Boophis haingana, 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 : 48-51

Boophis haingana sp. nov.

( Fig. 23 , Appendix 9)

Remark. This species has been referred to as Boophis sp. aff. ankaratra "Andohahela fast" by Glaw & Vences (2007:172–173) and as Boophis sp. 20 by Vieites et al. (2009).

Holotype. ZSM 5109 /2005 ( FGZC 2390 ), 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., southeastern Madagascar, collected on 26 January 2005 by P. Bora, F. Glaw and M. Vences.

Paratypes. UADBA 24749 and UADBA ( FGZC 219 , 220 ), three adult males, from Andohahela , between Isaka and Eminiminy, Camp 2, 24°44'18''S, 46°50'25''E, ca. 600 m a.s.l., collected on 1–4 February 2004 by F. Glaw, M. Puente , R. Randrianiaina and M. Thomas ; UADBA ( FGZC 2448 , 2486 , 2537 ) , ZSM 5110 / 2005 ( FGZC 2447 ), four males , and ZSM 5111 / 2005 ( FGZC 2487 ) , ZSM 5112 / 2005 ( FGZC 2536 ), two females , all from Andohahela , stream at high altitude, ca. 45 minutes walking distance from holotype locality (no coordinates available), collected on 28–30 January 2005 by P. Bora, F. Glaw and M. Vences ; ZFMK 90153 (formerly ZSM 122 /2004 [ FGZC 218 ]) and ZSM 129 / 2004 ( FGZC 239 ), two adult males, from Andohahela , between Isaka and Eminiminy, Camp 2, 24°44'18''S, 46°50'25''E, ca. 600 m a.s.l., collected on 1–4 February 2004 by F. Glaw, M. Puente , R. Randrianiaina and M. Thomas .

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

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 25–29 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 yellow-whitish 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 its high morphological similarity to B. ankaratra . The new species differs from all other species in the Boophis albipunctatus group by a moderate to strong genetic differentiation (see below). Within the B. albipunctatus group, the new species belongs to a clade of morphologically very similar species ( B. ankaratra , B. schuboeae , B. miadana , and B. haingana ) 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. haingana is characterized by the shortest duration of notes in advertisement calls (see Fig. 25 and Comparisons section below).

Description of the holotype. Adult male, SVL 25.7 mm. Body moderately slender; head as long as wide, wider than 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 39% of ED; supratympanic fold barely distinct; vomerine odontophores distinct, well separated in two elongated patches, positioned posteromedial to choanae; choanae mediumsized, 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(1.25), 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 25.7, HW 9.3, HL 9.3, ED 3.3, END 2.1, NSD 2.4, NND 3.2, TD 1.3, TL 13.2, HAL 8.6, FOL 10.6, FOTL 18.1.

After almost three years in preservative, ground colour of upper surfaces of head, dorsum, and limbs creamy yellow; there is a brown small spot on dorsum and two more on head, one in the interorbital region and another on the right upper eyelid; dark pigmentation around nostrils. Ventral surfaces uniformly creamy yellow.

In life, the holotype was dorsally pale green, translucent, with scattered, diffuse yellow flecks, and three brown spots, one on dorsum and two on head. The throat was greenish blue, translucent; the ventral skin was transparent, and the visceral peritoneum white. Iris was white, red around the pupil, with a black ring surrounding the iris externally; from the pupil to the posterior part of eye, the colours are successively red, white, black, blue, and black again.

Variation. Morphometric variation is given in Appendix 8. Females are larger, at average having approximately 136 % of male SVL. All collected specimens are very similar in colouration and external morphology. In calling males we observed a highly extensible single subgular vocal sac.

Natural history. At higher elevation of Andohahela National Park, specimens were collected in syntopy with Boophis andohahela and B. miadana (see above), along a stream flowing through an exposed and largely unforested area, at about 100–200 m from closed forest. Specimens were calling at night from perch heights of 1–2 m in the shrubby vegetation along the stream. At low elevations of Andohahela National Park, specimens were collected from perch heights of at least 2 m, in vegetation in closed rainforest at some distance from a stream.

Vocalization. The call of B. haingana consists of a long series of short pulsatile notes repeated in fast and regular succession ( Fig. 24B ). Pulses within notes are clearly recognizable but not distinctly separated from each other, preventing exact counts. Three distinct frequency bands are evident in the spectrogram. With higher temperature, note repetition rate increases, but note duration roughly remains the same. Notes exhibit clear amplitude modulation, with maximum energy at the middle of the note. Here we present data for two populations of the new species from Andohahela National Park, one from low altitude (600 m a.s.l., air temperature 23.2°C, recorded specimen ZSM 129/2004), and the other from 1550 m a.s.l. (air temperature 17.6°C). Low altitude population ( Fig. 24B ): duration of note series, 16.2 seconds; note duration, 36–60 ms (49 ± 7; n = 25); inter-note interval, 142–232 ms (184 ± 24; n = 25); note repetition rate, 4.2–4.5 notes/second; dominant frequency range 2200–3200 Hz, maximum call energy at 2770–2810 Hz. High altitude population: duration of note series, 28 seconds; note duration, 55–90 ms (72 ± 9; n = 29); inter-note interval, 245–365 ms (306 ± 32; n = 29); note repetition rate, 2.6–3.0 notes/second; dominant frequency range 2300–3200 Hz, maximum call energy at 2680–2880 Hz ( Vences et al. 2006, CD 1, track 29).

Comparative call data. In comparison to calls of B. ankaratra and B. schuboeae , note duration in B. haingana is significantly shorter (see Glaw & Vences 2002; Fig. 25 ). Moreover, amplitude modulation of notes differs by the highest energy present in the middle of notes in B. haingana vs. at the end of the notes in B. ankaratra and B. schuboeae . Notes of B. schuboeae are generally of slightly pulsatile nature, but have a melodious character compared to B. haingana . Notes of B. ankaratra have distinctly separated pulses, whereas the pulses in notes of B. haingana are partly fused. Compared to calls of the syntopical B. miadana , note duration in B. haingana is much shorter and note repetition much faster (see above; Fig. 25 ).

Molecular relationships. The molecular phylogenetic analysis places Boophis haingana sister to B. schuboeae ( Fig. 21 ) but this relationship receives no bootstrap or Bayesian support. Molecular divergence of B. haingana is 4.1–4.6% from B. ankaratra , 4.4–4.6% from B. miadana , and 4.6–4.8% from B. schuboeae . The single specimen of B. haingana studied from high elevations of Andohahela National Park differs by 0.4% from the low-altitude specimens which all have identical sequences.

Comparisons. See Comparisons section of B. miadana above for a general discussion of the morphological and bioacoustic differentiation in the clade of species formed by B. ankaratra , B. haingana , B. miadana , and B. schuboeae . The closest relationships of B. haingana are with B. schuboeae . The two species cluster in the molecular analysis ( Fig. 21 ) albeit without significant support, and they are similar in their relative fast calls with short inter-note intervals. Recordings from low and high elevations at Andohahela demonstrate that the inter-note intervals in B. haingana strongly depend on the temperature and become distinctly larger at low temperatures. However, similar to what has been reported in B. ankaratra (see Glaw & Vences 2002), note duration of B. haingana appears to be unaffected by temperature, and the differences to B. schuboeae remain stable ( Fig. 25 ), supporting their status as two different species differing by a distinct call.

Distribution. At present Boophis haingana is only reliably known from its type locality, Andohahela National Park (Appendix 10), where it occurs at both low and high elevations (600-1550 m a.s.l.).

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 23. Male holotype of Boophis haingana sp. nov. (ZSM 5109/2005) from Andohahela: (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).