Boophis andrangoloaka ( Ahl, 1928 )

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 : 12-16

Boophis andrangoloaka ( Ahl, 1928) - bona species

( Fig. 4 , Appendix 9)

Remark. This species has been referred to as Boophis sp. aff. rhodoscelis "Ambohitantely" in Glaw & Vences (2007:151–152) and as Boophis sp. 34 in Vieites et al. (2009).

Identity of the northern populations of Boophis rhodoscelis and resurrection of Boophis andrangoloaka . The identity of B. rhodoscelis has long remained uncertain because of the limited natural history data available on this species. Glaw & Vences (1997b) provided the first bioacoustic data based on one adult male specimen from Ambohitantely, at the western border of the Northern Central East region, which showed morphological similarities to the types of B. rhodoscelis . Since this time, evidence has accumulated in several respects indicating that more than one species may be included in Boophis rhodoscelis sensu lato. First, a second male specimen was collected at Ambohitantely which is similar morphologically and bioacoustically to the previously collected specimen. Second, several morphologically similar specimens were collected near Ranomafana in the southern central east (Andranoroa river near Ranomafanakely; 21° 14.872' S, 47° 22.580' E; 1138 m a.s.l., collected on 29 January 2004 by M. Vences and I. De la Riva). This locality is in the same general region as the type locality of Rhacophorus rhodoscelis Boulenger, 1882 ("East Betsileo"), and thus this population is best considered to represent typical B. rhodoscelis . These new specimens, however, differ by chromatic and morphological details, a moderate genetic differentiation, and differences in advertisement calls, from those collected at Ambohitantely (see Diagnosis, Vocalizations, and Comparative call data below). We conclude that these differences are best reflected by considering specimens from the two populations as distinct species, and as a classificatory consequence we propose to apply the name Boophis rhodoscelis to the animals from Ranomafana, and to revalidate the name Boophis andrangoloaka for the specimens from Ambohitantely.

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 , especially B. rhodoscelis . Species group assignment of B. rhodoscelis has long been controversial, and is therefore not straightforward for B. andrangoloaka based on morphology alone. Its morphological characters are congruent with species of the B. majori species group: small size (male SVL 28–30 mm); single subgular vocal sac; presence of vomerine teeth; smooth dorsal skin without folds, spines or tubercles; absence of distinct heel flaps or spines; presence of webbing between fingers; nontransparent ventral skin; brownish dorsal ground colour without green elements; occurrence of red colour on the hidden parts of the thighs and on the webbing of the feet. Molecular data, however, clearly place B. androngoloaka as well as B. rhodoscelis in the B. microtympanum group (see Glaw & Vences 2006; Vieites et al. 2009), and in this group, B. andrangoloaka is distinguished from the other included species (except B. rhodoscelis ) by its smaller size, brownish dorsal colour without distinct dorsal markings (vs. green or brown with distinct rounded markings or reticulations), and presence of red colour on hidden parts of thighs and webbing of the feet (vs. absence); furthermore, from B. microtympanum and B. laurenti it differs by having a brownish (vs. green) iris and strongly different advertisement calls; and from B. williamsi , by absence of orange markings on the dorsum, and tympanic region colour darker than flanks and dorsum. Boophis andrangoloaka also shows similarities to some species in the B. goudoti group (see Glaw & Vences 1997b) but can be distinguished from all species in the group by presence of red colour on the hidden parts of thighs and webbing. This latter chromatic character is shared with B. rhodoscelis and is also found in several species of the B. majori group; this probably led Blommers-Schlösser (1979) to group B. rhodoscelis with species today included in the B. majori group. However, all species in the B. majori group have advertisement calls that strongly differ from those of B. andrangoloaka (and of B. rhodoscelis ), and they furthermore can be diagnosed by mostly lacking a tympanic region of distinctly darker colouration than the flanks and dorsum, and by lacking a distinct dark marbling on the throat. Boophis andrangoloaka is most similar to B. rhodoscelis but differs by (1) a moderate genetic divergence (see below), (2) a longer and slower call (note duration 178–198 vs. 56–100 ms; interval duration 208–265 ms vs. 93–152 ms; see below), (3) on average, a larger size (male SVL 28–30 mm vs. 25–28 mm), (4) a less contrasted ventral colour pattern with a more weakly defined light frenal stripe and a more weakly defined dark tympanic region, (5) a less contrasted ventral marbling, and (6) a slightly curved (vs. straight) supratympanic fold.

Redescription of the lectotype. ZMB 30510 (Appendix 9), adult female (designated by Glaw & Vences 1997b) , SVL 37.4 mm. Body moderately slender; head slightly longer than wide, approximately as wide as body; snout rounded in dorsal and lateral view, nostrils directed laterally, slightly nearer to eye than to tip of snout; canthus rostralis rounded in cross section, straight in dorsal view; loreal region slightly concave; tympanum distinct, round; TD 54% of ED; supratympanic fold distinct; vomerine odontophores distinct, small, forming two elongated patches, positioned posteromedial to choanae; choanae medium-sized, rounded. Tongue bifid posteriorly, free behind. Arms slender, subarticular tubercles single, round; metacarpal tubercles not recognizable; fingers scarcely webbed, with lateral dermal fringes; webbing formula 1(1.5), 2i(1.), 2e(1), 3i(2), 3e(1.5), 4(1.25); relative length of fingers 1<2<4<3 (finger 2 distinctly shorter than finger 4); finger discs enlarged. Hindlimbs slender; tibiotarsal articulation reaching the eye when hindlimb is adpressed along body; lateral metatarsalia separated by webbing; inner metatarsal tubercle small, distinct, elongated; no outer metatarsal tubercle; toes moderately webbed; webbing formula 1(0.25), 2i(1), 2e(0.5), 3i(1.25), 3e(1), 4i(1.5), 4e(1.5), 5(0.5); relative length of toes 1<2<5=3<4; toe discs enlarged. Skin smooth on dorsal surfaces, slightly granular on throat, coarsely granular on chest, belly and ventral surfaces of thighs.

Measurements (in mm): SVL 37.4, HW 12.5, HL 13.0, ED 4.6, END 2.5, NSD 2.7, NND 3.7, TD 2.5, TL 17.8, HAL 11.4, FOL 17.2, FOTL 28.0.

In preservative, ground colour of upper and lower surfaces of head, dorsum, and limbs beige, with small brown flecks and irregular markings on dorsum, flanks, lips, tympanic region, and limbs, which have a barred pattern; a cream labial stripe extending below tympanic region to the level of insertion of hind limb. Ventral parts greyish beige with brown markings on throat and chest. There are no data on colour in life of the lectotype.

New material. ZSM 5190 /2005 ( FGZC 2139 ), adult male (call voucher), from Ambohitantely Special Reserve , large swamp near administration buildings of the reserve, 18°11.967'S, 47.16.853'E, 1580 m a.s.l., central Madagascar, collected on 18 January 2005 by L. du Preez and M. Vences . ZFMK 60134 , adult male (call voucher), collected between the road RN4 and Ambohitantely Special Reserve , on 8 April 1995 by F. Glaw and D. Vallan .

Variation. Morphometric variation is given in Appendix 1. The male specimen from Ambohitantely, ZSM 5190 /2005 ( Fig. 4 ), is overall quite similar to ZFMK 60134 and the lectotype, but in preservative it exhibits a marked dark stripe from temporal region to snout, outlined above with a cream stripe along the supratympanic fold, the upper eyelid, and the canthus rostralis, ending at the tip of the snout. The foot webbing, upper surfaces of toes, internal surfaces of tarsi, posterior surfaces of shank and anterior and posterior surfaces of thighs are reddish purple. Calling specimens were not observed in detail during call emission but as far as recognizable upon capture had a single subgular vocal sac .

Natural history. In 2005, two to three males were heard calling late at night (no calls were heard before 22:00 h; see also Vences et al. 2006) when large and noisy choruses of Heterixalus rutenbergi and H. betsileo had largely fallen silent. The single collected specimen was sitting ca. 1 m high in the vegetation, next to some isolated trees, in a large exposed swampy area formed by a slow moving stream. Distance to the next patch of closed forest was 100– 200 m. Calls were emitted after intervals of some minutes. A further specimen had been collected in 1995 in the same general area under similar conditions, calling at 1.5 m height in the vegetation ( Glaw & Vences 1997b).

Vocalization. Calls of Boophis andrangoloaka are arranged in long series of notes emitted in regular intervals. A call series recorded on 18 January 2005 at Ambohitantely had a duration of 17.65 seconds and contained 43 notes. Notes are distinctly pulsed and show irregular amplitude modulation, with lowest energy in the middle of the note. Distinct frequency bands are recognisable in the spectrogram ( Fig. 5A ). Numerical call parameters are as follows: note duration, 178–198 ms (189 ± 7; n = 28); inter-note intervals, 208–265 ms (229 ± 18; n = 28); note repetition rate, 2.4 notes/second; 54–61 pulses/note; pulse repetition rate, 320 pulses/ second; dominant frequency range 1600–3200 Hz, maximum call energy at 2470–2730 Hz ( Vences et al. 2006, CD 1, track 56). These data largely coincide with those of another specimen recorded at Ambohitantely, as reported by Glaw & Vences (1997b), as Boophis cf. rhodoscelis ).

Comparative call data. As first reported by Vences et al. (2006), male specimens of Boophis rhodoscelis were observed in 2005 calling at night from low positions (perch heights below 1.0 m) within dense vegetation in a partly degraded forest bordering an exposed swampy area at the edge of Ranomafana National Park (locally known as Ranomafanakely), formed by a slow-moving stream. The call is of very low intensity which increases towards the end, and calling males are therefore difficult to find. The call of B. rhodoscelis consists of a long series of soft pulsatile notes repeated at regular intervals. Clearly separated pulses within notes are not recognizable. A note series recorded on 28 January 2004 at Ranomafanakely had a total length of 22.6 seconds ( Fig. 5B ). Numerical call parameters are as follows: note duration, 56–100 ms (80 ± 13; n = 24); inter-note intervals, 93–152 ms (119 ± 17; n = 25); note repetition rate, 4.6–5.0 notes/second; dominant frequency range 2000–3400 Hz, maximum call energy at 2490–3060 Hz ( Vences et al. 2006, CD 1, track 55).

Additional synonyms. The type locality of B. andrangoloaka is Andrangoloaka in the Northern Central East of Madagascar. Although this site is not in the immediate vicinity of Ambohitantely, it is in an area that has biogeographic links with Ambohitantely (e.g., haplotypes of the lizard Phelsuma lineata from Ambohitantely also occur in Antananarivo and in Fierenana, two localities not very far from Andrangoloaka, see Boumans et al. 2007). Biogeographically it would thus be possible that the same species occurs in Ambohitantely and Andrangoloaka, which further supports our decision to propose the resurrection of the name Boophis andrangoloaka and apply it to the Ambohitantely population.

One additional taxon is currently considered as junior synonym of Boophis rhodoscelis and needs to be discussed (see Glaw & Vences 1997b): Rhacophorus brevirostris Ahl, 1928 (type locality: northwestern Madagascar without further information). The two nomina, andrangoloaka and brevirostris , were described by E. Ahl in the same publication ( Ahl 1928); the types of these two nomina were collected by J. M. Hildebrandt, and it is obvious that the locality data of parts of the Hildebrandt collection are dubious (see discussion in Vences & Glaw 2001, 2004). This is also true for the type locality of Rhacophorus brevirostris because no species similar to Boophis rhodoscelis is known from northwestern Madagascar. ZMB 30518, the holotype of Rhacophorus brevirostris Ahl, 1928 (Appendix 9), is quite similar to the B. andrangoloaka lectotype in general colouration; it has some brown, irregular, moderately large spots on flanks. In the absence of reliable locality data and considering this general similarity of the types, we propose to consider Rhacophorus brevirostris as a junior synonym of Boophis andrangoloaka .

Molecular relationships. According to Glaw & Vences (2006), B. andrangoloaka and B. rhodoscelis belong in the B. microtympanum group. This group is here not resolved as monophyletic lineage, probably due to insufficient informative sites in the short DNA fragment analysed. However, B. andrangoloaka is clearly placed sister to B. rhodoscelis with high support (97% BS, BPP significant; Fig. 1 ). The molecular differentiation among these two species is low (2.4%). Boophis andrangoloaka and B. rhodoscelis are both highly divergent from other species of the B. microtympanum group (6.2–7.5%) and the B. majori group (8.2– 12.6%). The analysis further provides evidence for a significant and complex differentiation among mitochondrial lineages assigned to B. laurenti and B. microtympanum (up to 2.5% divergence), indicating that this complex of species is also in need of taxonomic revision (see also Glaw & Vences 2007).

Distribution. Under the current definition, two sites are reliably known for Boophis andrangoloaka , its type locality Andrangoloaka and Ambohitantely Special Reserve (Appendix 10).

Figures

FIGURE 1. Maximum parsimony 16S rRNA phylogram for species in the Boophis majori and B. microtympanum groups. From 480 total characters, 336 were constant and 129 parsimony informative. MP searches retained 39 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 4. Dorsolateral view (A) and ventral view (B) of male of Boophis andrangoloaka (FGZC 2139) from Ambohitantely; (C) dorsolateral view of Boophis andrangoloaka (ZFMK 60134) from Ambohitantely; dorsolateral view (D) and ventral view (E) of a dark coloured specimen of Boophis rhodoscelis from Ranomafanakely; (F) dorsolateral view of a light coloured specimen of Boophis rhodoscelis from Ranomafanakely.

FIGURE 5. Spectrograms and waveforms of advertisement calls of: (A) Boophis andrangoloaka from Ambohitantely Special Reserve (recorded on 18 January 2005, air temperature app. 18°C); (B) Boophis rhodoscelis from Ranomafanakely, Ranomafana National Park (recorded on 28 January 2004, air temperature app. 21°C).