Boophis kirki, Vences & Köhler & Hutter & Preick & Petzold & Rakotoarison & Ratsoavina & Glaw & Scherz, 2024

Vences, Miguel, Köhler, Jörn, Hutter, Carl R., Preick, Michaela, Petzold, Alice, Rakotoarison, Andolalao, Ratsoavina, Fanomezana M., Glaw, Frank & Scherz, Mark D., 2024, Communicator whistles: A Trek through the taxonomy of the Boophis marojezensis complex reveals seven new, morphologically cryptic treefrogs from Madagascar (Amphibia: Anura: Mantellidae), Vertebrate Zoology 74, pp. 643-681 : 643-681

Boophis kirki sp. nov.

Lineage A = Ca 51 Figures 6 , 8

Identity.

This species has previously been referred to as B. marojezensis [Ca 51 JQ 518198 ] = B. marojezensis [Ca 51] by Randrianiaina et al. (2012) and B. sp. Ca 51 in Hutter et al. (2018). It was included in B. marojezensis sensu lato by Glaw et al. (2001) and Glaw and Vences (2007) and not explicitly included or mentioned in the studies of Vieites et al. (2009) and Perl et al. (2014).

Holotype.

ZSM 699 / 2003 (FGMV 2002.331), adult male, collected by F. Glaw, M. Puente, L. Raharivololoniaina, M. Thomas, and D. R. Vieites on 20 January 2003 at Kidonavo bridge , near Vohiparara, Ranomafana National Park (21.2167 ° S, 47.3667 ° E), ca. 1000 m a. s. l., Southern Central East of Madagascar.

Paratypes.

ZSM 700 / 2003 (FGMV 2002.332), adult male, with same collection data as holotype . KU 336874 (CRH 17), adult male collected by C. R. Hutter, Z. F. Andriampenomanana, and S. Justin on 13 January 2014 at Valohoaka , Ranomafana National Park (21.2987 ° S, 47.4385 ° E, 1085 m a. s. l.) . KU 336875 (CRH 18) adult male collected by C. R. Hutter, Z. F. Andriampenomanana, and S. Justin on 13 January 2014 at Valohoaka , Ranomafana National Park (21.2987 ° S, 47.4386 ° E, 1086 m a. s. l.) . UADBA - CRH 15 (CRH 15), adult male collected by C. R. Hutter, Z. F. Andriampenomanana, and S. Justin on 13 January 2014 at Valohoaka , Ranomafana National Park (21.2973 ° S, 47.4389 ° E, 1067 m a. s. l.) . KU 336876 (CRH 19), adult male, collected by C. R. Hutter, Z. F. Andriampenomanana, and S. Justin on 14 January 2014 at Valohoaka , Ranomafana National Park (21.2975 ° S, 47.4390 ° E, 1065 m a. s. l.) . KU 336967 (CRH 20), adult male, collected by C. R. Hutter, Z. F. Andriampenomanana, and S. Justin on 14 January 2014 at Valohoaka , Ranomafana National Park (21.2975 ° S, 47.4390 ° E, 1065 m a. s. l.) . KU 336877 (CRH 105), adult male, collected by C. R. Hutter, Z. F. Andriampenomanana, E. Rajery, and S. Justin on 28 January 2014 at Maharira , Ranomafana National Park (21.3399 ° S, 47.4108 ° E, 1272 m a. s. l.) . KU 336880 (CRH 185), adult male, collected by C. R. Hutter, Z. F. Andriampenomanana, and S. Justin on 26 December 2013 at Valohoaka , Ranomafana National Park (21.2978 ° S, 47.4389 ° E, 1066 m a. s. l.) . MRSN - A 2245 (FAZC 11467), adult, collected by F. Andreone between 30 January and 3 February 2003 at Farihimazava (= Farimazava) Forest , near Antoetra (ca. 20.8350 ° S, 47.3325 ° E, 1380–1420 m a. s. l.) .

Additional material.

The following specimens from Vohidrazana are not included in the paratype series due to their relatively high genetic divergence compared to specimens from the type locality: UADBA - CRH 430 (CRH 430), adult female, collected by C. R. Hutter, S. M. Lambert, and Z. F. Andriampenomanana on 3 January 2015 at Vohidrazana (18.9861 ° S, 48.5015 ° E, 1164 m a. s. l.) . KU 340727 (CRH 449) and KU 340730 (CRH 455), two adult males, collected by C. R. Hutter, S. M. Lambert, and Z. F. Andriampenomanana on 4 January 2015 at Vohidrazana (18.9794 ° S, 48.5181 ° E, 1105 m a. s. l.) .

Definition.

A small treefrog assigned to the genus Boophis , subgenus Boophis , in the family Mantellidae based on occurrence on Madagascar, presence of intercalary element between ultimate and penultimate phalanx of fingers and toes (verified by external examination), presence of webbing between fingers, presence of nuptial pads in males, and absence of femoral glands in males. Assigned to the Boophis blommersae group based on small body size (male SVL 20.0– 23.4 mm), predominantly brownish dorsal coloration, suctorial stream-dwelling tadpoles, and molecular phylogenetic relationships. Within the B. blommersae group, defined by absence of dorsolateral bands, presence of red color in the outer iris area, especially at the dorsal and ventral edges, in many specimens, and advertisement calls at 3499–5604 Hz, consisting of a series of 9–19 whistling notes of successively increasing durations of 54–105 ms. Also characterized by numerous diagnostic nucleotide positions in the mitochondrial 16 S rRNA gene: MolD identified the following robust diagnostic nucleotide combination compared to all other species in the B. marojezensis complex (sites given relative to the full-length 16 S sequence of Mantella baroni ): “ A ” in the site 17, “ C ” in the site 50, “ T ” in the site 159, “ A ” in the site 179.

Diagnosis.

Within the B. blommersae group, distinguished from B. blommersae by calls consisting of frequency-modulated whistles (vs. pulsed trills); and from B. vittatus by calls consisting of frequency-modulated whistles (vs. series of short clicks), and absence of dorsolateral stripes (vs. presence). Furthermore, distinguished from B. marojezensis by presence of red color in outer iris area in many specimens (vs. absence), and calls consisting of 9‒19 whistling notes of successively increasing durations of 54–105 ms (vs. 7–8 notes, with short and long notes distinguishable). For a distinction from other species of the B. marojezensis complex described herein, see accounts of these new species below.

Description of the holotype.

Adult male, in good state of preservation, SVL 23.4 mm, tongue and right forelimb removed as tissue samples for molecular analysis. Body slender; head wider than long, wider than body; snout rounded in dorsal view, truncate in lateral view; nostrils directed laterally, nearer to tip of snout than to eye; canthus rostralis indistinct, slightly concave in dorsal view, loreal region slightly concave; tympanum indistinct but recognizable, round, TD 50 % of ED; supratympanic fold not recognizable; vomerine odontophores weakly developed, well-separated in two very small rounded aggregations, positioned posteromedial to choanae; choanae medium-sized, rounded; maxillary teeth present. Tongue removed. Arms slender, subarticular tubercles single, round; metacarpal tubercles not recognizable; fingers weakly webbed and with lateral dermal fringes; webbing formula 1 (traces), 2 i (traces), 2 e (traces), 3 i (traces), 3 e (1.75), 4 (1); relative length of fingers 1 <2 <4 <3 (finger 2 distinctly shorter than finger 4); finger discs enlarged, rounded; nuptial pads recognizable as unpigmented swelling on first finger. Hindlimbs slender; tibiotarsal articulation reaching nostril when hindlimb 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), 2 i (1), 2 e (0), 3 i (1), 3 e (0.25), 4 i (1.5), 4 e (1.5), 5 (0.25); relative length of toes 1 <2 <3 <5 <4; toe discs enlarged, rounded. Skin smooth on dorsal surfaces, throat, chest, and ventral surface of thighs, finely granular on belly; cloacal region surrounded by an area of distinct, large, white-colored granules.

In preservative, 20 years after collection (Fig. 6 ), dorsally reddish brown with a distinct and strongly contrasted dark brown hourglass-shaped marking on anterior part of the dorsum, and a dark brown transverse bar, somewhat chevron-shaped, on the posterior part of the dorsum. In addition, a few small dark brown and cream spots are scattered across the dorsum. A distinct light beige vertebral stripe runs from snout to cloaca and interrupts the dark markings. Limbs light brown with darker brown crossbands: 4–5 on forearm, 6–7 on shank, 6 on thigh. Ventrally cream, white on belly, with some dark pigment only on ventral side of feet. Color of holotype in life not recorded.

Variation.

The paratype ZSM 700 / 2003 has a brown dorsal ground color with an irregular pattern of strongly contrasted small light markings, and neither vertebral stripe nor hourglass-patch. For variation of color in life in other paratypes, see Figure 8 . A vertebral stripe as in the holotype is also observed in KU 336875 , but not in the remaining specimens. Some individuals show a fine dotting with dark brown spots dorsally (e. g., KU 336967 and KU 336875 , others have a dense spotting of small yellowish spots, mostly dorsolaterally (e. g., paratypes KU 336874 and KU 340730 ). Some specimens in life had relatively distinct red color ventrally on hindlimbs (Fig. 8 D, E ) while this was not apparent in others (e. g., Fig. 8 J ). The outer iris area was reddish in some specimens ( KU 336874 from Ranomafana; KU 340730 from Vohidrazana) but only light orange in others (e. g., KU 336967 ). One female collected in January had light-colored oocytes visible through the ventral skin ( UADBA - CRH 430 ; Fig. 8 G ). Iris periphery turquoise.

Etymology.

Named after the fictional character Captain James T. Kirk, first portrayed by William Shatner in Gene Roddenberry’s Star Trek (The Original Series), and also portrayed by Chris Pine in J. J. Abrams’ Star Trek films.

Tadpole.

The tadpole of this species (under the name B. marojezensis [Ca 51]) was described and illustrated by Randrianiaina et al. (2012), based on the DNA barcoded specimen ZSM 267 / 2008 (ZCMV 3691; GenBank accession number JQ 518198 ) from Ranomafana. As typical for all tadpoles of the group, the larvae belong to the “ suctorial ” ecomorphological guild. They have a large oral disk used to adhere to stones in fast-flowing water, a labial tooth row formula of 7 (5-7) / 3, and large numbers of oral papillae (297 marginal and 309 submarginal; without dorsal gap). They are characterized by absence of a lateral transparent area of the integument, tail muscle covered by reticulations mainly on the anterior half, and eyes situated between the anterior 3 / 10 and 4 / 10 of the body.

Natural history.

An arboreal, nocturnal treefrog found in humid rainforests along fast flowing streams. Little is known of the ecology of the species. At Valohoaka in December 2013 and January 2014, male specimens were found calling sitting on leaves or branches, 1‒2 m above the ground along streams. Additionally, calling males generally were perched 1 meter to occasionally several meters above the ground, at places that often could not be reached for observation.

Calls.

Advertisement calls of B. kirki sp. nov. recorded at Ranomafana on 1 March 1996 (ca. 22–23 ° C air temperature) consist of multiple tonal notes of medium duration, repeated at regular intervals. In each call, the first note is always lower in dominant frequency (4640–4895 Hz) compared to subsequent notes (5528–5668 Hz). Moreover, the first 3–5 notes of each call have a lower relative amplitude than subsequent notes. Each note exhibits a distinct upward frequency modulation, encompassing a shift in dominant frequency range of about 700 Hz from the beginning to the end of the note. Within calls, notes tend to become slightly longer in duration from the beginning to the end of the call. Call energy is distributed in a narrow frequency band. Numerical parameters of four analyzed calls are as follows: call duration 2036–2355 ms (2170.0 ± 165.8 ms); notes / call 16–18 (16.8 ± 0.9); note duration 60–105 ms (75.7 ± 10.0 ms); inter-note interval 45–65 ms (54.0 ± 5.2 ms); note repetition rate within calls varies between ca. 6.5–8.2 notes / second; dominant frequency 5538–5604 Hz (5567 ± 34 Hz); prevalent bandwidth 4600–6100 Hz.

Calls recorded at Valohoaka, Ranomafana, on 12–13 January 2014 (air temperature not recorded) and corresponding to the voucher specimens KU 336874 –336876 agree with the calls described above in overall character, although some shorter calls are evident in the recordings. Numerical parameters of seven analyzed calls of three individuals are as follows: call duration 1180–2630 ms (1944.7 ± 564.5 ms); notes / call 10–19 (14.5 ± 3.2); note duration 54–104 ms (74.4 ± 15.9 ms); inter-note interval 33–71 ms (59.8 ± 9.9 ms); dominant frequency 4981–5604 Hz (5371 ± 205 Hz); prevalent bandwidth 4000–5900 Hz.

Calls recorded at Vohidrazana, Andasibe region, on 4 January 2015 (air temperature 19 ° C) and corresponding to voucher specimen CRH 455 also agree in character with those from the Ranomafana region described above, but are lower in dominant frequency. Numerical parameters of four analyzed calls are as follows: call duration 1370–1537 ms (1427.3 ± 85.5 ms); notes / call 9–12 (10.0 ± 1.4); note duration 59–105 ms (86.5 ± 13.5 ms); inter-note interval 60–104 ms (72.8 ± 16.3 ms); dominant frequency 3499–4242 Hz (3998 ± 300 Hz); prevalent bandwidth 3300–4500 Hz.

Distribution.

According to the molecular data summarized herein, the species is known from (1) the type locality, Vohiparara, and many other sites in Ranomafana National Park (Ambatolahy, Ambatovory, Fompohonina, Imaloka, Maharira, Mariavaratra, Ranomena, Sahateza, Samahalaotra, Valohoaka, Vatoharanana, Vohimanara), (2) from Antoetra (Farihimazava), based on barcoded specimen MRSN A 2245 ( Andreone et al. 2007); and (3) from Vohidrazana in the Andasibe region. The elevational range spans from mid elevations (e. g., 915 m a. s. l. at Ambatolahy) to relatively high elevations (1272 m a. s. l. at Maharira, up to 1420 m a. s. l. at Antoetra).

Figures

Figure 6. Preserved holotypes in dorsal and ventral views of the eight nominal species in the Boophis marojezensis complex described in this study.

Figure 8. Individuals of Boophis kirki sp. nov. in life. A, D Male paratype KU 336967 (CRH 20) from Ranomafana in dorsolateral and ventral view. B, E Male paratype UADBA - CRH 15 (CRH 15) from Ranomafana in dorsolateral and ventral view. C Male paratype KU 336874 (CRH 17) from Ranomafana. F Male paratype KU 336875 (CRH 18) from Ranomafana. G Female (no type status) UADBA - CRH 430 (CRH 430) from Vohidrazana. H Male (no type status) KU 340727 (CRH 449) from Vohidrazana. I, J Male (no type status) KU 340730 (CRH 455) from Vohidrazana in dorsolateral and ventral view. Note the variation in iris color in both populations (Ranomafana and Vohidrazana), with some individual having red color in the outer iris area while others only have light orange color.