Boophis miadana, Glaw & Köhler & Riva & Vieites & Vences, 2010

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 : 45-47

Boophis miadana sp. nov.

( Fig. 22 , Appendix 9)

Remark. This species has been referred to as Boophis sp. aff. ankaratra "Andohahela slow" by Glaw & Vences (2007:172–173) and as Boophis sp. 19 in Vieites et al. (2009).

Holotype. ZSM 5107 /2005 ( FGZC 2388 ), adult male, from Andohahela, near campsite of the 2005 expedition of P. Bora, F. Glaw and M. Vences, 24°32.642'S, 46°42.847'E, 1548 m a.s.l., collected on 26 January 2005 by P. Bora, F. Glaw & M. Vences.

Paratype. ZSM 5108 /2005 ( FGZC 2389 ) , adult male, same collecting data as holotype .

Etymology. The specific name is used as a noun in apposition and is derived from the Malagasy word "miadana" meaning "slow", referring to the slow note repetition rate in advertisement calls of this species, especially in comparison to the syntopic B. haingana .

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), 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 albipunctatus group based on the following combination of characters: small size (male SVL 26–27 mm); absence of tubercles or flaps on heel and elbow; presence of webbing between fingers; indistinct canthus rostralis; dorsal colouration translucent green in life and whitish-yellow in preservative; absence of red ventral colour; ventral skin in life non-transparent; single subgular vocal sac; presence of vomerine teeth; molecular phylogenetic relationships; and high morphological similarity to B. ankaratra and B. schuboeae . The new species differs from all other species in the Boophis albipunctatus group by a moderate to strong genetic differentiation (see below) and by advertisement calls. Within the B. albipunctatus group, the new candidate species belongs to a clade of morphologically very similar species ( B. ankaratra , B. schuboeae , B. miadana , and B. haingana as described below) characterized by (1) the lack of well-defined brown markings on the iris, and (2) lack of a dense dorsal spotting with small and sharply defined white spots. Within this complex, B. miadana is characterized by the longest duration of notes and of inter-note intervals (see Figs. 24–25 and Comparisons section below).

Description of the holotype. Adult male, SVL 25.5 mm. Body moderately slender; head slightly longer than wide, wider than body; snout rounded in dorsal and lateral view, nostrils directed laterally, nearer to eye than to tip of snout; canthus rostralis rounded in cross section, slightly concave in dorsal view, loreal region slightly concave; tympanum distinct, round, TD 44% of ED; supratympanic fold barely distinct; vomerine odontophores distinct, well separated in two elongated patches, positioned posteromedial to choanae; choanae medium-sized, rounded. Tongue posteriorly bifid, free. Arms slender, subarticular tubercles single, round; metacarpal tubercles not recognizable; fingers moderately webbed and with lateral dermal fringes; webbing formula 1(1.5), 2i(1.5), 2e(1), 3i(2), 3e(1.5), 4(1); relative length of fingers 1<2<4<3 (finger 2 distinctly shorter than finger 4); finger discs enlarged. Hindlimbs slender; tibiotarsal articulation reaching the tip of snout when hind limb is adpressed along body; lateral metatarsalia separated by webbing; inner metatarsal tubercle small, distinct, elongated; no outer metatarsal tubercle; toes broadly webbed; webbing formula 1(0.5), 2i(0.75), 2e(0.25), 3i(1), 3e(0.25), 4i(1.25), 4e(1.5), 5(0.5); relative length of toes 1<2<3<5<4; toe discs enlarged. Skin smooth on dorsal surfaces, finely granular on throat and chest, coarsely granular on belly and ventral surfaces of thighs. Muscle from right thigh was removed for tissue sample.

Measurements (in mm): SVL 25.5, HW 8.9, HL 9.1, ED 3.4, END 1.7, NSD 2.6, NND 2.8, TD 1.5, TL 14.1, HAL 8.6, FOL 11.5, FOTL 18.7.

After almost three years in preservative, ground colour of upper surfaces of head, dorsum, and limbs uniformly creamy yellow; dark pigmentations around nostrils. Ventral surfaces uniformly creamy yellow.

In life, the holotype was dorsally pale green, translucent, with few scattered, diffuse yellow flecks. Throat greenish blue, translucent; ventral skin transparent, visceral peritoneum white. Iris yellowish white, red around the pupil; a black ring surrounding the iris externally; from the pupil to the posterior part of eye, the colours are successively red, yellowish white, black, blue, and black again.

Variation. The topotypical specimen ZSM 5108/2005 is identical except for two small brown spots on dorsum. In calling males we observed a highly extensible single subgular vocal sac.

Natural history. Specimens were heard along a stream flowing through an exposed and largely unforested area at Andohahela. The stream was bordered by some trees and dense shrub vegetation at some sites, and distance to closed rainforest was 100– 200 m. Along this stream, at night large mixed choruses of Boophis andohahela and B. haingana (see below) were heard. In between, a few specimens emitting a different call in very regular intervals could be detected, and two of these were eventually collected. They were sitting in dense shrub, on leaves at 1–2 m perch height.

Vocalization. The following description is based on recordings of the type specimens which were both identified as calling males. The call of B. miadana consists of a series of moderately long pulsed notes repeated in slow, but regular succession ( Fig. 24A ). Pulses within notes are clearly recognizable, but the slightly noisy recording prevents exact pulse counts. Numerous indistinct frequency bands are recognizable in spectrograms at high frequency resolution. Notes exhibit distinct amplitude modulation with energy constantly increasing towards the end of the note. Numerical parameters of calls from Andohahela National Park (1550 m a.s.l.) are as follows: duration of note series, 13.1 seconds; note duration, 239–309 ms (267 ± 24; n = 13); inter-note interval, 670–906 ms (746 ± 69; n = 11); note repetition rate, 1.0–1.2 notes/second; dominant frequency range 2100–3300 Hz, maximum call energy at 2720–2820 Hz ( Vences et al. 2006, CD 1, track 30).

Comparative call data. Compared to calls of B. ankaratra , note duration in B. miadana is longer, as are intervals between notes (see Glaw & Vences 2002; Fig. 25 ). Moreover, pulses are clearly separated and the pulse rate within notes seems to be significantly higher in B. ankaratra . Calls of the sympatric B. haingana clearly differ by shorter note duration and significantly higher note repetition rate. Calls of B. schuboeae are more melodious, have shorter note duration and are repeated at a much higher rate ( Fig. 25A ).

Molecular relationships. The phylogenetic pattern observed in the subclade containing Boophis miadana ( Fig. 21 ) is rather complex. This species is placed sister to B. ankaratra , but the bootstrap and Bayesian analyses provide no significant support for this placement; B. haingana (described below) and B. schuboae form a separate lineage. Boophis ankaratra itself is further divided into one lineage spanning much of its distribution area (here including specimens from Mandraka, Manjakatompo and Col des Tapias south of Antsirabe), and specimens from Antoetra. The latter individuals were collected by F. Andreone and showed rather slow calls ( Boophis sp. aff. ankaratra "Antoetra slow" in Glaw & Vences 2007); their molecular differentiation from typical B. ankaratra (which seems to occur in the Antoetra region as well, but molecular data are not available) is 2.2–2.9% and their status requires a further in-depth study (see Comparisons below). The differentiation of B. miadana is 2.3–2.5% from typical B. ankaratra and 3.5% from B. schuboeae .

Taxonomic remarks. As discussed previously ( Glaw & Vences 2002), a morphological differentiation of B. ankaratra and B. schuboeae is not possible, and this applies also to B. miadana (and B. haingana ) as described herein, relative to B. ankaratra and B. schuboeae and to each other. All these species form a monophyletic group and are morphologically very similar, but can be distinguished by note duration and inter-note interval duration of their advertisement calls ( Fig. 25 ).

The closest relationships of B. miadana are probably with B. ankaratra , although it is not grouped as its direct sister species in the molecular analysis. The two species are similar in having a relatively slow call, with long intervals and long notes (see comparative call data below). Such call parameters, in frogs, are known to differ with temperature and with state of sexual motivation, as also indicated by the calls of B. haingana from two sites of different elevation (and temperature) at Andohahela ( Fig. 25 ). However, we are convinced that such temperature or motivational differences cannot explain the long note and interval durations of B. miadana . The calls of B. ankaratra are known to be rather similar across its range, from Ambohitantely to Andringitra, across a north-south transect of over 400 km in the central highlands of Madagascar ( Glaw & Vences 2002). Even the slowest call recorded of B. ankaratra (from a male with very low motivation, calling only very sporadically in Itremo) still is characterized by, on average, a shorter inter-note interval (671 ms) than the calls of B. miadana , and note duration is consistently and distinctly shorter in this and all other available B. ankaratra recordings (range in six populations 94–204 ms; see data in Glaw & Vences 2002). Conversely, the calls of B. miadana were emitted by various highly motivated males that called very continuously at Andohahela.

A further candidate species of this complex exists, and was designated Boophis sp. aff. ankaratra "Antoetra slow" in Glaw & Vences (2007). This species was observed by F. Andreone in probable sympatry with B. ankaratra in the Antoetra region, which would strongly support its status as a separate, reproductively isolated species. A detailed revision of the respective material will be necessary, but it is probable that the specimens FAZC 11454, 11462 and 11480 belong to this new species. By molecular data, these species is grouped closer to B. ankaratra than to B. miadana ( Fig. 21 ). If the identity of these specimens was verified, it would provide a further argument for the species status of B. miadana relative to B. ankaratra , although at present the underlying rationale is indirect and requires further study.

Distribution. At present, Boophis miadana is only reliably known from its type locality, Andohahela National Park, at elevations above 1500 m a.s.l. (Appendix 10).

Figures

FIGURE 21. Maximum parsimony 16S rRNA phylogram for the Boophis albipunctatus group. From 485 total characters, 391 were constant and 72 parsimony informative. MP searches retained 26 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 herein are in bold.

FIGURE 22. Male holotype of Boophis miadana sp. nov. (ZSM 5107/2005) from Andohahela, 1550 m a.s.l.: (A) dorsolateral view; (B) ventral view.

FIGURE 24. Spectrogram and waveform of advertisement calls of: (A) Boophis miadana sp. nov. from Andohahela National Park, 1550 m a.s.l. (recorded on 26 January 2005, air temperature app. 17.6°C); (B) Boophis haingana sp. nov. from Andohahela National Park, low altitude (recorded on 3 February 2004, air temperature app. 23.2°C).

FIGURE 25. Comparative waveform sections (each 2000 ms duration) of advertisement calls of species in the Boophis albipunctatus group: (A) Boophis schuboeae (Ranomafana National Park, 23°C); (B) Boophis haingana sp. nov. (Andohahela National Park, low altitude, 23.2°C); (C) Boophis haingana sp. nov. (Andohahela National Park, 1600 m a.s.l., 17.6°C); (D) Boophis ankaratra (Manjakatompo, 18°C); (E) Boophis miadana sp. nov. (Andohahela National Park, 1550 m a.s.l., 17.6°C).