Mantidactylus fergusoni, Scherz & Crottini & Hutter & Hildenbrand & Andreone & Fulgence & Köhler & Ndriantsoa & Ohler & Preick & Rakotoarison & Rancilhac & Raselimanana & Riemann & Rödel & Rosa & Streicher & Vieites & Köhler & Hofreiter & Glaw & Vences, 2022

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 : 237-244

Mantidactylus fergusoni sp. nov.

Identity and justification.—This lineage has been previously considered as confirmed candidate species M. sp. 26 by Vieites et al. (2009) and M. sp. Ca26 by Perl et al. (2014). It was depicted as ‘ Mantidactylus sp. aff. betsileanus “Andranofotsy”’ by Glaw and Vences (2007). Our phylogenomic analysis confirms that this lineage is in a major clade (here named the M. fergusoni clade) containing only scientifically unnamed lineages, and its status as distinct species is therefore out of question. However, deciding how many species exist in this clade is complicated. Mantidactylus sp. Ca26 forms a clade with several other divergent mitochondrial lineages of uncertain status; here we consider the lineage previously named M. sp. 21 ( Vieites et al. 2009) or M. sp. Ca21 ( Perl et al. 2014) from Nosy Mangabe, Makira, Masoala, and Cap Est/Ambato as conspecific with M. fergusoni (note that M. sp. 21 was wrongly placed in the tree of Vieites et al. [2009], probably due to a sequence confusion in the alignment used for phylogenetic analysis). As a further deep conspecific lineage we consider samples from Marojejy and additional sites in the North East. Samples from Nosy Boraha (M. sp. Ca27) according to our phylogenomic analysis ( Fig. 5 ) form a clade with the lineage M. sp. Ca25 (see Vieites et al. 2009) from different sites on the mainland adjacent to Nosy Boraha, and together are sister to M. fergusoni sp. nov.; the Nosy Boraha population is described below as M. jahnarum sp. nov. based on its bioacoustic differentiation.

Holotype.— ZSM 126/2002 (MV 2001.1389), adult male, collected by M. Vences on 17 December 2001 at Andranofotsy (15.4353°S, 049.8439°E, 85 m a.s.l.), Analanjirofo Region , Madagascar. A 16S barcode sequence of the holotype is available from GenBank (accession AY848214 ).

Paratypes.— A total of six paratypes : ZSM 124/2002 ( MV 2001.1433 ), female, ZSM 125/2002 ( MV 2001.1434 ), adult male, and ZSM 176/2002 ( FGMV 2001.1383 ), specimen of unknown sex and maturity, all with the same collection data as the holotype; ZSM 5050/2005 ( ZCMV 2125 ), adult female, and ZSM 5051/2005 ( ZCMV 2136 ), adult male, collected by F. Glaw, M. Vences, and R.D. Randrianiaina on 22 February 2005 on Nosy Mangabe (ca 15.50°S, 049.77°E, 50–100 m a.s.l.); ZSM 355/2010 ( FGZC 4277 ), adult female, collected by F. Glaw, J. K̂hler, P.-S. Gehring, M. Pabijan, F.M. Ratsoavina on 3 April 2010 at Ambodivoahangy (15.2899°S, 049.6203°E, ca 100 m a.s.l.) .

Additional material.— The following three specimens are assigned to M. fergusoni sp. nov. but come from a genetically divergent population and have in part (ZFMK specimens) not been sequenced, and therefore they are not included in the paratype series: ZSM 201/2005 ( FGZC 2746 ), adult male, collected by F. Glaw, M. Vences, and R.D. Randrianiaina on 14 February 2005 at Marojejy, Camp 1 ‘Mantella’ (14.4377°S, 049.7756°E, 481 m a.s.l.); ZFMK 59938 , adult male, and ZFMK 59939 , adult female, collected by F. Glaw and O. Ramilison on 22 February 1995 at Marojejy (near Camp Mantella ).

Diagnosis.—A member of the M. fergusoni clade as revealed by the phylogenomic analysis, and sister to M. jahnarum sp. nov. described below. See Table 4 for a list of diagnostic morphological characters. The combination of a small to moderate body size in males (SVL up to 25– 30 mm) and distinctly larger body size in females (36– 42 mm), tubercular dorsal skin, large tympanum size in males (10–14% of SVL), absence of white spots on flanks and of white marking on snout tip, and advertisement call consisting of a single-pulse note distinguishes M. fergusoni sp. nov. from most species of the other clades. Two species from the M. ulcerosus clade ( M. ulcerosus and M. bellyi ) can be morphologically similar, but they occur in the Sambirano and North West regions, and have strongly differing advertisement calls ( Table 4 ). One species of the M. betsileanus clade ( M. katae ) has an advertisement call of similar general structure, but has a faster and more regular call repetition rate, less tubercular dorsum, larger femoral glands, and a distinct white marking on snout tip ( Table 4 ). M. fergusoni sp. nov. may also show superficial similarities to other species of the M. betsileanus clade but does not appear to occur sympatrically with any of them; in general it has a more tubercular dorsum and differs from all of these by advertisement call structure ( Table 4 ). The M. fergusoni clade contains only species newly named herein; for a distinction from these other species, see below. A full list of molecular diagnostic sites in the 16S gene of M. fergusoni sp. nov. in pairwise comparisons to all other Brygoomantis species is provided as Supplementary appendix.

Description of the holotype.—Adult male in good state of preservation ( Fig. 48 ). Part of left shank muscle removed as tissue sample, femoral glands partly detached for examination in internal view. Body slender. Head wider than body. Snout rounded.Nostrils directed laterally, slightly protuberant. Nostrils nearer to tip of the snout than to eye. Canthus rostralis very weak, slightly concave.

Loreal region concave. Tympanum distinct, large, slightly wider than high, its horizontal diameter about 91% of eye diameter. Supratympanic fold present, beginning straight, with a rather distinct bend midway towards jaw / forelimb insertion. Tongue ovoid, distinctly bifid. Maxillary teeth present. Vomerine teeth present in two rounded to ovoid aggregations, positioned posterolateral to choanae. Choanae rounded. Subarticular tubercles single. Inner and outer metacarpal tubercles present. Fingers without webbing.

Relative length of fingers: I≤II<IV<III. Finger discs slightly enlarged. Nuptial pads absent. Foot slightly longer than tibia (104%). Lateral metatarsalia separated. Inner and outer metatarsal tubercles present. Webbing formula: 1(0.5), 2i(1.5), 2e(0.5), 3i(2), 3e(1), 4i(2.5), 4e(2), 5(0.5).

Relative length of toes: I<II<V=III<IV. Skin on the upper surface quite smooth in preservative (but rather tubercular in life). Ventral side smooth. Femoral glands present, with a distinct and large distal ulcerous macrogland internally consisting of six large granules. Proximal granular gland field relatively indistinct, only recognisable in internal view.

Colour in preservative: dorsum brown with a minimal reddish shade. Forelimbs and hindlimbs with distinct brown crossbands. Venter beige, chest and throat rather dark brown with distinct light markings and a central median line on throat. Colour in life was similar to preservative, but with a distinct reddish-brown colour dorsally.

Variation.—Variation in measurements is given in Table 8. See Fig. 49 for colouration in life and its variation. There is pronounced sexual size dimorphism (confirmed male SVL 24.9–29.9 mm [n = 5] vs confirmed female SVL 35.7–42.2 mm [n = 4]). Males have a somewhat larger tympanum than females (HTD/ED ratio is 69–67% in females, 67–96% in males). Femoral glands are distinct but not particularly prominent in males, and only with a slight yellowish tone in life; very small, rudimentary glands recognisable in females.

Natural history.—Habitat and habits of this species are poorly known, but so far it has been found in primary or somewhat degraded rainforest. At Andranofotsy, calling males were observed at night from the shore of a shallow puddle next to a small spring in rainforest.

Calls.—The advertisement call of M. fergusoni , recorded on 16 December 2001 near Andranofotsy, 25.4°C air temperature ( Vences et al. 2006, CD 2, track 69), consists of a simple, short, single pulse ‘click’ note, emitted in series ( Fig. 50 ). Inter-call intervals were irregular with some calls (= notes) occurring in pairs with lower inter-call interval inbetween. Call energy was distributed in a wide frequency band. Numerical parameters of 13 analysed calls were as follows: call duration (= note duration) 9–12 ms (10.5 ± 0.8 ms); 1 pulse per note (1.0 ± 0.0); pulse duration = note duration = call duration; dominant frequency 1626–1690 Hz (1669 ± 26 Hz); prevalent bandwidth 700–5700 Hz; call repetition rate (= note repetition rate) within series ca 210–290 calls/min.

Calls recorded on 31 March 2010 at Ambodivohangy, Makira area (from specimen ZSM 361/2010 = FGZC 4219), 24°C estimated air temperature, agree with those described above from Andranofotsy, apart from somewhat lower call repetition rate within series. Calls consisted of a simple short ‘click’ note emitted isolated or more often in series at irregular intervals. Numerical parameters of 28 analysed calls were as follows: call duration (= note duration) 7–13 ms (8.9 ± 1.4 ms); 1 pulse per note (1.0 ± 0.0); pulse duration = note duration = call duration; dominant frequency 1571–1722 Hz (1638 ± 54 Hz); prevalent bandwidth 700–5500 Hz; call repetition rate (= note repetition rate) within series ca 100–170 calls/min.

Tadpoles.— The tadpole of this species has not been described.

Voucher Field number Sex Locality SVL HW HL ED HTD END NSD NND FORL HAL HIL FOTL FOL TIBL FGL FGW M. fergusoni sp. nov. (Ca26) ZSM 126/2002 [HT] FGMV 2001.1389 M Andranofotsy 27.8 10.3 11.6 4.4 4.0 3.0 1.9 2.8 17.5 8.7 48.7 22.5 15.1 14.5 3.6 2.6 ZFMK 59938 # NA M Marojejy, Camp Mantella 26.0 10.6 9.7 3.9 2.6 2.9 1.8 2.9 8.9 8.0 NM NM 13.4 14.5 2.8 2.2 ZSM 125/2002 [PT] FGMV 2001.1434 M Andranofotsy 26.2 10.1 11.2 4.2 3.1 2.4 2.0 3.1 15.8 7.7 41.8 19.1 13.3 13.4 3.9 2.4 ZSM 201/2005 # FGZC 2746 M Marojejy, Camp Mantella 24.9 9.9 10.0 4.1 3.3 2.7 1.8 2.7 10.2 7.9 NM NM 12.3 14.0 3.4 2.3 ZSM 5051/2005 [PT] ZCMV 2136 M Nosy Mangabe 29.9 11.4 12.8 4.1 3.6 3.5 2.4 3.3 17.6 8.5 45.6 21.0 14.0 14.8 3.7 2.5 ZFMK 59939 # NA F Marojejy, Camp Mantella 35.7 14.7 13.4 5.4 2.9 3.8 2.1 4.0 12.7 10.4 NM NM 16.3 19.6 NA NA ZSM 124/2002 [PT] FGMV 2001.1433 F Andranofotsy 36.1 13.6 14.5 5.6 3.6 3.9 2.3 3.1 22.5 10.2 60.2 28.3 19.4 18.9 NA NA ZSM 355/2010 [PT] FGZC 4277 F Makira 40.3 15.2 16.3 5.5 3.8 4.1 2.4 3.9 24.6 11.8 66.5 30.0 21.2 21.2 NA NA ZSM 5050/2005 [PT] ZCMV 2125 F Nosy Mangabe 42.2 15.4 16.7 6.0 4.0 4.2 2.7 3.8 24.4 11.9 69.4 30.6 21.0 21.7 NA NA M. georgei sp. nov. (Ca35/Ca36) ZSM 455/2005 [HT] ZCMV 806 M Toamasina 30.7 11.9 12.4 4.9 4.7 3.2 1.9 3.5 17.4 8.0 46.2 20.6 14.1 13.7 4.0 3.3 ZSM 454/2005 ZCMV 803 M Maroantsetra 29.0 10.9 12.0 4.6 3.7 3.3 1.8 3.4 17.4 8.6 46.9 20.3 13.9 13.8 4.0 2.4 ZSM 456/2005 [PT] ZCMV 807 M Toamasina 28.4 10.5 11.9 4.4 4.2 2.9 1.8 3.5 16.3 8.4 46.3 20.4 13.8 13.5 4.6 3.3 M. jahnarum sp. nov. (Ca27) ZSM 423/2006 [HT] ZCMV 3390 M Nosy Boraha 30.3 11.1 12.6 4.7 3.3 3.1 1.8 3.2 17.2 8.9 46.1 21.1 14.0 14.4 4.8 3.0

Distribution.— Endemic to low-elevations of Northern Central East and North East ( Fig. 7 ). This species is known from Ambato, Ambinanifaho, Ambodirafia Tokana, Ambodiriana, Ambodivohangy (Makira), Ampasimazava, Andranofotsy (type locality), Andrantambe, Antanambe, Antsahanoro, Befanjana, Belambo, various sites within Marojejy National Park, Masoala, Nosy Mangabe, and the Sambava region.

Elevation range: 12–1326 m a.s.l.

Etymology.—We dedicate this species to Barry Ferguson, an outspoken worker on environmental justice for Madagascar, in acknowledgement of his support of the first author’s work on Madagascar’s herpetofauna.

Figures

FIGURE 5. Maximum-Likelihood tree based on a partitioned analysis of 12,818 nuclear-encoded markers obtained via the FrogCap strategy, calculated with IQ-tree, for 58 representative individuals of species-level lineages in the subgenus Mantidactylus (Brygoomantis). Note that three species are missing from this analysis (M. bletzae sp. nov., M. marintsoai sp. nov., and M. riparius sp. nov.) and the identity of the two samples of M. katae sp. nov. in this tree is uncertain. For those lineages that previously (Perl et al. 2014; Vieites et al. 2009) had candidate species numbers assigned, these are reported in parenthesis after the name used in the classification proposed herein. All branches were fully supported by SH-like approximate likelihood ratio tests with 1000 pseudoreplicates (100% support, symbolized by black dots at nodes).The tree was rooted with Mantidactylus grandidieri (subgenus Mantidactylus) as outgroup (removed from graphical representation for better visualization of ingroup relationships), with the inclusion of M. melanopleura (subgenus Chonomantis) as hierarchical outgroup. Red arrows in the M. curtus clade indicate the two reticulation events detected by a Phylonetworks analysis performed separately for this clade (note that the topology recovered by this analysis in the Phylonetworks analysis differs in the position of M. bourgati; see original results of the Phylonetworks analysis in Zenodo repository, DOI 10.5281/zenodo.668741

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 48. Preserved holotype specimens of newly named species in the Mantidactylus fergusoni clade. Scale bars equal 5 mm.

FIGURE 49. Mantidactylus fergusoni sp. nov. in life, in dorsolateral, dorsal, and ventral view. (a,b) Adult male (holotype ZSM 126/2002 = FGMV 2001.1389) from Andranofotsy. (c,d) Adult female (ZSM 124/2002 = FGMV 2001.1434) from Andranofotsy. (e,f,g) Female specimen (ZCMV 15063) from a large stream near Camp 1 ‘Mantella’, Marojejy, photographed in 2016.

FIGURE 50. Audiospectrogram and corresponding oscillogram of three advertisement calls of Mantidactylus fergusoni, recorded on 21 December 2001 at Andranofotsy (25.4°C air temperature). Recording bandpass-filtered at 500–8000 Hz.