Boophis ulftunni, Wollenberg & Andreone & Glaw & Vences, 2008

Wollenberg, K. C., Andreone, F., Glaw, F. & Vences, M., 2008, Pretty in pink: A new treefrog species of the genus Boophis from North-Eastern Madagascar, Zootaxa 1684 (1), pp. 58-68 : 59-65

Boophis ulftunni sp. n.

Holotype. MRSN A4287, adult male, from the Masoala Peninsula, Menamalona (Campsite 5), Ilampy Corridor, 15°22.87'S, 49°59.27'E, 610–630 m altitude in North-Eastern Madagascar, collected on 1 December 1998 by F. Andreone and J. E. Randrianirina.

Paratypes. All paratypes are from North-Eastern Madagascar. MRSN A4286, adult male, from same locality and same collection data as holotype; MRSN A2572, adult female, from the Masoala Peninsula , Andasiny Governera (Campsite 3), Ambatoledama Corridor, 15°18'S, 50°01'E, 610–630 m alt., collected on 5 December 1998 by F. Andreone and J. E. Randrianirina; MRSN A2559–2562, one adult female and three adult males, from the Masoala Peninsula, Ambohitsitondroina (Campsite 6), 15°26.00’S, 49°57.34’ E, 1106 m alt., collected on 31 January 2002 by J. E. Randrianirina .

Further material. All further material is from North-Eastern Madagascar. MRSN A1858, adult male, from Tsararano Chain , Campsite 2, Andatony Anivo , 14°54.80’S, 49°42.60’E, 600–750 m alt., collected on 15 December 1996 by F. Andreone and J. E. Randrianirina; MRSN A4448–4450, two adult females and one adult male, from the western slope of the Anjanaharibe-Sud Massif , Valley of Analabe River, 14°46.62’S, 49°26.60’E, 1050 m alt., collected on 3 February 1996 by F. Andreone, J. Randriamahazo and J. E. Randrianirina; ZSM 80 /2005, adult male from Marojejy National Park, Campsite locally known as Camp Simpona, 14°26.199’S, 49°44.6’E, 1326 m alt., collected on 16 February 2005 by F. Glaw, M. Vences and R.- D. Randrianiaina .

Diagnosis. A species assigned to the genus Boophis based on the presence of intercalary elements between terminal and subterminal phalanges of fingers and toes (externally verified), absence of femoral glands, presence of (weakly developed) nuptial pads in males, general morphological resemblance to other Boophis species , and molecular phylogenetic evidence. All species of Boophis in the subgenus Sahona and in the B. albilabris group, B. goudoti group and B. microtympanum group have larger body sizes and no translucent green ground colour. Distinguished from species in the B. majori group by green translucent (rather than brownish) ground colour, and by an advertisement call consisting of trills (not known from any species of the B. majori group except B. blommersae). Distinguished from species in the B. albipunctatus group and the B. luteus group by smaller size (male SVL 22–24 vs. 24–46 mm) and by the presence of distinct reddish-brown to pink spots and patches on the dorsum. Distinguished from species in the B. mandraka group and B. rappiodes group by non-transparent ventral skin. Although some other species of green Boophis have trill calls of similar general structure as B. ulftunni (especially B. erythrodactylus , B. andohahela, B. jaegeri), the detailed temporal call parameters of B. ulftunni differ from these species.

The molecular analysis reveals that B. ulftunni is related to species of the B. microtympanum group. B. ulftunni strongly differs from all species currently recognised in the B. microtympanum group by morphology and by molecular characters (see below).

Description of the holotype. Adult male, SVL 23.0 mm (for measurements see Table 1). Body slender; head as long as wide, wider than body; snout rounded in dorsal view, slightly truncate in lateral view, nostrils directed laterally, slightly nearer to tip of snout than to eye; canthus rostralis and loreal region both slightly concave; tympanum distinct, rounded, 40% of eye diameter; supratympanic fold not recognizable; tongue ovoid, distinctly bifid, posteriorly half free; vomerine odontophores distinct; positioned posteromedian to choanae; choanae small, rounded. Arms slender, subarticular tubercles single, round; metacarpal tubercles unrecognizable; fingers with weak webbing; webbing formula 1(2), 2i(1.5), 2e(1.25), 3i(2.5), 3e(1.5), 4(0.75); relative length of fingers 1<2<4<3 (finger 2 shorter than finger 4); finger disks moderately enlarged; small unpigmented nuptial pads faintly recognizable on inner side of first finger. Hindlimbs slender; tibiotarsal articulation reaches nostril when hindlimb is adpressed along body; lateral metatarsalia separated by webbing; inner metatarsal tubercle distinct, no outer metatarsal tubercle; webbing formula between toes 1(0.5), 2i(1.25), 2e(0.5), 3i(1.75), 3e(0.5), 4i(2), 4e(2), 5(0.5); relative length of toes 1<2<5=3<4; toe disks slightly enlarged. Skin on dorsal surfaces and ventrally on throat smooth; ventral skin on belly and around cloacal opening glandular.

In preservative uniformly cream-white with a thin reddish-brown line reaching from eye to snout tip, supraorbital reddish-brown marks converging into a spot on the head ( Figure 1 ). Colour in life unknown.

Variation. The morphological variation of the type specimens is shown in table 1. The specimen from Marojejy (ZSM 80/2005) has the following differences to the holotype: hand webbing formula 1(2), 2i(1.5), 2e(1.25), 3i(2.5), 3e(1.5), 4(1); webbing formula between toes 1(0.5), 2i(1), 2e(0.25), 3i(1.25), 3e(0.25), 4i(1.25), 4e(1.25), 5(0.5); nostrils directed slightly nearer to eye than to tip of snout; dorsolaterally with a thin brownish-pink line that reaches until each nostril, and irregular pink spots on dorsum, arms and thighs.

Colouration in life (based on photographs shown in Figure 2 ): Dorsum translucent green; dorsolaterally with a metallic-cream white line accompanied by pink spots extending to snout tip and converging at the urostyle; supraorbital reddish-brown to pink marks converging into a reddish-brown or pink blotch on the middle of the head (y-shaped); and irregular pink spots and blotches on dorsum, flanks, knees, upper arms and upper thighs which can be accompanied by metallic-cream-white marks. Iris with outer yellow area and inner purple area which irregularly border onto each other. Toes and finger disks uniformly green. The amount of pink colour pattern on head, dorsum and extremities seems to be variable among specimens and populations, and the same accounts for the metallic-white colour elements ( Figure 2 ). In the Marojejy specimen, additional blue hue can be observed on thighs and rear end of dorsum.

Vocalization. The call of Boophis ulftunnni sp. n. consists of single pulsed notes that can be described as trills and that are repeated after relatively irregular intervals. Each note is a succession of short pulses with considerable variation in interpulse durations. In some of the available recordings (especially in those from Masoala, partly in those from Marojejy), most notes are of noisy appearance and pulses are only weakly discernible in parts of the call ( Figure 3a–b ), while other notes are clearly pulsed. In other recordings (especially in those from Anjanaharibe-Sud), the pulses are clearly recognizable in all notes ( Figure 3c–d ). Whether this is due to variation among populations, or due to a different motivational state of specimens, cannot be determined at present. Possibly two note types exist, one with fast and one with slow pulse repetition rate ( Figure 3 ), but these note types are not always clearly distinguishable and their temporal and spectral parameters are therefore merged in the analysis ( Table 2). We furthermore note the presence of single or double "click" sounds that can be emitted between calls. No significant frequency modulation could be observed.

Molecular phylogenetic relationships. The phylogeny reconstructed from a fragment of the mitochondrial 16S rRNA gene shows B. ulftunni as belonging into a distinct evolutionary lineage, sister to B. microtympanum ( Figure 4 ). Despite the obvious phenotypical similarities to members of the B. rappiodes group such as translucent green colour on dorsum, reddish spots, or a y-shaped pattern on the head, the pairwise genetic dis- tances between these and B. ulftunni are very high (10.7% to B. rappiodes ). Furthermore, B. ulftunni does not bear genetic similarity to the phenotypically similar B. mandraka group (genetic distances to B. mandraka 14.1–14.9%). The sister relationship of B. ulftunni sp. n. with B. microtympanum receives relevant support in ML and MP bootstrap analyses. Pairwise genetic distances between B. ulftunni sp. n. and B. microtympanum are also higher than 10%, which supports the status of B. ulftunni as a valid species. Based on more comprehensive phylogenetic analyses including all currently described species of Boophis (not shown), B. ulftunni is in fact confirmed as related to the B. microtympanum group (which in turn is monophyletic, containing the species B. laurenti, B. microtympanum , B. rhodoscelis, and B. williamsi), but more extended analyses including more genetic markers have yet to show if these two Boophis lineages are in fact sister to each other. The sequenced type specimens of B. ulftunni from Masoala (which are genetically identical) furthermore showed considerable genetic variation as compared to the single specimen from Marojejy (pairwise genetic distances 5.0%).

Natural history. At Marojejy, specimens were heard at night, calling from high perches (2–4 m) in the vegetation along a small stream in rainforest, at an elevation of approximately 1300 m above sea level. Specimens were relatively common but difficult to observe at this site. The sites at Masoala where the species has been found are all typical low- and mid-altitude rainforests, being represented by patches of rather intact pristine or re-grown secondary forest. The individuals were found along forest streams, mainly in areas characterized by dense vegetation. All the Masoala sites lie outside the Parc National de Masoala boundaries, and represent corridors between larger forest nuclei. The habitat in Analabe (Anjanaharibe-Sud Massif) is a patchwork of pristine and altered forest, with most of the unaltered forest occurring on its ridge and steepest slopes. In the degraded patches, the original vegetation has been replaced by ferns and grasses. The Tsararano Chain lies south of the Andapa Basin, midway between the Anjanaharibe-Sud Massif and the Masoala Peninsula and is formed by several hills (altitude 400–1,269 m). The forest of Tsararano appears to be relatively intact, most likely due to its distance from large villages.

Etymology. The specific name is dedicated to Dr. Ulf Walter Tunn in recognition for his support of research and nature conservation through the Biopat initiative.

ysis.

Figures

FIGURE 1. Specimens of Boophis ulftunni sp. n. I. male holotype from Masoala (MRSN A4287); II. male paratype from Masoala (MRSN A2562); III. male specimen from Marojejy (ZSM 80/2005); IV. female specimen from Anjanaharibe-Sud (MRSN A4449). Scale represents 10 mm.

FIGURE 2. Life colouration of B. ulftunni. The photos show specimens from I, Masoala, II, Tsararano, IIIa, Marojejy (ZSM 80/2005; IIIb, ventral view), and IVa, Anjanaharibe-Sud (IVb, ventral view).

FIGURE 3. Sonagrams and oscillograms of advertisement calls of Boophis ulftunni. (a) and (b) show a fast and a slow pulsed note, respectively, from Masoala (type locality). (c) and (d) show a fast and a slow-pulsed note from Anjanaharibe-Sud. Note that the pulses in the fast Masoala call are poorly recognizable and pulse rate is much faster than in Anjanaharibe. However, this could be due to a higher motivational state in the Masoala specimens which were recorded while calling in a dense chorus, whereas the Anjanaharibe specimen was calling from a smaller and less dense aggregation of individuals. The additional short sounds in (a) and (b) may have at least partly been emitted by B. ulftunni as well, but this cannot be ascertained from the available recordings on which also other syntopic frogs can be heard.

FIGURE 4. Maximum-likelihood tree of 13 Boophis species including B. ulftunni sp. n. Numbers on nodes indicate bootstrap values higher than 50% in MP (first numbers) and ML tree searches (second numbers).