Rhombophryne guentherpetersi ( Guibé, 1974 ), Guibe, 1974

Scherz, Mark D., Hawlitschek, Oliver, Andreone, Franco, Rakotoarison, Andolalao, Vences, Miguel & Glaw, Frank, 2017, A review of the taxonomy and osteology of the Rhombophryne serratopalpebrosa species group (Anura: Microhylidae) from Madagascar, with comments on the value of volume rendering of micro-CT data to taxonomists, Zootaxa 4273 (3), pp. 301-340 : 307-312

Rhombophryne guentherpetersi ( Guibé, 1974)

Common name: Tsaratanana saw-browed diamond frog (modified from Frank & Ramus 1995) ( Figs 4–7 , S1–S2)

Mantipus guentherpetersi Guibé, 1974: 1181 –1182

Plethodontohyla guentherpetersi — Blommers-Schlösser & Blanc, 1991: 56 –57. First depicted in life under this name in Stuart et al. (2008).

Rhombophryne guentherpetersi — Glaw & Vences, 2007: 118. The photo provided on page 119 of this book is misattributed and depicts an undescribed species (Scherz et al. unpubl. data).

Holotype. MNHN 1953.165, an adult female specimen captured by an unknown collector on an unknown date on the Tsaratanana Massif at 2600 m a.s.l. ( Figs 4 , 5 , S2)

Paratypes. MNHN 1953.165A and MNHN 1953.165B, a juvenile and adult female with the same collection data as the holotype. MNHN 1973.592 and MNHN 1973.593 , a subadult female and juvenile collected by Charles P. Blanc in 1966 on Mission ORSTOM from the same location as the holotype .

Referred specimens. ZSM 606/2014 (DRV 6220), a female, ZSM 607/2014 (DRV 6223), a male, and ZSM 608/2014 (DRV 6231), a female (Fig. S1), three adult specimens collected by D. Vieites, M. Vences, R.D.

Randrianiaina, F.M. Ratsoavina, S. Rasamison, A. Rakotoarison, E. Rajeriarison, F. Randrianasolo, F. Randrianasolo and T. Rajoafiarison, ZSM 606 /2014 and 607/2014 on the 16th of June 2010 at Andranomadio (camp 4), Tsaratanana, 14.0801°S, 48.9854°E, 2503 m a . s.l.; ZSM 608 /2014 on the 18th of June 2010 at a site on the Tsaratanana mountain 14.0665°S, 48.9832°E, 2732 m a .s.l. A further three specimens from Andranomadio (with same collecting data as ZSM specimens from this site) were deposited in the UADBA collection: UADBA-A 60775 (DRV 6210) and UADBA-A 60776 (ZCMV 12401), adults; UADBA-A 60782 (ZCMV 12435), subadult.

Diagnosis and comparisons. Rhombophryne guentherpetersi is a member of the genus Rhombophryne on the basis of molecular phylogenetic affinities ( Fig. 3 ) and the possession of a clavicle combined with the absence of T- or Y-shaped terminal phalanges (vs. either absence of a clavicle or possession of a clavicle combined with T- or Yshaped terminal phalanges in the morphologically similar Plethodontohyla Boulenger, 1882 ). Within the genus Rhombophryne , it is assigned to the R. serratopalpebrosa species group on the basis of possessing superciliary spines and of molecular phylogenetic affinities ( Fig. 3 , Table 1).

Rhombophryne guentherpetersi is distinguished from all other described congeners by the following unique suite of characters: adult SVL 27.3–35.7 mm; TDH/ED = 0.4 5–0.66; a weak supratympanic fold running from the rear corner of the eye to curve slightly over and behind the tympanum toward the axilla; two or three small superciliary spines; distinct, raised dorsolateral glands, and bulbous tibial glands. The pectoral girdle is distinctly narrower than that seen in its congeners (see Fig. 7 ; 8.2–9.4% of SVL). Furthermore, R. guentherpetersi is separated from all other Rhombophryne species except R. ornata and R. serratopalpebrosa by uncorrected pairwise distances of at least 4.4% in a segment of the 16S rRNA mitochondrial gene (see Table 1; no molecular data available for R. serratopalpebrosa )—for distinction from R. ornata , see below.

Rhombophryne guentherpetersi is distinguished from all Rhombophryne species except the R. serratopalpebrosa group by the possession of superciliary spines, and from all members of this group, and indeed all cophyline microhylids, by the possession of bulbous tibial glands. Genetically, R. guentherpetersi is very closely related to R. ornata —they are separated by just 2.4–3.4% in one fragment of the 16S gene (see Table 1), which is lower than our standard threshold for candidate species recognition ( Vieites et al. 2009). However, the two species are highly morphologically distinct, differing not just in the presence or absence of tibial glands, but also in the shorter relative hindlimb length of R. guentherpetersi (HIL/SVL 1.33–1.45 vs. 1.46–1.64), tibiotarsal articulation reaching the axilla or tympanum (vs. between the tympanum and the eye), absence (vs. presence) of red colouration in the inguinal region, partially ossified limb epiphyses and carpals (vs. unossified), and much narrower pectoral girdle (length of coracoid <10% of SVL vs.>12%; see Fig. 7 ). A differential diagnosis from all other cophyline microhylids is unnecessary because the tibial glands allow easy unambiguous distinction. These are noticeable, if not well developed, even in subadults.

Re-description of the holotype. ( Figs 4 , 5 ) An adult female specimen in moderately good state of preservation. Ventral incision and left lateral incision present.

Body robust. Head wider than long (HW/HL = 1.35). Pupils horizontally oval. Snout rounded in dorsal and lateral views. Canthus rostralis concave. Loreal region concave. Nostrils nearer to snout tip than to eye (END/NSD = 1.24), directed laterally, slightly protuberant. Tympanum distinct, TDH/ED = 0.47. Weak supratympanic fold, from middle rear of eye curving slightly over and behind tympanum toward the axilla. Two small superciliary spines above each eye. Vomerine teeth present, curved, not meeting at the midline.

Arms robust. Fingers without webbing; relative lengths 1<2<4<3, fourth finger distinctly longer than second; finger tips not expanded; fingers not reduced; nuptial pads absent; inner metacarpal tubercle present, outer metacarpal tubercle divided, faint; subarticular tubercles distinct, undivided. Hindlimbs short and thick; tibiotarsal articulation reaches the axilla; TIBL/SVL = 0.35. Strongly developed tibial glands cover almost the entirety of the dorsal tibia. Inner metatarsal tubercle present, enlarged, outer metatarsal tubercle absent. Toes unwebbed; relative lengths 1<2<5<3<4, fifth toe distinctly shorter than third. Toe tips not expanded.

Dorsal skin slightly granular except on the head, where it is slightly rougher, with a slightly raised ridge on the midline of the head. Dorsolateral folds absent. A porous glandular formation extends from the suprascapular region to the inguinal region on either side of the body. Ventral skin smooth.

Colouration of the holotype: ( Figs 4 , 5 ) Light reddish-brown above with irregular small dark speckling. Loreal and tympanic regions lighter than dorsal head, without speckling. Glandular formations on tibiae and dorsum darker brown, as are the anterior surfaces of head and above eyes. Flanks fading from dorsal colour to ventral colour. Venter uniformly tan to cream. Limbs coloured as the dorsum.

Variation. The type series is composed of two juveniles, one subadult, and one poorly preserved adult, in addition to the holotype. Our newly added material consists of three well-preserved adults, including the first male specimen. All specimens, including the juveniles, possess superciliary spines, but they are small and variable in number, and in poorly preserved specimens cannot be well distinguished (but can be distinguished in life; see Fig. 6 ). ZSM 606/2014 has three superciliary spines, whereas all other specimens have two. The paratype MNHN 1953.165B is darker than the rest of the type series and has much rougher skin (but is also particularly poorly preserved). All specimens, including the juveniles, have tibial glands, but these are less bulbous in the juveniles and subadult, becoming large only in the adults (confirming that all members of the type series are indeed conspecifics). The one male specimen is smaller than the adult females, but is in all other aspects highly similar in morphology (see Appendix 1). The tibiotarsal articulation reaches either the axilla or the tympanum. A prepollex is well developed in the one available male specimen, ZSM 607/2014. The species may have some degree of sexual size dimorphism, as the only male specimen is slightly smaller than all adult female specimens available (27.3 vs. 28.9–35.7 mm).

Colouration is relatively homogeneous, but shade and pattern differ somewhat ( Fig. 6 ). The newly collected specimens are much darker brown in colour than the type series, but generally have commonalities to their colour patterns: a pair of blackish oblong markings above the suprascapular region ( Fig. 6 ). These markings are present only in one member of the type series (MNHN 1973.592). The lateral body has several dark-brown flecks. These are present in all of the paratypes but not in the holotype. The venter is mottled dark and light brown in some specimens but is almost solid dark brown in others. A light brown interocular bar is sometimes present, anterior to which the snout is typically lighter brown than the dorsum. The dorsolateral glands can also be this light brown, or they can be continuous with the rest of the dorsum.

Remarks. The following inconsistencies exist between our re-description and the original description of this species by Guibé (1974): Superciliary spines are present; these were apparently overlooked in his description. Tibiotarsal articulation was given as reaching the eye. This could not be verified in any member of the type series except the poorly preserved paratype MNHN 1973.592, the vertebral column of which is inverted (i.e. convex instead of concave), possibly misleading tibiotarsal articulation. The holotype is 10 mm longer than described (34.6 mm vs. 25 mm). Guibé (1974, 1978) stated that the prepollex was developed in males, but the type series does not contain any males. Nevertheless, we have confirmed this observation with a newly collected male specimen (see Variation above).

Natural history. At Andranomadio, specimens were found during the day in high-altitude rainforest with rather open canopy (2503 m a.s.l.), burrowed several centimetres deep in the ground. Another individual (ZSM 608/2014) was collected above the treeline (2732 m a.s.l.), in an area of grassland with some scattered heath, hidden under a stone during the day.

Distribution and conservation status. Rhombophryne guentherpetersi is currently listed in the IUCN Red List as Endangered under criterion B1ab(iii) (IUCN SSC Amphibian Specialist Group 2016a), meaning an extent of occurrence of <5000 km 2 (B1), a severely fragmented habitat or known from Ẽ5 locations (a), and an observed, estimated, inferred, or projected on-going decline in the area, extent and/or quality of habitat (b(iii)). At present, R. guentherpetersi is known only from the Tsaratanana Massif. The exact collecting locality of the type specimens is not clear ( Guibé 1974), but three specimens were collected on a recent expedition to the Tsaratanana Massif (ZSM 606–607/2014 at 14.0801°S, 48.9854°E at 2503 m a.s.l; ZSM 608/2014 at 14.0665°S, 48.9832°E, 2732 m a.s.l.; Fig. 8 ). These two localities are well inside the protected area of Tsaratanana Strict Nature Reserve, to which only researchers and conservation workers are permitted access. Although it is possible that the species may occur in the forest corridor between Marojejy and Tsaratanana (COMATSA; see Rabearivony et al. 2015), which is pending official protected status, we consider this unlikely: we suspect that R. guentherpetersi is found only at high elevations, possibly near to and above the tree line, which in Tsaratanana is around 2550 m a.s.l. No part of the COMATSA corridor exceeds 2300 m a.s.l. The likely extent of occurrence of this species is therefore limited to an area of 36.4 km 2. Deforestation and habitat degradation pressure at such high altitude is minimal relative to the lower reaches of the forest, especially due to the strict conservation status of this forest. However, it is not free from threats: Climate change may be a significant factor for species living near the tops of mountains, as their niche space diminishes with rising temperatures. Fires in the high mountain grassland could swiftly eradicate the suitable open habitat and leave only forest habitat available. To balance (1) the small range of this species, (2) the highly protected status it enjoys, and (3) the threats that persist despite this protection, we propose to maintain a status of Endangered B1ab(iii) (IUCN 2012), but encourage further surveys within COMATSA and Tsaratanana Strict Nature Reserve in order to better understand the distribution and ecology of this species.

Figures

FIGURE 3. Majority-rule consensus tree of the Rhombophryne serratopalpebrosa species group and its sister clade, obtained by partitioned BI analysis, based on 2491 nucleotide characters of two mitochondrial and one nuclear gene (16 S, cox 1, sacs). Asterisks indicate Bayesian posterior probability values (* 0.95 – 0.98, ** 0.99 – 1.0; not shown if <0.95). Stumpffia psologlossa and other species of Rhombophryne were used as hierarchical outgroups and are here excluded from the figure as they are not the subject of this study. Members of the R. serratopalpebrosa species group are depicted in life, not to scale.

FIGURE 4. Photographs of the holotypes of the species treated in this manuscript, in dorsal (top row) and ventral (bottom row) views.

FIGURE 5. Comparative morphology of the heads, feet, and hands of members of the Rhombophryne serratopalpebrosa species group. All specimens are the holotypes of their respective species, except R. coronata, which is paratype ZSM 694 / 2001. Asterisks indicate mirrored images. Not to scale.

FIGURE 6. Rhombophryne guentherpetersi in life. (a – c) ZSM 607 / 2014 in (a) dorsolateral (with inset showing superciliary spines), (b) dorsal, and (c) ventral view; and (d, e) other specimens in dorsolateral view (assignment to field and collection numbers unknown).

FIGURE 7. Osteology of Rhombophryne guentherpetersi (MNHN 1953.165). Full skeleton in (a) dorsal, (b) ventral, and (c) lateral view; skull in (d) dorsal, (e) ventral, and (f) lateral view. Abbreviations: angspl = angulosplenial, col = columella, exoc = exoccipital, fpar = frontoparietal, max = maxilla, mmk = mentomeckelian, npl = neopalatine, pmx = premaxilla, povom = postchoanal vomer, proot = prootic, prvom = prechoanal vomer, prsph = parasphenoid, pter = pterygoid, qj = quadratojugal, smax = septomaxilla, spheth = sphenethmoid, sq = squamosal.

FIGURE 8. Map of the north of Madagascar showing the collection localities of specimens of the focal species of this paper, Rhombophryne guentherpetersi, R. regalis sp. nov., and R. diadema sp. nov. Basemap from www. vegmad. org. Hashing indicates protected areas; note that the full extent of Tsaratanana Strict Nature Reserve is not shown.