Mantidactylus inaudax ( Peracca, 1893 )

Scherz, Mark D., Crottini, Angelica, Hutter, Carl R., Hildenbrand, Andrea, Andreone, Franco, Fulgence, Thio Rosin, Köhler, Gunther, Ndriantsoa, Serge Herilala, Ohler, Annemarie, Preick, Michaela, Rakotoarison, Andolalao, Rancilhac, Loïs, Raselimanana, Achille P., Riemann, Jana C., Rödel, Mark-Oliver, Rosa, Gonçalo M., Streicher, Jeffrey W., Vieites, David R., Köhler, Jörn, Hofreiter, Michael, Glaw, Frank & Vences, Miguel, 2022, An inordinate fondness for inconspicuous brown frogs: integration of phylogenomics, archival DNA analysis, morphology, and bioacoustics yields 24 new taxa in the subgenus Brygoomantis (genus Mantidactylus) from Madagascar, Megataxa 7 (2), pp. 113-311 : 282-287

Mantidactylus inaudax ( Peracca, 1893) bona species

Type material.— The nomen is based on a series of three syntypes, originally under the single number MZUT An727 , but now divided into An727.1 – An727.3 , from ‘ dintorni di Andrangoloaka e dalla vicina valle dell’Umbi’ ( Gavetti &Andreone1993; Peracca1893). Andrangoloaka is at ca 19.00°S, ca 047.95°E. These specimens were thought lost by Guibé (1978) and Blommers-Schl̂sser and Blanc (1991) but were rediscovered by Gavetti and Andreone (1993). We here designate as lectotype MZUT An727.1 , an adult female individual of 32.1 mm SVL ( Fig. 73 ). Lectotype designation is justified by the need to stabilize this and other nomina in Brygoomantis , given the uncertain identity and morphological similarity of many taxa in the subgenus.

Identity.— The name Rana inaudax Peracca, 1893 was placed in the synonymy of M. curtus by BlommersSchl̂sser and Blanc (1991) although this synonymy was doubted by Gavetti and Andreone (1993) because it was not based on specimen examination (see also Frost 2021). We here provide a 16S sequence of the lectotype that clusters with a lineage from various localities not far from the type locality of Andrangoloaka (e.g. Fierenana and the road between Moramanga and Anosibe An’Ala). We thereby provide genetic evidence of the assignment of the nomen inaudax to this lineage, which was previously considered as the true M. biporus ( Vieites et al. 2009) , and we therefore revalidate the name M. inaudax for this lineage. The lineage to which the lectotype belongs is closely related to another from Ambohitantely and other nearby sites that has been assigned to candidate species M. sp. 17 by Vieites et al. (2009), and M. sp. Ca17 by Perl et al. (2014). It was depicted as ‘ M. sp. aff. biporus “Ambohitantely”’ by Glaw and Vences (2007). In the course of this study, we discovered several other deep lineages from the western slope of the Makira reserve, from Ampotsidy, and from Fierenana and the road Moramanga to Anosibe An’Ala (previously considered as the true M. biporus ) that all form a mitochondrial clade with Ca17 and partly share Rag-1 haplotypes with it. Our phylogenomic analysis of this clade recovers these different lineages as a monophyletic group, but with a different topology of relationships among them than recovered in our mitochondrial tree. We conservatively treat all of these deep lineages as conspecific.

Additional material. — The following specimens are all tentatively assigned to M. inaudax , despite substantial genetic variation among several populations (visualized in Fig. 2 ): ZSM 180/2005 ( FGZC 2146 ), adult male, and ZSM 181/2005 ( FGZC 2147 ), adult female, collected by M. Vences, L. du Preez, P. Bora, L. Raharivololoniaina, R.D. Randrianiaina, T. Razafindraibe, and E. Randriamitso on 18 January 2005 at Ambohitantely Jardin Botanique (ca 18.17°S, ca 047.27°E, ca 1580 m a.s.l.) ; ZFMK 60141–60142 , adult male and female, collected by F. Glaw and D. Vallan on 6 April 1995 at Ambohitantely (ca 18.17°S, ca 047.27°E, ca 1580 m a.s.l.) ; ZMA 19310 ( FGMV 2002.2435 ), ZMA 19311 ( FGMV 2002.2439 ), ZMA 19314 ( FGMV 2002.2429 ), ZMA 19331 ( FGMV 2002.2441 ), four adult females, ZMA 19341 ( FGMV 2002.2252 ), putative female, and ZMA 19343 ( FGMV 2002.2423 ) and ZMA 19345 ( FGMV 2002.2251 ), two adult males, collected by M. Vences, D.R. Vieites, and collaborators on 19 February 2003 in Fierenana (18.5299°S, 048.5901°E) ; ZSM 1768/2008 ( ZCMV 8869 ), adult male, collected by D.R. Vieites, J. Patton, P. Bora, and M. Vences on 22 February 2008 in the Andranogorika forest fragment, near the road to Brieville (17.76781°S, 047.98415°E) ; ZSM 363/2010 ( FGZC 4358 ), adult male, collected by F. Glaw, J. K̂hler, P.-S. Gehring, M. Pabijan, K. Mebert, E. Rajeriarison, F. Randrianasolo, and S. Rasamison on 8 April 2010 in Fanamby forest (18.4214°S, 047.9383°E, 1315 m a.s.l.) ; ZSM 398/2006 ( ZCMV 3259 ), adult male, collected by M. Vences, R.D. Randrianiaina, and E. Edwards on 25 March 2006 at the crossroad between Moramanga–Anosibe An’Ala and Besariaka (19.0959°S, 048.2402°E) ; ZSM 548/2009 ( ZCMV 11213 ), adult male, collected by M. Vences, D.R. Vieites, F.M. Ratsoavina, R.D. Randrianiaina, E. Rajeriarison, T. Rajofiarison, and J. Patton on 23 June 2009 at Hevirina (pandanus swamp), Makira (15.4490°S, 049.1119°E, 1093 m a.s.l.) ; ZSM 85/2016 ( MSZC 0161 ), adult male, collected by M.D. Scherz, J. Borrell, L. Ball, T. Starnes, E. Razafimandimby, D.H. Nomenjanahary, and J. Rabearivony on 8 January 2016 beside a muddy spring in Ampotsidy , Bealanana District (14.4194°S, 048.7194°E, 1340 m a.s.l.) ; ZSM 88/2016 ( MSZC 0178 ), adult male, collected by M.D. Scherz, J. Borrell, L. Ball, T. Starnes, E. Razafimandimby, D.H. Nomenjanahary, and J. Rabearivony on 8 January 2016 in a pandanus swamp in Ampotsidy , Bealanana District (14.4169°S, 048.7144°E, 1371 m a.s.l.) .

Diagnosis.— Mantidactylus inaudax belongs to the M. inaudax clade according to our phylogenomic analysis.See Table4 for a list of diagnostic morphological characters. The combination of small to moderate body size (male SVL 22–30 mm, female SVL 27–33 mm), rather smooth dorsal skin without dorsolateral ridges, large tympanum size in males (12–16% of SVL), presence of white spots on flanks in at least some individuals, and absence of a white marking on the snout tip, distinguishes M. inaudax from species of the M. betsileanus , M. curtus , M. fergusoni , M. tricinctus , and M. ulcerosus clades. M. stelliger ( M. stelliger clade) differs by smaller body size and less developed foot webbing. Species of the M. biporus clade differ as follows: M. biporus by smaller tympanum in males, and a higher pulse repetition rate in advertisement calls; M. augustini by longer hindlimbs, fewer pulses per note, and lower pulse repetition rate in advertisement calls; M. bletzae by a somewhat smaller body size, presence of dorsolateral ridges, longer hindlimbs, and more developed foot webbing; M. brevirostris by less developed foot webbing, possibly smaller body size, and differences in colour pattern; M. eulenbergeri by smaller body size; M. glosi by smaller body size, more granular dorsal skin and shorter hindlimbs ( Table 4 ). For a distinction from new species and subspecies in the M. inaudax clade, see the diagnoses in the respective taxa accounts below. A full list of molecular diagnostic sites in the 16S gene of M. inaudax in pairwise comparisons to all other Brygoomantis species is provided as Supplementary appendix.

Translation of original description.— To facilitate a revised treatment of this nomen, we here provide a translation of Peracca’s detailed description of Rana inaudax from the original Italian:

Vomerine teeth in two oblique groups behind the posterior margin of the choanae.

Cordiform tongue, rather small, bifurcated in two posteriorly short rounded appendages.

Moderate head, subacute snout protruding about 1 mm over the lower jaw; rounded canthus rostralis; slightly concave loreal region; inter-orbital space equal in width to the upper eyelid, equaling the distance between the antero-internal eye and nostril.

Tympanum clearly visible, about ¾ of the eye diameter, equal in diameter to the distance between the antero-internal corner of the eye and the nostril, surmounted by a small skin fold starting from the posterior-external corner of the eye and disappearing at the origin of the arm.

Digits of the feet terminated by discs almost twice as large as those of the hands. Internal metatarsal tubercle oval, protruding, very large. A small external metatarsal tubercle, conical. Almost entirely webbed toes. By pulling the posterior extremities forward along the body, the tibio-tarsal joint barely reaches the posterior corner of the eye.

The skin of the head, the back, the hips, the upper surface of the posterior extremities, and the posterior surface of the thighs is finely granular; in other regions it is smooth. On the lower surface of the thighs a small circular glandular relief can be observed on each side, presenting a median depression in which 5 or 6 point-like pores (femoral pores) are visible.

Colouration—Basic colour of the upper parts grey-brown or slate grey, more or less light. A black spot connects the eyes, preceded by a lighter band. On the back there is an irregular dark spot, sometimes shaped like a V. The posterior extremities have narrow black bands. The lips and cheeks are dotted with white. Lower face of a dirty yellowish white, turning to flesh-grey on the throat, irregularly speckled with white.

Dimensions:

♀ ♀ ♁ Length from snout to vent mm 33 29.5 22

of the arm 18.5 15.5 13.5

of the leg 47.5 38 32

of the shank 14.5 12 10

of the foot 15 13 10.5 Head width 13 11 9 Inner metatarsal tubercle 2 2 1.5 Three specimens.

Description of referred specimen ZSM 180/2005 (FGZC 2146).— Adult male in good state of preservation.

Tissue removed from right thigh; femoral glands partly detached for examination in internal view. Body rather stout. Head as wide as body. Snout rounded in dorsal and lateral views. Nostrils directed laterally, slightly protuberant. Nostrils nearer to tip of the snout than to eye.

Canthus rostralis weak, slightly concave. Loreal region weakly concave. Tympanum distinct, large, elliptical, diameter 78% of eye diameter. Supratympanic fold distinct, beginning straight, with a rather distinct bend midway towards insertion of forelimb, following the outer edge of the tympanum. Tongue ovoid, distinctly posteriorly bifid. Maxillary teeth present. Vomerine teeth present in two rounded aggregations, positioned posterolateral to choanae. Choanae rounded. Subarticular tubercles single.

Outer and inner metacarpal tubercles present. Fingers without webbing. Relative length of fingers: I<II<IV<III.

Finger discs slightly enlarged. Nuptial pads absent. Foot longer than tibia (113%). Lateral metatarsalia separated.

Inner metatarsal tubercle present. Outer metatarsal tubercle not clearly recognisable. Webbing formula: 1(1), 2i(1), 2e(0.5), 3i(1.5), 3e(1), 4i(2), 4e(2), 5(1). Relative length of toes: I<II<V<III<IV. Skin on the upper surface smooth.

Ventral side smooth. Femoral glands present, in external view consisting of a well-recognisable distal ulcerous macrogland and a distinct proximal granular gland field.

Colour in preservative: dorsum brown, with indistinct irregular darker markings. Dark brown band between eyes present. Forelimbs brown with poorly defined darker markings. Hindlimbs light brown with indistinct darker crossbands. Inguinal region with few scattered whitish dots. Snout tip with an indistinct light dot. Venter beige, throat darker than belly. Lower lip with indistinct alternating light and brown spots. Toe discs dark. Fourth toe quite short in relation to third and fifth toe.

Variation.—Variation in measurements is given in Table 11. See Fig. 74 for colouration in life and its variation. There is pronounced sexual size dimorphism (confirmed male SVL 21.7–25.1 mm [n = 10] vs confirmed female SVL 26.9–32.1 mm [n = 7]). Males have larger tympanum sizes than females (HTD/ED ratio is 63–82% in females, 84–111% in males). Skin on the back is smooth (ZSM 180/2005) or granular (ZFMK 60141, ZFMK 60142). Colour on the back is light brown with few indistinct markings in ZFMK 60141 and ZFMK 60142, darker brown with few indistinct markings in ZSM 180/2005. A dark brown more or less triangular band between eyes is always present. Two dark spots on the back at the level of the forelimb insertion are always present (not visible for ZFMK 60141 and ZFMK 60142 because their skin is in pieces). A light vertebral line or a light vertebral band are never present. A small but distinct light dot on the snout tip is present in the two males. Lower lip with more (e.g. ZFMK 60141) or less (e.g. ZFMK 60142) distinct alternating light and brown spots. Venter and throat from uniformly beige in ZFMK 60141 and ZFMK 60142 or brown with distinct mottling in ZSM 180/2005. A longitudinal white median line on abdomen and throat is never present. Hindlimbs more or less distinctly striped. Forelimbs brown with irregular darker markings and stripes. Femoral glands of adult males are consistently large and prominent. The femoral glands of ZSM 180/2005 have an extensive proximal granular gland field, while such a structure is not recognisable in ZFMK 60141. In external view an external central depression in the distal ulcerous macrogland component of the femoral glands can be seen, and in life, the glands are of yellowish colour. In females femoral glands cannot be recognised in preservative, but in life, rudimentary glands consisting of two or three small structures of similar size are recognisable ( Fig. 74e, l ).

Natural history.—Regularly found in clean, running waters, often in areas of highly disturbed and degraded rainforest, but also in springs and swamps within undisturbed rainforest. Near Moramanga calling males were heard and collected during the day, from a slowly moving small stream near degraded rainforest and with just some remaining trees close to the water.

Calls.—The advertisement call of M. inaudax , recorded on 23 June 2009, at Makira West, at an estimated air temperature of 20–25°C, consisted of a pulsed note, emitted isolated or in short series containing 5–7 calls ( Fig. 75 ). Notes exhibit amplitude modulation, with call energy rapidly increasing from the beginning of the note, reaching its maximum after approximately one third of the note’s duration. Pulse repetition rate within notes was highest at the beginning and decreases towards the note’s end. Numerical parameters of 14 analysed calls were as follows: call duration (= note duration) 196–367 ms (268.6 ± 66.4 ms); 19–28 pulses per note (22.6 ± 3.9); pulse duration 3–6 ms (4.3 ± 0.9 ms); pulse repetition rate within notes 55.6–130.4 pulses/s (85.8 ± 23.9); dominant frequency 1146–1276 Hz (1200 ± 41 Hz); prevalent bandwidth 800–3400 Hz; call repetition rate (= note repetition rate) within series ca 75 calls/min.

Calls recorded on 25 March 2006 at the crossing of the Moramanga-Anosibe An’Ala and Besariaka roads, at an estimated air temperature of 20–25°C, were emitted in regular series and agreed perfectly in character with the calls described from Makira West above and differd only slightly in numerical parameters (n = 9): call duration (= note duration) 199–312 ms (254.9 ± 35.9 ms); 17–23 pulses per note (20.3 ± 2.2); pulse duration 3–7 ms (4.7 ± 1.1 ms); pulse repetition rate within notes 61.2–142.9 pulses/s (87.1 ± 28.9); dominant frequency 738–961 Hz (814 ± 72 Hz); prevalent bandwidth 500–3500 Hz; call repetition rate (= note repetition rate) within series ca 60–90 calls/min. The most significant difference was the lower dominant frequency which was possibly due to a larger SVL of the calling male.

Tadpoles.— The tadpole of M. inaudax was described under the name ‘ M. biporus ’ by Knoll et al. (2007).

Distribution.— Endemic to the highlands and rainforests of the Northern Central East and Central Madagascar, also occurring at sites in the North West and Ambirano Regions ( Fig. 7 ). This species is known from Ambohitantely, Ampotsidy, Andrangoloaka, Anjozorobe, Fierenana, the vicinity of Lake Alaotra, the western slope of Makira, and the Moramanga-Anosibe An’Ala/ Besariaka crossroad. Elevation range: 948–1580 m a.s.l.

Etymology.— Latin adjective meaning ‘shy’ or ‘hesitant’. It is a third-declension one-termination adjective, and thus is effectively invariable with respect to the gender of the genus.

Figures

FIGURE 2. Maximum Likelihood tree of 1305 sequences of a fragment of the 16S rRNA gene (alignment length 519 bp) from a RAxML analysis. Numbers at nodes are bootstrap proportions in percent (100 ML fast bootstrap replicates); not shown if <50%. A sequence of Mantidactylus melanopleura was used as the outgroup (removed from the tree after analysis for better graphical representation). Note that some of the ‘Museomics’ sequences (obtained by targeted capture from historical type specimens) are represented twice, after assembly with different reference sequences. Some sequences in the analysis (several ‘Museomics’ sequences as well as others obtained from Illumina sequencing) only partially covered the fragment analysed (226 sequences <300 bp). We emphasize that this tree is based on a single short mitochondrial marker and therefore is unlikely to represent the deep relationships among lineages correctly; for such relationships, refer to the phylogenomic tree (Fig. 5).

FIGURE 7. Mantidactylus subgenus Brygoomantis species distribution based on verified records, divided by clade (Mantidactylus stelliger sp. nov. is presented alongside the inaudax clade for practicality). Colours for species correspond to those in Figs 2 and 4. Inset map shows the geographic regions of Madagascar identified by Boumans et al. (2007), referred to throughout the text.

FIGURE 73. Preserved lectotype of Mantidactylus inaudax, and holotype specimens of newly named species and subspecies in the M. inaudax clade. Scale bars equal 5 mm.

FIGURE 74. Mantidactylus inaudax in life, in dorsolateral and ventral view. (a,b) Adult male from a forest fragment west of Lake Alaotra, photographed in 2008. (c,d,e) Adult female from a forest fragment west of Lake Alaotra, photographed in 2008, and femoral gland closeup (e). (f,g) Adult male from a forest fragment west of Lake Alaotra, photographed in 2008. (h,i) Adult male from a forest fragment west of Lake Alaotra, photographed in 2008. (j,k,l) Adult female from Fierenana, photographed in 2003, and femoral gland closeup (l). (m,n,o) Adult male from Fierenana, photographed in 2003, and femoral gland closeup (o). All of these specimens correspond to collected voucher specimens but cannot be reliably assigned to specific voucher numbers.

FIGURE 75. Audiospectrogram and corresponding oscillogram of one advertisement call of Mantidactylus inaudax, recorded on 23 June 2009 at Makira West (air temperature estimated at 20–25°C). Recording bandpass-filtered at 640–6500 Hz.