nosy Mangabe Special Reserve, Madagascar Frank Glaw*, 1, Jrn Khler2 and Miguel Vences3 1

Zoologische Staatssammlung Mnchen, Mnchhausenstr. 21, 81247 Mnchen, Germany Department of Natural History, Hessisches Landesmuseum Darmstadt, Friedensplatz 1, 64283 Darmstadt, Germany 3 Zoological Institute, Technical University of Braunschweig, Spielmannstr. 8, 38106 Braunschweig, Germany 2

Abstract Received 1 December 2009 Accepted 7 May 2010 Published 24 September 2010

Key Words Amphibia Anura Microhylidae Cophylinae Rhombophryne mangabensis sp. nov.

We describe a new species of fossorial microhylid frog from rainforest on Nosy Mangabe island, north-eastern Madagascar. The new species is assigned to the genus Rhombophryne based on its molecular phylogenetic affinities. It is characterized by its loud call that consists of 2–5 melodious whistles, and differs from all other nominal species of Rhombophryne by a substantial divergence of more than 10 % pairwise nucleotide differences in the mitochondrial 16S rRNA gene. Morphologically it is distinctly smaller than all other Rhombophryne except R. minuta. The latter species, besides being strongly divergent genetically, has relatively longer hands and feet and a different advertisement call with an unusual note structure, consisting of two units. The discovery of the new species reinforces the hypothesis that northern Madagascar is the center of diversity of Rhombophryne, and is in accordance with the hypothesis of small range sizes and elevated microendemism in this genus.

Introduction Narrow-mouthed frogs (family Microhylidae) of the subfamily Cophylinae form a species-rich endemic radiation in Madagascar (Van der Meijden et al. 2007), with currently 51 nominal species. Most species are distributed in the rainforests of the east but a few recently discovered species occur in the dry west (Glaw et al. 2007; Andreone & Randrianirina 2008). Cophyline frogs are characterized by non-feeding tadpoles that develop in tree-holes, foam nests or jelly nests in the leaf-litter (Blommers-Schlsser 1975; Glaw & Vences 1992), and comprise arboreal as well as terrestrial and fossorial lineages (Andreone et al. 2005; Wollenberg et al. 2008). In general, microhylids are known to comprise large numbers of undescribed species, but in particular the fossorial taxa of the genera Rhombophryne (nine nominal species) and Plethodontohyla (nine nominal species) are taxonomically very complex: many divergent genetic lineages have been identified (Andreone et al. 2005; Wollenberg et al. 2008; Vieites et al. 2009), but for only few of these secretive frogs are basic data on morphological variation, advertisement calls and natural history available. Species delimi-

* Corresponding author, e-mail: [email protected]

# 2010 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

tation and definition is therefore usually a very difficult task. Thus, although Vieites et al. (2009) distinguish a total of 13 potentially undescribed species (candidate species) in these two genera, in the last ten years descriptions of only three new Plethodontohyla and one new Rhombophryne species (Vences & Glaw 2003; Vences et al. 2003; Glaw & Vences 2007b; Glaw et al. 2007) have been published, with an additional new species of Rhombophryne described only recently (D’Cruze et al. 2010). One small-sized candidate species of Rhombophryne has already become known as early as in 1992 (Glaw & Vences 1992). This species was observed emitting its characteristic calls during very heavy rain at Nosy Mangabe on Madagascar’s east coast, a small offshore island that is included in Madagascar’s network of protected areas as Special Reserve. Because of the lack of convincing diagnostic morphological characters due to low available sample sizes, the Nosy Mangabe specimens were tentatively assigned to Plethodontohyla (now Rhombophryne) minuta (see also Glaw & Vences 1994), another small-sized species from the Marojejy massif in north-eastern Madagascar. However, already Glaw & Vences (1992) mentioned differences between

Glaw, F. et al.: New fossorial Rhombophryne

236

the type material of P. minuta and the Nosy Mangabe specimens, in particular the longer hands and feet of minuta. Eventually, in 2005 we collected fresh material and recorded advertisement calls of minuta at the type locality Marojejy, allowing for bioacoustic and molecular comparisons. It became clear that both, minuta and the Nosy Mangabe form, are to be assigned to the genus Rhombophryne, and that both of them are likely to represent different species. In subsequent accounts, the Nosy Mangabe candidate species was referred to as Plethodontohyla sp. (Nosy Mangabe) by Vences et al. (2006), Rhombophryne sp. aff. minuta by Glaw & Vences (2007a), Rhombophryne sp. 2 by Wollenberg et al. (2008), and R. sp. 5 by Vieites et al. (2009). The goal of the present paper is to summarize the data on the molecular and bioacoustic differentiation of the Rhombophryne specimens from Nosy Mangabe, provide comparative data on the advertisement call of R. minuta, and scientifically name and describe the Nosy Mangabe species.

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. Specimens studied in this paper are deposited in the collection of the Universit d’Antananarivo, Dpartement de Biologie Animale, Antananarivo (UADBA), Zoologisches Forschungsmuseum Alexander Koenig, Bonn (ZFMK), and Zoologische Staatssammlung Mnchen (ZSM). ZCMV refers to field numbers of M. Vences. Morphological measurements (in millimetres) were all taken by M. Vences with digital calipers (precision 0.01 mm) to the nearest 0.1 mm. Terminology and description scheme follow Vences & Glaw (2003). Calls of the new species were recorded in the field using a Sony microcasette tape recorder with internal microphone. Recordings were sampled at 22.05 kHz and 16-bit resolution and computer-analysed using the software Adobe Audition version 1.5. Frequency information was obtained through Fast Fourier Transformation (FFT; width 1024 points). Spectrograms were obtained at Hanning window function with 256 bands resolution. Temporal measurements are given as range, with mean  standard deviation in parentheses. Terminology in call descriptions follows Khler (2000). DNA sequences of the new species (from the holotype specimen) were obtained by Wollenberg et al. (2008) and Vieites et al. (2009) and retrieved from Genbank for comparisons. For further details see section “Molecular differentiation”. Abbreviations SVL HW HL ED END NSD NND TD TL HAL

snout–vent length greatest head width head length horizontal eye diameter eye–nostril distance nostril–snout tip distance nostril–nostril distance horizontal tympanum diameter tibia length, actually referring not to the tibia bone but to the shank hand length

museum-zoosyst.evol.wiley-vch.de

HIL FOL FOTL FORL RHL

hindlimb length foot length foot length including tarsus forelimb length relative hindlimb length

Results Rhombophryne mangabensis sp. nov. Figures 1–2 Holotype. Adult male, ZSM 470/2005 (ZCMV 886, GenBank accession number for the 12S and 16S rRNA genes EU341109), from Nosy Mangabe island (15 300 S, 49 460 E, ca. 50–100 m above sea level), off the north east coast of Madagascar next to the town of Maroantsetra, collected on 22 February 2005 by Frank Glaw, Roger Daniel Randrianiaina and Miguel Vences. Paratypes. ZSM 471/2005 (field number ZCMV 2118), ZSM 472/2005 (ZCMV 2154), UADBA uncatalogued (ZCMV 2119) and UADBA uncatalogued (ZCMV 890), three adult specimens (probably males) and one subadult, with the same collection data as holotype; ZFMK 52769– 52771, three adult males, and ZFMK 52772, one subadult specimen, all collected by Frank Glaw and Miguel Vences on 13 March 1991 at the type locality.

Etymology. The species name is an adjective derived from the type locality, Nosy Mangabe. Diagnosis. Among fossorial Malagasy microhylids, a reliable assignment to genera and especially a distinction between Plethodontohyla and Rhombophryne is at present only possible based on molecular data (Andreone et al. 2005; Frost et al. 2006; Wollenberg et al. 2008). We therefore assign Rhombophryne mangabensis to the genus Rhombophryne on the basis of the molecular phylogenetic analyses in Wollenberg et al. (2008). The molecular results indicate a high divergence of the new species to all Rhombophryne (except R. guentherpetersi for which data are lacking) and Plethodontohyla (see section on molecular differentiation below). The advertisement call of R. mangabensis furthermore provides a distinct differentiation from R. coronata, R. alluaudi, R. testudo, R. minuta, as well as Plethodontohyla inguinalis, P. mihanika, and P. notosticta (see section on advertisement calls below, and Vences et al. 2006; calls of other Rhombophryne or Plethodontohyla are unknown). Among all Rhombophryne, as well as all Plethodontohyla and species of the likewise terrestrial (but less fossorial) genera Madecassophryne and Stumpffia, the species can be identified by the following combination of morphological characters: small size (male SVL 20– 24 mm), generally smooth dorsal skin, a pair of blackish dorsal tubercles, terminal discs of fingers and toes not enlarged, tibiotarsal articulation reaches at least the tympanum when hindlimb is adpressed along body, short hands and feet (ratio HAL/SVL 0.20–0.21; FOL/ SVL 0.44–0.45), second finger of same length as fourth finger, fifth toe shorter than third toe, presence of distinct vomerine teeth, absence of sharp dorsolateral color border, absence of dorsolateral folds, absence of

# 2010 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

Zoosyst. Evol. 86 (2) 2010, 235 –243

dermal spines above eyes, absence of dermal spines along lower lip, absence of inguinal ocellae or spots, absence of contrasted pattern in inguinal region and on posteroventral part of thighs. Within Rhombophryne, the species is morphologically distinguished from its congeners as follows: from R. alluaudi by smaller size (20–24 mm vs. 40–60 mm) and presence of a pair of blackish dorsal tubercles (vs. absence); from R. coronata by absence of a series of dermal spines above eye (vs. presence); from R. laevipes by smaller size (20–24 mm vs. 45–47 mm) absence of a distinct pattern of white rounded markings on dark background in inguinal region and posteroventral side of thighs (vs. presence); from R. coudreaui by smaller size (20–24 mm vs. 28 mm), a generally smooth dorsal skin (vs. a very granular dorsal skin with dermal spines and other structures); from R. guentherpetersi by smaller size (20–24 mm vs. 32–35 mm) and absence of glandular structures in the anterior dorsolateral part of body (vs. presence according to BlommersSchlsser & Blanc 1991); from R. minuta by larger size (20–24 mm vs. 16–17 mm), presence of a pair of blackish dorsal tubercles (vs. absence), and longer relative length of hands and feet (see Glaw & Vences 1992 and photo of holotype in Blommers-Schlsser & Blanc 1991); from R. serratopalpebrosa by smaller size (20– 24 mm vs. 29–52 mm) and absence of a series of dermal spines above eye (vs. presence); from R. testudo by smaller size (20–24 mm vs. 33–45 mm), absence of a distinct pair of dorsal ridges (vs. presence) and absence of dermal barbels along the lower lip (vs. presence); and from Rhombophryne matavy, recently described by D’Cruze et al. (2010) by smaller size (20–24 mm vs. 39–49 mm) and absence of a distinct pair of dorsal ridges (vs. presence).

237

Because several species in the genus Plethodontohyla are morphologically very similar to Rhombophryne, we here also provide a brief morphological comparison of the new species to all nominal Plethodontohyla species. Rhombophryne mangabensis is distinguished from Plethodontohyla bipunctata by absence of distinct dorsal folds (vs. presence), absence of inguinal spots (vs. usually presence); from P. brevipes by longer hindlimbs (tibiotarsal articulation reaching at least tympanum vs. reaching only forelimb insertion) and presence of a pair of blackish dorsal tubercles (vs. absence); from P. fonetana by smaller size (20–24 mm vs. 54–65 mm), presence of a pair of blackish dorsal tubercles (vs. absence), and absence of distinct dorsal folds (vs. presence of thin folds); from P. guentheri by absence of enlarged finger discs (vs. presence), presence of a pair of blackish dorsal tubercles (vs. absence), and absence of a distinct dorsolateral color border (vs. presence); from P. inguinalis by much smaller size (20–24 mm vs. 55–100 mm), presence of a pair of blackish dorsal tubercles (vs. absence), and absence of enlarged finger discs (vs. presence); from P. mihanika by absence of enlarged finger discs (vs. presence), smaller size (20– 24 mm vs. 26–31 mm), absence of a distinct dorsolateral color border (vs. presence), presence of a pair of blackish dorsal tubercles (vs. absence), and absence of bluish iris color (vs. presence); from P. notosticta by smaller size (20–24 mm vs. 35–42 mm), absence of enlarged finger discs (vs. presence), presence of a pair of blackish dorsal tubercles (vs. absence), and absence of a distinct dorsolateral color border (vs. presence); from P. ocellata by smaller size (20–24 mm vs. 45– 65 mm), presence of a pair of blackish dorsal tubercles (vs. absence), and absence of large inguinal ocellae (vs. presence); and from P. tuberata by smaller size (20–

Figure 1. a. Dorsal view and b. ventral view of the preserved holotype of Rhombophryne mangabensis sp. nov. (ZSM 470/2005).

# 2010 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

museum-zoosyst.evol.wiley-vch.de

Glaw, F. et al.: New fossorial Rhombophryne

238

24 mm vs. 35–45 mm) and a generally smooth dorsal skin (vs. coarsely granular dorsal skin). Description of the holotype. Specimen in good state of preservation. A tissue sample has been removed from the right thigh (Fig. 1b). Body stout; head distinctly wider than long, not clearly wider than body; snout rounded in dorsal and lateral views; nostrils directed laterally, not protuberant, slightly nearer to eye than to tip of snout; canthus rostralis recognizable but rather indistinct, almost straight; loreal region slightly concave; tympanum distinct, rounded, 70 % of eye diameter; supratympanic fold moderately distinct but only very slightly elevated, curved behind the tympanum; tongue ovoid, posteriorly free, broader at its terminal end, not notched; maxillary teeth present; vomerine teeth present, forming two thin oblong rows posteromedial to choanae which fuse in a central patch; choanae rounded. Arms slender, very faintly marked single subarticular tubercles, well recognizable on the longest finger; flat, indistinct outer metacarpal tubercle; inner metacarpal tubercle large, forming distinct protuberance at prepollex; fingers without webbing; relative length of fingers 1 < 2 ¼ 4 < 3, fourth finger as long as second; terminal finger disks not enlarged; nuptial pads absent. Hindlimbs stout; tibiotarsal articulation reaching tympanum when hindlimb adpressed along body; tibia length 47 % of SVL; lateral metatarsalia strongly connected; an indistinct inner metatarsal tubercle present, outer metatarsal tubercles not recognizable; no webbing between toes; relative length of toes 1 < 2 < 5 < 3 < 4;

third toe distinctly longer than fifth. Skin on dorsum leathery smooth without distinct tubercles or ridges and without dorsolateral folds. Ventral skin very slightly granular. No supraocular crest above the eyes. For measurements see Table 1. After four years in preservative, dorsum light brown with slightly darker marbling. Two brownish interrupted lines, which look like elevated ridges, run from behind the eyes, converge at mid-dorsum, and run parallel for about 3 mm before fading posteriorly. In each of these lines, there is one distinct light spot at mid-dorsum, which is encircled by black spotting. Slightly behind the posterior end of these lines, there is one distinct light, darkly encircled dot on each lateral side of the dorsum. The supratympanic fold is brown and the tympanic region is partially brown, with a light patch from the posterior end of the eyes to the maxillary comissure. Flanks with a reticulated pattern of light grey. Hindlimbs light brown with distinct narrow brown crossbands on thighs, shanks and tarsus. Throat and ventral surfaces of thighs and shanks with white-brown marbling, venter uniformly light grey, with some creamy irregular patches. Throat grey with dark marbling and irregular reticulation. Cloacal region and ventral parts of tarsus and foot dark brown. Color in life unknown. Variation. The paratypes largely resemble the holotype in morphology and coloration and were thus unambiguously attributed to R. mangabensis (DNA sequences of paratypes not available). The juvenile paratype (ZFMK 52772) measured 11.8 mm SVL. All but one of the stud-

Table 1. Morphometric measurements of holotype and five adult paratypes of Rhombophryne mangabensis sp. nov. Values in parentheses refer to structures that are only weakly recognizable. Relative hindlimb length (RHL) is coded as follows: when adpressed along body, tibiotarsal articulation reaches (1) the tympanum, (2) the posterior corner of the eye, (3) the eye center. Abbreviations: M – male; HT – holotype; PT – paratype. For other abbreviations, see Materials and methods. Catalogue number

ZSM 470/2005

ZSM 471/2005

ZSM 472/2005

ZFMK 52769

ZFMK 52770

ZFMK 52771

Field number

ZCMV 886

ZCMV 2118

ZCMV 2145







Status

HT

PT

PT

PT

PT

PT

Sex

M

M (?)

M (?)

M

M

M

SVL

21.0

24.0

21.8

20.4

21.4

22.3

HW

9.7

10.4

9.4

8.8

8.9

9.9

HL

8.0

8.4

7.6

7.4

7.7

9.4

ED

2.3

2.3

2.2

2.0

2.1

2.4

TD

1.6

1.6

(1.4)

1.5

(1.4)

1.5

END

1.5

1.5

1.1

1.5

1.7

1.5

NSD

1.7

1.6

1.6

1.6

1.7

1.7

NND

2.4

3.0

2.9

3.0

2.9

3.0

HAL

4.5

4.9

4.4

4.5

4.6

4.9

FORL

8.8

10.4

8.9

10.4

9.8

10.8

HIL

30.9

36.4

32.4

32.3

34.2

35.3

FOTL

14.3

16.8

14.3

15.0

15.7

16.3

9.5

10.9

9.5

9.8

10.5

10.6

TIBL

9.9

11.2

9.6

9.8

10.5

10.7

RHL

1

1

1

2

3

FOL

museum-zoosyst.evol.wiley-vch.de

2

# 2010 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

Zoosyst. Evol. 86 (2) 2010, 235 –243

239

Figure 2. Paratypes of Rhombophryne mangabensis sp. nov. in life: a. ZSM 471/2005; b. Dorsolateral and c. ventral view of UADBA specimen (probably ZCMV 890); d. ZFMK 52770; e. ZFMK 52769.

# 2010 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

museum-zoosyst.evol.wiley-vch.de

240

ied adult paratypes have relative similar snout-vent lengths (20–22 mm), whereas ZSM 471/2005 is distinctly larger (SVL 24.0 mm). This specimen also has a more contrasting coloration especially on the dorsum including two brown chevron-like markings that run from the center posteriolaterally to the flanks. These chevron-markings are present, but indistinct in the holotype. ZSM 471/2005 also has a broader pattern of brown reticulation on the throat. Measurements of the paratypes are provided in Table 1. Color photographs of paratypes were published in Glaw & Vences (1994, 2007a) and are here shown in Figure 2. In life, the iris was bronze with irregular small black markings in its upper and lower half (with largely black areas left and right of the pupil), and without an obviously colorful iris periphery (Fig. 2). Natural History. As reported by Glaw & Vences (1992), all three adult specimens from 1991 were collected in one night, during heavy rain, when the characteristic calls of this species were heard in a rather intense chorus. Males were calling from concealed positions deep in the leaf litter of apparently primary low-altitude rainforests. We could not directly observe calling specimens, but found all three male individuals while searching for the source of call emission, and upon collection the specimens had an inflated body as typical for calling Rhombophryne. A subadult specimen, and additional smaller juveniles assigned to this species, were found exposed during the day, being active on the forest floor. Specimen collected in 2005 were found in the evening and at night in the leaf litter. As far as is known, no other species of Rhombophryne is known from Nosy Mangabe, but at least two species of Plethodontohyla (P. notosticta, P. ocellata) occur in syntopy with R. mangabensis.

Glaw, F. et al.: New fossorial Rhombophryne

cally identical vocalizations of several other males were heard. The call of Rhombophryne mangabensis (Fig. 3) consists of short series of 2–5 (3.3  0.5; n ¼ 7) whistles repeated in reasonably regular intervals. Usually, note series are widely spaced (8820 ms; n ¼ 1), but intervals between series are highly irregular. Numerical call parameters are as follows (range followed by mean  standard deviation in parentheses): note duration, 180–237 ms (198.3  14.5; n ¼ 20); inter-note interval within notes, 419–822 ms (483.8  112.7; n ¼ 14); dominant frequency range, ca. 2800–7500 Hz; maximum call energy at 3300–3550 Hz (3434  85; n ¼ 11). Weak harmonic frequency bands are recognizable at approximately 5250 and 6760 Hz. Although tonal in character, notes exhibit irregular amplitude modulation, but no distinct units are recognizable. Each note shows distinct frequency modulation, starting at approximately 3000 Hz and increasing in frequency up to 3550 Hz at about two thirds of the note’s duration, ending with a terminal drop in frequency down to 3260 Hz.

Advertisement call. Vocalizations were recorded on Nosy Mangabe on 13 March 1991 and are publicly available on audio CD (Vences et al. 2006, CD3, track 31). Calls of at least one male were analyzed, but basi-

Comparative call data. Vocalizations of the other known small species of Rhombophryne, R. minuta, from Marojejy National Park (not far from Campsite Simpona on the trail leading to the summit), were recorded on 17 February 2005 (air temperature < 20  C) using a Sony Professional Walkman (WM-D6C) with external microphone (Vivanco EM 238). The call consists of a short whistle repeated at long irregular intervals (Fig. 4). Each tonal note is composed of two distinctly separated units, with the second unit being slightly longer in duration. Numerical call parameters are as follows (range followed by mean  standard deviation in parentheses): note duration, 114–162 ms (137.7  16.4; n ¼ 10); duration of units within notes, 44–94 ms (60.7  13.3; n ¼ 18); inter-note intervals, 4660–8050 ms (6520  1416; n ¼ 5); dominant frequency range, 3500–6400 Hz; maximum call energy at 4030–4230 Hz (4143  59; n ¼ 8). A weak harmonic frequency band is recognizable at approximately 6200

Figure 3. Spectrogram and corresponding oscillogram of the advertisement call of Rhombophryne mangabensis sp. nov., recorded on Nosy Mangabe on 13 March 1991.

Figure 4. Spectrogram and corresponding oscillogram of the advertisement call of Rhombophryne minuta recorded on 17 February 2005 at Marojejy.

museum-zoosyst.evol.wiley-vch.de

# 2010 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

Zoosyst. Evol. 86 (2) 2010, 235 –243

Hz. Notes exhibit no distinct frequency modulation (Vences et al. 2006, CD3, track 30). In contrast to other Rhombophryne species which call from terrestrial positions in the leaf litter or from a few centimeters underground, this montane species emitted its calls from low but elevated positions in the vegetation. Molecular differentiation. DNA sequences of Rhombophryne mangabensis (from the holotype specimen) and most other described cophyline species were provided by Wollenberg et al. (2008) and Vieites et al. (2009). In the multi-gene phylogeny of Wollenberg et al. (2008), the species was placed with moderate bootstrap support sister to R. coudreaui, another low-elevation species from the east coast of Madagascar (however, this grouping was not supported by the Bayesian analysis). The tree of Vieites et al. (2009) was based on DNA sequences of a fragment of the 16S rRNA gene only, but included a broader sampling of candidate species of uncertain status. There, the sequence of R. mangabensis was sister to an unconfirmed candidate species

241

(R. sp. 4) from Marojejy, with high support. Uncorrected pairwise genetic distances of R. mangabensis in the 16S gene were higher than 10 % to all nominal Rhombophryne species included (all except R. guentherpetersi). The distance to R. minuta from Marojejy was 13.7 %, whereas the distance to the closest relative (R. sp. 4 from Marojejy) was 8.3 %.

Discussion As analyzed more in detail by Wollenberg et al. (2008), cophyline microhylids are characterized by a high degree of microendemism. While a few widespread species such as Platypelis grandis and P. tuberifera, Plethodontohyla notosticta, P. mihanika or P. ocellata exist, most species are known only from very small ranges or even single localities. Although this might be due to incomplete knowledge of some species, it might reflect reality in others. The new species described

Figure 5. Rhombophryne minuta from Marojejy in life: a. ZSM 476/2005; b. UADBA (uncatalogued); c. ZSM 477/2005; d. ZSM 476/2005.

# 2010 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

museum-zoosyst.evol.wiley-vch.de

Glaw, F. et al.: New fossorial Rhombophryne

242

herein, Rhombophryne mangabensis, has so far been recorded from only a single locality, Nosy Mangabe, and the population that appears genetically most closely related occurs on the Marojejy massif (Vieites et al. 2009) and has a very high genetic differentiation. We assume that R. mangabensis also occurs on the mainland adjacent to Nosy Mangabe as do most other frog species present on this tiny offshore island, and is possibly also more widespread on the Masoala peninsula. In general, the center of diversity and endemism of Rhombophryne is in northern Madagascar (Wollenberg et al. 2008, D’Cruze et al. 2010). The distribution of R. mangabensis fits into this picture. In general, advertisement calls of fossorial microhylids are poorly known. Because only few Rhombophryne calls are so far known, it is difficult to discuss call evolution in this lineage. However, it is remarkable that Rhombophryne calls appear to deviate at least partly from the general cophyline pattern. Species in this subfamily are usually characterized, with few exceptions, by a simple structure of calls: a single melodious note is usually repeated after regular intervals in long series that can last several minutes (Glaw & Vences 1994, 2007a; Vences et al. 2006). In Rhombophryne, a slight deviation from this pattern is that the call of Rhombophryne testudo has a relatively low frequency, and the calls of R. testudo and R. alluaudi are repeated usually after very long intervals, hardly definable as note series, as intervals become irregular (see Vences et al. 2006 for the corresponding sound files). Only during heavy rainfalls short note series (2–3 notes) followed by minutes of silence can be heard in Rhombophryne testudo. Also in R. coronata, and in the recently described R. matavy (D’Cruze et al. 2010), the note series are relatively short (5–12 notes only) instead of being a long monotonous series that can last for several minutes. Rhombophryne minuta emits a single melodious note, which, however, is composed of two units. This unusual note structure including two units is so far unknown from other cophylines and needs further study. It might suggest a sound production system in R. minuta, which differs from the purely expiratory sound production typical for the other species in this subfamily. Rhombophryne mangabensis, similar to R. coronata, emits a short series of notes, and these note series are repeated after long and irregular intervals. Thus, although some aspects of call structure in Rhombophryne agree with other microhylids (a single note type only; notes usually being melodious), it appears that in this genus especially the long and monotonous repetition of notes in series has been modified in various ways. One shared character of at least some species with fossorial calling positions like Rhombophryne testudo, the recently described R. matavy (D’Cruze et al. 2010), and R. mangabensis is the fact that calling intensity is high and calling activity at least somewhat regular only during very heavy rainfalls. Under these conditions it is comparatively easy for humans to locate calling males, which however are very hard to find when no or little rain is

museum-zoosyst.evol.wiley-vch.de

falling. Although the calls of R. mangabensis are quite easy to recognize and there are few other records of small-sized Rhombophryne species except from the general area comprising Masoala, Marojejy and Tsaratanana, the current knowledge does not allow any reliable statement of the extent of occurrence and area of occupancy of this species. We therefore propose a Red List status of “Data Deficient” for this species.

Acknowledgements We are grateful to Roger-Daniel Randrianiaina for his help in the field. This work has been carried out in the framework of collaboration agreements of the author’s 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.

References Andreone, F. & Randrianirina, J. E. 2008. An unexpected Rhombophryne record at Tsingy de Bemaraha confirms the presence of cophyline frogs in western Madagascar. – Zootaxa 1812: 46–48. Andreone, F., Vences, M., Vieites, D. R., Glaw, F. & Meyer, A. 2005. Recurrent ecological adaptations revealed through a molecular analysis of the secretive cophyline frogs of Madagascar. – Molecular Phylogenetics and Evolution 34: 315–322. Blommers-Schlsser, R. M. A. 1975. Observations on the larval development of some Malagasy frogs, with notes on their ecology and biology (Anura: Dyscophinae, Scaphiophryninae and Cophylinae). – Beaufortia 24 (309): 7–26. Blommers-Schlsser, R. M. A. & Blanc, C. P. 1991. Amphibiens (premire partie). – Faune de Madagascar 75 (1): 1–379. D’Cruze, N., Khler, J., Vences, M. & Glaw, F. 2010. A new fat fossorial frog (Microhylidae: Cophylinae: Rhombophryne) from rainforest of the Fort d’Ambre Special Reserve, northern Madagascar. – Herpetologica 66 (2): 182–191. Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F. B., De Sa, R. O., Channing, A., Wilkinson, M., Donnellan, S. C., Raxworthy, C. J., Campbell, J. A., Blotto, B. L., Moler, P., Drewes, R. C., Nussbaum, R. A., Lynch, J. D., Green, D. M. & Wheeler, W. C. 2006. The amphibian tree of life. – Bulletin of the American Museum of Natural History 28: 1–370. Glaw, F., Khler, J., Bora, P., Rabibisoa, N. H. C., Ramilijaona, O. & Vences, M. 2007. Discovery of the genus Plethodontohyla (Anura: Microhylidae) in dry western Madagascar: description of a new species and biogeographic implications. – Zootaxa 1577: 61–68. Glaw, F. & Vences, M. 1992. A Fieldguide to the Amphibians and Reptiles of Madagascar, First Edition. Vences and Glaw Verlag, Kln. Glaw, F. & Vences, M. 1994. A Fieldguide to the Amphibians and Reptiles of Madagascar, Second Edition. Vences and Glaw Verlag, Kln. Glaw, F. & Vences, M. 2007a. A Field Guide to the Amphibians and Reptiles of Madagascar. Third Edition. Vences and Glaw Verlag, Kln. Glaw, F. & Vences, M. 2007b. Plethodontohyla guentheri, a new montane microhylid frog species from northeastern Madagascar. – Mitteilungen des Museums fr Naturkunde Berlin, Zoologische Reihe 83: 33–39. Khler, J. 2000. Amphibian diversity in Bolivia: a study with special reference to montane forest regions. – Bonner zoologische Monographien 48: 1–243.

# 2010 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

Zoosyst. Evol. 86 (2) 2010, 235 –243

Van der Meijden, A., Vences, M., Hoegg, S., Boistel, R., Channing, A. & Meyer, A. 2007. Nuclear gene phylogeny of narrowmouthed toads (Family: Microhylidae) and a discussion of competing hypotheses concerning their biogeographical origins. – Molecular Phylogenetics and Evolution 44: 1017–1030. Vences, M. & Glaw, F. 2003. New microhylid frog (Plethodontohyla) with a supraocular crest from Madagascar. – Copeia 2003: 789– 793. Vences, M., Glaw, F. & Marquez, R. (eds) 2006. The Calls of the Frogs of Madagascar. 3 Audio CD’s and booklet, 44 pp. Alosa, Barcelona.

# 2010 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

243

Vences, M., Raxworthy, C. J., Nussbaum, R. A. & Glaw, F. 2003. New microhylid frog (Plethodontohyla) from Madagascar, with semiarboreal habits and possible parental care. – Journal of Herpetology 37: 629–636. Vieites, D. R., Wollenberg, K. C., Andreone, F., Khler, J., Glaw, F. & Vences, M. 2009. Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory. – Proceedings of the National Academy of Sciences of the U.S.A. 106: 8267–8272. Wollenberg, K. C., Vieites, D. R., van der Meijden, A., Glaw, F., Cannatella, D. C. & Vences, M. 2008. Patterns of endemism and species richness in Malagasy cophyline frogs support a key role of mountainous areas for speciation. – Evolution 62: 1890–1907.

museum-zoosyst.evol.wiley-vch.de