Boophis obscurus ( Boettger, 1913 )

Glaw, Frank, Köhler, Jörn, Riva, Ignacio De La, Vieites, David R. & Vences, Miguel, 2010, Integrative taxonomy of Malagasy treefrogs: combination of molecular genetics, bioacoustics and comparative morphology reveals twelve additional species of Boophis 2383, Zootaxa 2383 (1), pp. 1-82 : 31-35

Boophis obscurus ( Boettger, 1913) - bona species

( Fig. 14 , Appendix 9)

Remark. This species has been referred to as Boophis sp. aff. goudoti by Glaw & Vences (2007:164–165) and as Boophis sp. 13 in Vieites et al. (2009).

Resurrection of Boophis obscurus . Boophis Goudotii Tschudi, 1838 was the first frog species described from Madagascar. With just four lines, its original description written in Latin is very short and its type locality is only given imprecisely as " Madagascar " ( Tschudi 1838). However, this description is in agreement with the widespread species from central Madagascar that is traditionally considered as Boophis goudoti and there is no character that would indicate its attribution to the form from the Ranomafana region. We therefore follow the definition of B. goudoti as used by Glaw & Vences (2007) whereas the morphologically similar species tentatively named Boophis sp. aff. goudoti ( Glaw & Vences 2007) is in need of a scientific name. Numerous names are currently considered as synonyms of Boophis goudoti . The oldest available name is Polypedates Goudotii D. Bibr. var. variolosa , described by Steindachner (1864). The synonymy and Malagasy origin of this taxon is somewhat doubtful (see Guibé 1978: 72). According to the original description a row of skin tubercles is present on the integument located ventral sides of the metacarpal and metatarsal bones contradicting an attribution to the B. goudoti species group. The next oldest synonym, Rhacophorus obscurus Boettger, 1913 , was described based on four specimens from Fianarantsoa. The male lectotype of this taxon (SMF 6763) shows distinct spines on the back and legs as is typical for Boophis sp. aff. goudoti and the description of Boettger (1913) agrees with this form as well. We therefore resurrect Boophis obscurus ( Boettger, 1913) as valid species name for the form previously considered as candidate species Boophis sp. aff. goudoti .

Diagnosis. Assigned to the genus Boophis based on the presence of an intercalary element between ultimate and penultimate phalanges of fingers and toes (verified by external examination), presence of nuptial pads and absence of femoral glands in males, absence of gular glands in males, enlarged terminal discs of fingers and toes, lateral metatarsalia separated by webbing, absence of outer metatarsal tubercle, molecular phylogenetic relationships (see Vieites et al. 2009 for a complete molecular analysis of Boophis ), and overall similarity to other Boophis species. Assigned to the Boophis goudoti group based on the following combination of characters: moderate to large size (male SVL 42–82 mm); brownish dorsal ground colour; non-transparent ventral skin; single subgular vocal sac; presence of vomerine teeth; presence of webbing between fingers; presence of a sharp canthus rostralis; and molecular phylogenetic relationships (see Vieites et al. 2009). Boophis obscurus differs distinctly from all described species in the B. goudoti group by its moderate to strong genetic differentiation (see below). It furthermore differs from B. boehmei , B. rufioculis , B. burgeri , B. reticulatus , and B. axelmeyeri by its larger size (SVL of males 42.4–81.9 mm vs. 27–43 mm) and iris colouration (absence of red colour in the outer iris area as is typical for B. axelmeyeri , B. boehmei , and B. rufioculis ; absence of a pattern of dark stripes typical for B. reticulatus ; no distinct blue iris periphery as in B. boehmei , B. burgeri , and B. rufioculis ). It differs from B. madagascariensis , B. roseipalmatus , B. entingae , B. brachychir , B. boehmei , B. rufioculis , B. burgeri , B. reticulatus , and B. axelmeyeri by the absence of distinct dermal flaps or tubercles on heels. It differs from B. spinophis by the absence of distinct dermal tubercles along the lateral parts of the tarsus and around the elbow. It differs from Boophis goudoti by a dorsal colouration that usually includes orange-brown spots (hitherto not seen in B. goudoti ) and a ventral colouration without yellow colour (yellow ventral colour being typical for B. goudoti ). The new species is superficially also similar to B. periegetes , but breeding males can easily be distinguished from that species by the different types of skin rugosities (small keratinised spicules rather than larger warts), and by their advertisement calls (irregular pulsed croaking notes vs. whistling notes in B. periegetes ; see below).

Redescription (based on ZMA 20220). Adult male, SVL 63.2 mm. Body moderately robust; head longer than wide, slightly wider than body; snout long, rounded in dorsal view and lateral view, nostrils directed laterally, nearer to eye than to tip of snout; canthus rostralis sharp in cross section, straight in dorsal view, almost reaching the tip of snout; loreal region concave; tympanum large, distinct, rounded, TD 83% of ED; supratympanic fold thick, clearly distinct; vomerine odontophores distinct, well separated in two elongated patches, positioned posteromedial to choanae; choanae large, elongated. Tongue posteriorly bifid, free. Arms moderately robust; subarticular tubercles single, round; inner palmar tubercle poorly distinct, elongated, in close contact with nuptial pad; nuptial pad creamy yellow, covering dorsal and posterior surfaces of first finger and dorsal surface of basis of second finger; outer palmar tubercle indistinct; fingers scarcely webbed and with lateral dermal fringes; webbing formula 1(1.5), 2i(1.5), 2e(1), 3i(2.25), 3e(1.75), 4(1); relative length of fingers 1<2<4<3 (finger 2 distinctly shorter than finger 4); finger discs enlarged. Hind limbs moderately robust; tibiotarsal articulation barely reaching tip of snout when hind limb is adpressed along body; lateral metatarsalia separated by webbing; inner metatarsal tubercle distinct, elongated; no outer metatarsal tubercle; toes moderately webbed; webbing formula 1(0), 2i(1), 2e(0), 3i(1), 3e(0.5), 4i(1.5), 4e(1.5), 5(0.25); relative length of toes 1<2<3=5<4; toe discs enlarged. Skin texture on dorsal surfaces smooth, but covered by small warts with keratinized black spicules, more abundant on the two posterior thirds of dorsum and upper surfaces of hind limbs. Ventral skin finely granular on throat and chest, coarsely granular on belly and ventral surface of thighs; keratinized spicules like those of dorsum (but not on the top of a wart) on venter and periphery of gular region, below the jaws.

Measurements (in mm): SVL 63.2, HW 21.3, HL 23.0, ED 6.8, END 4.6, NSD 5.4, NND 7.0, TD 5.7, TL 35.1, HAL 19.8, FOL 31.2, FOTL 49.5.

After almost four years in preservative, ground colour of upper surface of head, dorsum and legs brown with reddish brown, irregular blotches; warts grey with tiny black spicules; flanks brown with irregular cream blotches; an irregular, unconnected cream stripe along upper lip. Legs with dark brown bars. Ventral surfaces beige with irregular, diffuse brown blotches. Colouration of the holotype in life unknown.

New material. ZMA 20219 ( ZCMV 347 ) , ZMA 20220 ( ZCMV 348 ), and UADBA 24309 ( ZCMV 349 ), three adult males, from Ranomafana National Park , rice field close to Andranoroa river, near Ranomafanakely, 21°14.872' S, 47°22.580' E, 1138 m a.s.l., southeastern Madagascar, collected on 29 January 2004 by I. De la Riva and M. Vences ; UADBA ( ZCMV 5748 , 5750 , 5759 ), sex unknown, from Isalo National Park , collected on 15–16 February 2007 by M. Vences and J. Glos ; ZMA 19452 ( FG / MV 2002–1403 ), male, from the Maharira area , Ranomafana National Park, collected by E. Rajeriarison and T. Rajoafiarison in January 2003 ; ZSM 740 /2001 ( FGMV 2001.540 ), from Andohariana plateau (Andringitra), 22°10'49'' S, 46°54'01'' E, 2114 m, collected on 13–14 March 2001 by L. Raharivololoniaina, D. Rakotomalala, M. Vences and D . R. Vieites ; ZSM 2293 /2007 ( ZCMV 5774 ) and ZSM 2294 /2007 ( ZCMV 5781 ), two males, from Isalo , Cascade des Nymphes, collected on 16 February 2007 by M. Vences and J. Glos ; ZSM 2292 /2007 ( ZCMV 5903 ), female, from Ambatovaky (road from Vohiparara to National Road RN 7 Antananarivo-Fianarantsoa, at ca. 30 km direction from Vohiparara), collected on 1 March 2007 by M. Vences and P. Bora .

Variation. Morphometric variation is given in Appendix 4. No remarkable variation in colour pattern exists among the males from Ranomafana; two males from Isalo ( ZSM 2293–2294 /2007) also conform the general pattern of the holotype but are distinctly smaller. A male from Andringitra ( ZSM 740 /2001) is the largest specimen (81.9 mm SVL); it has poorly marked dorsal spicules, and marked brownish orange bars on limbs. The only female in our sample ( ZSM 2292 /2007) lacks spicules; it has a diffuse dorsal pattern of intermingled dark brown and brownish orange blotches, and limbs markedly barred. In life, paratypes had a dark reddish-brown dorsum, flanks yellowish, progressively becoming bluish downwards, with brown irregular blotches, and lower surfaces creamy white with brown markings. The iris was pale orange. In males, during call emission, a single subgular vocal sac was visible which however became only weakly extended .

Natural history. In the highlands of the Ranomafana area, specimens are regularly observed on the ground or on low perch heights along streams in more or less exposed areas next to rainforest. A chorus of calling specimens (reported as Boophis sp. aff. periegetes in Vences et al. 2006) was observed at night in slow-moving channels connecting rice fields close to rainforest. The specimens were sitting in close proximity of each other, at a rather exposed site at the borders of the canal or in the shallow water. At Andringitra, one large male was collected on the Andohariana plateau, above the tree line, next to a mountain stream during the day on the ground. At Isalo, males of the dwarf form here assigned to B. obscurus were observed at night calling from the ground or perched on branches and rocks in steep areas next to streams, and in areas were small amounts of water where constantly flowing and dripping and large boulders were creating small caves. Specimens were not in direct proximity but often at small distances of only a few meters from each other. Calls were also occasionally heard during the day.

Vocalization. Calls of B. obscurus are very variable and might be classified into several different call types like done for other species in the group, especially B. madagascariensis ( Narins et al. 2000) . However, our data do not allow for a proper classification, as calling motivation and the social context of our recordings remain largely unknown. We here describe some different types of vocalizations, being aware that several additional and/or intermediate call types may occur in this new species. What is here termed call type 1 might possibly represent some kind of advertisement call, as it is emitted with high energy and shows a relatively regular structure. It is a pulsed note with distinct temporal modulation of pulses. Type 2 is somehow similar, but is usually softer and shows more evenly distributed pulses within notes. Type 3 refers to various single clicks and shorter pulsed notes. Emission of these different note types does not seem to follow a particular pattern, as they rather appear randomly mixed and combined. Numerical call parameters for the different call types are as follows ( Vences et al. 2006, CD 1, track 60): Call type 1 ( Fig. 15A ): note duration, 137–238 ms (187 ± 40; n = 5); notes repeated at irregular intervals; 8 pulses/note (n = 5), intervals between pulses, 4–41 ms (16 ± 11; n = 27); duration of inter-pulse intervals decreasing towards end of note; pulse repetition rate variable, approximately 20–70 pulses/second; dominant frequency range 400–3000 Hz, maximum call energy at 550–810 Hz. Call type 2: note duration, 206–360 ms (264 ± 33; n = 15), notes repeated at irregular intervals; pulses/note, 8–16 (11.6 ± 2.4; n = 12); intervals between pulses, 9–25 ms (16 ± 5; n = 25); pulse repetition rate approximately 32–36 pulses/second; dominant frequency range 400–1800 Hz, maximum call energy at 420–760 Hz. Call type 3 (no detailed analysis possible): various short notes, composed of 1–5 pulses, repeated at irregular intervals; note duration, 14–112 ms (n = 9); dominant frequency range similar to types 1 and 2.

Comparative call data. The call of B. periegetes consists of a long unpulsed whistle, usually emitted in groups of 3–4 notes ( Fig. 15B ). An increase in note duration is evident towards the end of such a series. Frequency is generally distributed in a very narrow band, but modulation is recognizable with a slight upward sweep at the beginning and a distinct drop in frequency at the end of the note. Numerical call parameters are as follows: note duration, 225–637 ms (435 ± 147; n = 8); inter-note interval (within series), 320–967 ms (627 ± 243; n = 5); note repetition rate, approximately 0.6–1.8 notes/second; dominant frequency range 1100–1700 Hz, maximum call energy at 1320–1510 Hz ( Vences et al. 2006, CD 1, track 59).

Molecular relationships. The molecular phylogeny places the sequences assigned to this species in a clade together with B. goudoti . Although this clade is only poorly supported (BS 65%, BPP not significant), the close relationships between these two species are beyond doubt based on analyses of further mitochondrial gene sequences (work in progress by K. C. Wollenberg). Also, it seems clear that the sequences assigned to each species (except one; see below) do each form a clade, despite the lack of such a topology in our tree ( Fig. 7 ). Sequences assigned to B. goudoti and B. obscurus have divergences of 2.1–3.9%, depending on the length of the included fragment (in some specimens, fragments had many missing data in the generally quite conserved first section and sequence length for comparison was thus shorter and divergence values higher). One specimen morphologically clearly belonging to B. obscurus has a sequence identical to a specimen of B. goudoti from Antoetra, indicating either incomplete lineage sorting or, more probable, recent hybridization with mitochondrial introgression, as also known from other closely related mantellid species such as Mantella aurantiaca and M. crocea , and Mantella baroni and M. cowani ( Chiari et al. 2004; Rabemananjara et al. 2007).

Distribution. At present, specimens assignable to Boophis obscurus are known from different sites in the Vohiparara region, in or near Ranomafana National Park: Andranoroa river, Ranomafanakely, and Ambatovaky (Appendix 10). Specimens that are substantially different in size are known from Andringitra National Park and Isalo National Park. An individual from Ambohimitombo (ZFMK 28862) shows the typical colour pattern of B. obscurus and may belong to this species as well, but this identification is in need of confirmation.

Figures

FIGURE 7. Maximum parsimony 16S rRNA phylogram of species of the Boophis goudoti group. From 510 total characters, 340 were constant and 130 parsimony informative. MP searches retained 3681 trees of which a strict consensus is shown. Consensus support values higher than 50, from 2000 bootstrap replicates, are shown; an asterisk indicates Bayesian posterior probabilities equal or higher than 95%. Species newly described or resurrected herein are in bold.

FIGURE 14. Male Boophis obscurus (UADBA uncatalogued) from Ranomafanakely.

FIGURE 15. Spectrograms and waveforms of calls: (A) call type 1 of Boophis obscurus from near Vohiparara, Ranomafana National Park (recorded on 29 January 2004, air temperature app. 20.5°C); (B) advertisement call of Boophis periegetes from Andohahela National Park (recorded on 27 January 2005, air temperature app. 18°C)