Afrixalus phantasma Dehling, Greenbaum, Kusamba & Portik, 2022

Greenbaum, Eli, Portik, Daniel M., Allen, Kaitlin E., Vaughan, Eugene R., Badjedjea, Gabriel, Barej, Michael F., Behangana, Mathias, Conkey, Nancy, Dumbo, Bonny, Gonwouo, Legrand N., Hirschfeld, Mareike, Hughes, Daniel F., Igunzi, Félix, Kusamba, Chifundera, Lukwago, Wilber, Masudi, Franck M., Penner, Johannes, Reyes, Jesús M., Rödel, Mark-Oliver, Roelke, Corey E., Romero, Soraya & Dehling, J. Maximilian, 2022, Systematics of the Central African Spiny Reed Frog Afrixalus laevis (Anura Hyperoliidae), with the description of two new species from the Albertine Rift, Zootaxa 5174 (3), pp. 201-232 : 213-218

Afrixalus phantasma Dehling, Greenbaum, Kusamba & Portik sp. nov.

Ghost Spiny Reed Frog urn:lsid:zoobank.org:act:1B2DBF26-5B0A-4DA8-B65E-0BC01704C1B4

Afrixalus laevis (nec Megalixalus laevis Ahl 1930 )— Laurent 1972: 59 (partim); Laurent 1982: 33 (partim); Schiøtz 1999: 56 (partim); Channing & Howell 2006: 137 (partim); Spawls et al. 2006: 183 (partim); Channing & Rödel 2019: 158 (partim).

Holotype. ZFMK 103454 (field no. JMD 723 ), adult male, from Gishwati Forest (01.823745° S, 29.360373° E, 2084 m), now part of Gishwati-Mukura National Park, Western Province, Rwanda, collected on 5 April 2011 by J. Maximilian Dehling and Bonny Dumbo ( Figs. 7A , 8A–C ).

Paratypes. ZFMK 103455 (field no. JMD 722 ), adult female, collected with the holotype ; ZFMK 103456 (field no. JMD 2015-30 ), adult male , ZFMK 103457 (field no. JMD 2015-31 ), adult female, from the type locality in Gishwati Forest , both collected on 27 September 2015 by J. Maximilian Dehling and Bonny Dumbo ; ZFMK 103458–60 (field nos. JMD 677–679 ), three adult males, collected on 19 March 2011 by J. Maximilian Dehling , ZFMK 103461–62 (field nos. JMD 954–955 ), two adult males, collected on 16 February 2013 by J. Maximilian Dehling, all from Kamiranzovu Swamp (02.477165° S, 29.158243° E, 1962 m), Nyungwe National Park , Western Province, Rwanda ; UTEP 20791–20792 (field nos. EBG 2838 , 2843 ), two adult males, collected on 21 December 2009 by Chifundera Kusamba, Wandege M. Muninga, Mwenebatu M. Aristote, and Maurice Luhumyo from Nyakasanza Swamp near Tshibati (02.22886° S, 28.78017° E, 1979 m), South Kivu Province, DRC .

Referred specimens. UTEP 20802 (field no. EBG 1198 ), forest ca. 4 km NW of Lwiro (02.2226° S, 28.7754° E, 2077 m), South Kivu Province , DRC ; UTEP 20803 , 22418–20 (field nos. EBG 1232 , 1238–40 ), Kahuzi-Biega National Park , Mugaba (02.2750° S, 28.6631° E, 2298 m), South Kivu Province, DRC ; UTEP 20804 (field no. EBG 1283 ), Kahuzi-Biega National Park , Chinya (02.2671° S, 28.6455° E, 2267 m), South Kivu Province, DRC ; UTEP 20793–94 (field nos. EBG 2844–45 ), Nyakasanza Swamp near Tshibati (02.22886° S, 28.78017° E, 1979 m), South Kivu Province , DRC ; UTEP 20795–20800 , 22421 (field nos. ELI 414–20 ), Nyakasanza Swamp near Tshibati (02.22829° S, 28.77972° E, 1979 m), South Kivu Province , DRC ; UTEP 20801 (field no. ELI 425 ), Chanjoka (02.21261° S, 28.77644° E, 2115 m), South Kivu Province , DRC .

Diagnosis. The species is referred to the genus Afrixalus by exhibiting the following characteristics: fingers and toes webbed; tips of fingers and toes enlarged to discs; eye large; pupil vertically elliptical; tympanum indistinct; vomer ridges and teeth absent; dorsal surfaces finely shagreened with minute pointed tubercles; outer metatarsal tubercle distinct; gular gland in males. It is readily distinguished from most other members of the genus by its small size (SVL in males 20.1–24.6 mm, in females 22.6–26.4 mm), being smaller than A. dorsalis (males 25–28 mm, females 26–30 mm), A. fornasini (males 30–38 mm, females 35–40 mm), A. lacteus (males 22–27 mm, females 25– 29 mm), A. leucostictus (males 27–32 mm, females 25–36 mm), A. manengubensis (males to 32 mm), A. nigeriensis (males 28–34 mm, females 32–35 mm), A. osorioi (males 27–31 mm, females 32–35 mm), A. paradorsalis (males 28–34 mm, females 32–35 mm), A. septentrionalis (males 19–21 mm), and A. wittei (males 27–30 mm, females 29–33 mm); and larger than A. brachycnemis (males 18–21 mm, females 20–22 mm), A. delicatus (males 15–19 mm, females 17–22 mm), A. spinifrons (males to 20 mm, females to 25 mm), and A. stuhlmanni (males 15–21 mm, females 17–25 mm). Its differs in dorsal coloration and pattern from all species with longitudinal stripes or bands on a yellowish-brown background ( A. brachycnemis , A. crotalus , A. delicatus , A. dorsalis , A. enseticola , A. fornasini , A. fulvovittatus , A. knysnae , A. morerei , A. orophilus , A. quadrivittatus , A. schneideri , A. spinifrons , A. stuhlmanni , A. upembae , A. septentrionalis , A. vittiger , and A. wittei ); species with a conspicuous large dark dorsal blotch on a uniform background on anterior dorsum in combination with large blotches on both sides of the hip ( A. leucostictus , A. manengubensis , A. osorioi , A. paradorsalis , and A. schneideri ) or with longitudinal lateral dark bands ( A. equatorialis and A. nigeriensis ); species with a uniformly colored dorsum without conspicuous pattern except a dark dorsolateral stripe ( A. aureus , A. clarkei , A. delicatus , A. fornasini , A. lacteus , A. leucostictus [dorsum with small white tubercles], A. uluguruensis , and A. weidholzi [might have a black vertebral line and dark brown flanks]); and from all remaining species having either dark stripes running from tip of snout to back, crossing each other and continuing as dorsolateral stripes ( A. vibekensis , also males without asperities); anterior part of dorsum yellowish with brown pattern, posterior part of dorsum translucent ( A. laevis , also males without asperities); posterior part of dorsum and dorsal sides of limbs semi-translucent with dense small dark white-edged speckles ( A. dorsimaculatus ); and dark blotches and transverse marks with white speckles ( A. sylvaticus ).

The advertisement calls of the following species of Afrixalus consist of a long series of clicks, often initiated by a long buzzing note, and thus differ from the call of A. phantasma : A. aureus , A. brachycnemis , A. clarkei , A. crotalus , A. delicatus , A. dorsalis , A. fornasini , A. fulvovittatus , A. knysnae , A. nigeriensis , A. morerei , A. osorioi , A. quadrivittatus , A. septentrionalis , A. spinifrons , A. vibekensis , A. vittiger , A. weidholzi , and A. wittei . The advertisement calls of the remaining species for which information is available differ from the call of A. phantasma in the following characteristics (in parentheses): A. dorsimaculatus (soft, short buzzing rattle, usually repeated three times), A. equatorialis (series of five notes, repeated at 15–20/s and initiated by a long buzz, energy maximum at 2000–2500 Hz), A. lacteus (8–9 notes, 14–15 pulses,>300 pulses/s), A. paradorsalis (2–3 notes, energy maximum at 2700 Hz), A. stuhlmanni (2–9 notes, energy maximum at 4200–5100 Hz), and A. sylvaticus (2–5 notes, energy maximum at 4000–4500 Hz).

The new species is most similar to A. lacustris sp. nov. from which it differs by a number of characteristics (see below).

Description of holotype. Measurements of the holotype are provided in Table 2 . Body very slender, widest at temporal region, slightly tapering to groin ( Fig. 8A–C ); head small (HL/SVL 0.31, HW/SVL 0.30), about as long as wide (HW/HL 0.98); snout relatively long, rounded in dorsal view and in lateral profile, slightly longer than wide; canthus rostralis hardly distinct, straight between eye and nostril; loreal region oblique; nostrils rounded, directed anterodorsally and slightly laterally; situated much closer to tip of snout and to eye, separated from each other by distance larger than distance between eye and nostril (IN/EN 1.15); eye directed anterolaterally, strongly protruding, very large (ED/HL 0.41), its diameter shorter than snout (ED/SL 0.84); interorbital distance much wider than upper eyelid and wider than internarial distance (IO/IN 1.21); tympanum covered by skin, not visible externally; upper jaw with dentition; teeth on premaxilla larger than teeth on maxilla; choanae small, located far anterolaterally at margins of roof of mouth, its anterior edge covered by maxillary bone, therefore appearing semicircular in ventral view; vomer ridges and teeth absent; tongue short and moderately broad, bilobed for about one-sixth of its length, free distally for about half its length; densely covered with minute papillae; median lingual process absent.

Dorsal surfaces of head, trunk, and limbs and lateral surfaces of trunk finely shagreened; minute pointed, widely scattered tubercles on dorsum, more numerous posteriorly than anteriorly; supratympanic fold absent; small, subcircular, elevated glandular area in tympanic region posterior to eye and rear end of mandible, bearing large tubercles with pointed keratinous tips; ventral side of head smooth; vocal sac present; gular gland of vocal sac smooth, large and wide, covering about 70 percent of throat width ( Fig. 8B ); chest smooth, abdomen weakly areolate; ventral side of limbs smooth; short transverse fold above vent.

Forelimbs slender;hand large (HND/SVL 0.32); tips of fingers enlarged into large disks, each with circummarginal groove; relative length of fingers: I <II <IV <III; subarticular tubercles well developed, numbering one on Fingers I and II, two on Fingers III and IV, proximal tubercles on Fingers III and IV and tubercles on Fingers I and II singular, rounded; distal tubercles on Fingers III and IV indistinctly bipartite; webbing formula of the hand I 2+/2.25 II 2/3+ III 2.75/2.25 IV; thenar tubercle oval, small and low, about one-fourth length of metacarpal of Finger I; palmar tubercles indiscernible.

Hind limbs slender, moderately long; heel reaching to level of eye when legs adpressed forwardly to body; crus moderately long (TibL/SVL 0.48), about as long as thigh; heels meeting each other when knees flexed and thighs held perpendicularly to median plane; foot subequal in length to crus (FoL/TibL 0.96); relative length of toes: I <II <III <V <IV; toe tips rounded, enlarged into large disks, each with circummarginal groove; subarticular tubercles singular, numbering one on Toes I and II, two on Toes III and V, and three on Toe IV; pedal webbing formula I 2/2.25 II 1.5/3- III 1.75/3 IV 3-/1.75 V ( Fig. 8C ); inner metatarsal tubercle moderately prominent, elongated, about twothirds length of metatarsus of Toe I; outer metatarsal tubercle small, rounded.

Coloration in life. During night, skin on dorsal side of head, trunk, forelimbs, crus and tarsus light yellowishbrown with more or less regular dark brown speckling; indistinct darker brown transverse stripe between upper eyelids; large dark brown, irregularly shaped spot in scapula region, two less distinct, somewhat lighter brown, irregularly shaped spots at level of anterior end of pelvis, separated from each other by half their width; cloacal region with dark brown mottling; dorsal skin of thigh largely unpigmented with only a broad stripe of widely scattered brown pigmentation; weak brown stripe along canthus, continuing behind eye on anterior half of trunk on both sides; tubercles below eye, and in tympanic region at rear end of jaw white; indistinct dark brown stripe running diagonally on middle of tibia, forming interrupted, inverted U-shaped band together with pelvic spots when legs folded against body; ventral side of head, trunk and limbs largely unpigmented and translucent; gular gland bright yellow; fingers and toes yellow ( Fig. 7A ). During day, basic dorsal coloration brighter, very light brown to bright cream-colored; dark brown dorsal speckles, spots and stripes in more pronounced contrast to basic coloration, more distinctly visible ( Fig. 7B ).

Coloration in preservative. Dorsal basic coloration largely faded to yellowish white; darker dorsal pattern elements light to dark brown, clearly visible; yellow color of gular gland, fingers and toes faded to white ( Fig. 8A–C ).

Variation. The paratypes match the holotype in general appearance, proportions, coloration and color pattern. Mensural variation within the species is shown in Table 1. Pedal webbing variation is I 2+[100]/2.5[90],2.25[10] II 2[50],2+[40],2.25[10]/3[10],3+[40],3.5[50] III 1.75 [80],2-[20]/3[100] IV 3 -[40],3[60]/1.75[100] V.

Bioacoustics. Series of advertisement calls of six different males were recorded at the following ambient temperatures: 10.9°C (N = 1), 13.6°C (N = 3), and 16.2°C (N = 2). The advertisement call consisted of five to six, rarely four pulse groups (notes) ( Fig. 9 ). Depending on the ambient temperature, notes were repeated at a rate of 7.1–10.0/s (10.9°C), 8.2–11.7/s (13.6°C), and 10.2–11.4/s (16.2°C). The highest repetition rate was always between the first three notes of a series, the lowest at the end of the series. Each note consisted of 10–11 pulses ( Fig. 9 ). Probably due to echo effects, pulsation was often veiled in the waveforms, especially towards the end of the note. Pulse repetition rate varied from 190–210/s at 10.9°C, 222–250/s at 13.6°C, and 277–292/s at 16.2°C, resulting in a note length of 72–94 ms, 55–70 ms, and 36–50 ms, respectively. Amplitude modulation was prominent within individual notes ( Fig. 9 ). Total call length showed linear temperature dependence and varied from 388–397 ms at 16.2°C, 472–499 ms at 13.6°C, and 572–620 ms at 10.9°C for five-note calls ( Fig. 10 ). Energy maximum showed linear temperature dependence, with 3020–3150 Hz at 10.9°C, 3370–3550 Hz at 13.6°C, and 3660–3810 Hz at 16.2°C ( Figs. 9–10 ). There was no marked frequency modulation. Prominent harmonics were at about 6000–7000 Hz and 9000–11000 Hz ( Fig. 9 ).

Ecology and natural history. We collected males and females in swamps in forest openings, or at forest edges ( Fig. 11A ). Males were found calling above standing bodies of water with thick lower vegetation cover. In Gishwati Forest and Kamiranzovu Swamp in Nyungwe Forest, the species was found calling in syntopy with Hyperolius castaneus and H. discodactylus . One adult male (UTEP 20802) from Kahuzi-Biega National Park ( DRC) was found 3.5 meters above ground in montane forest. Tadpoles are unknown. Laurent (1955, 1983) listed the species from bushes in montane forest. Laurent (1982) noted that, in general, the species is common in the foliage of shrubs in dense forests. He also recorded it in banana trees in a deep valley (Nyungwe, Rwanda) and “des trous de prospection” (i.e., prospecting holes likely for gold mining, Upper Lubitshako, Kabobo Plateau, DRC).

Etymology. The species epithet derives from the Greek noun φάντασμα (phántasma), meaning ghost or phantom, in allusion to the coloration and general appearance of the new species. The epithet is used as an invariable noun in apposition.

Distribution and conservation. The occurrence of the species has been confirmed for several locations in western Rwanda (Nyungwe and Gishwati Forest) and eastern DRC (in and near Kahuzi-Biega National Park, Itombwe Plateau and Kabobo Plateau [ Laurent 1982], Fig. 5 ). We expect the species to be eventually found in the AR of southwestern Uganda and northwestern Burundi. So far, the species has been recorded from only a narrow elevation range between 1962 m (Kamiranzovu Swamp, Rwanda) and ca. 2400 m (May ya Moto [and possibly Luemba], Itombwe Plateau, Laurent 1982). Given the relatively limited overall geographic distribution of the species with an estimated extent of occurrence of 19,088 km 2 ( Fig. 5 ), an estimated area of occupancy of 52 km 2 (both calculated with GeoCAT; Bachman et al. 2011), the detection of the amphibian chytrid fungus in one adult male (UTEP 20791, Greenbaum et al. 2015), and the conservation challenges facing natural areas of the AR ( Greenbaum 2017; Ayebare et al. 2018), we categorize this species as Vulnerable under the IUCN Red List criteria ( IUCN 2021).

Figures

FIGURE 5. Distribution map of Afrixalus phantasma sp. nov. (black symbols) and A. lacustris sp. nov. (white symbols). Star, triangle, and circle symbols represent holotype, examined specimens, and literature records (Drewes & Vindum 1994; Laurent 1950, 1952, 1972, 1982; Vonesh 2001), respectively. Areas shaded in lighter gray are below 1700 meters, whereas areas shaded in darker gray are 1700 meters or higher. Lakes are shown in white. Gray triangle symbol represents A. lacustris specimens (RMCA 77-020-B-133–136) from a problematic locality at Tubutubu, Itombwe Plateau, DRC; see species account for details. B = Burundi, R = Rwanda.

FIGURE 7. Photos of Afrixalus phantasma sp. nov. in life. Adult male holotype, ZFMK 103454 (field no. JMD 723), from Gishwati-Mukura National Park, Rwanda, in the habitat showing nighttime coloration (A), adult male paratype, ZFMK 103460 (field no. JMD 679) from Kamiranzovu Swamp, Nyungwe National Park, showing daytime coloration in dorsal (B) and ventral views (C), adult male paratype UTEP 20802 (EBG 1198) from Kahuzi-Biega National Park, DRC (D), photographed the morning after capture.

FIGURE 8. Photos of the preserved holotype of Afrixalus phantasma sp. nov. (ZFMK 103454) in dorsal (A) and ventral (B) views (to scale), and plantar view of the left foot (C). Photos of the preserved holotype of A. lacustris sp. nov. (UTEP 20805) in dorsal (D) and ventral (E) views (to scale), and plantar view of the left foot (F).

FIGURE 9. Audiospectrogram (top) and corresponding waveform (bottom) of a five-note advertisement call of a paratype (ZFMK 103459) of Afrixalus phantasma sp. nov. recorded on 11 March 2011 at Kamiranzovu swamp, Nyungwe National Park, Rwanda.

FIGURE 10. Total call length (diamonds; five-note advertisement calls only) and energy maximum of dominant frequency (triangles) of the advertisement call of Afrixalus phantasma sp. nov. at varying ambient temperatures.

FIGURE 11. Photos of the habitat of (A) Afrixalus phantasma sp. nov. in Kamiranzovu Swamp, Nyungwe National Park, Rwanda, showing a forest edge in a montane marsh, and (B) A. lacustris sp. nov. from the vicinity of Kalundu, DRC, showing transitional forest.