Afrixalus lacustris Greenbaum, Dehling, 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 : 218-223

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

Great Lakes Spiny Reed Frog urn:lsid:zoobank.org:act:41D3C41A-4501-4BEC-BFB6-B9C6C1518DC3

Afrixalus laevis (nec Megalixalus laevis Ahl 1930 )— Laurent 1950: 24; 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. UTEP 20805 (field no. ELI 605 ), adult male, from the vicinity of Kalundu (03.15552° S, 28.42108° E, 1482 m), South Kivu Province, DRC, collected on 21 December 2010 by Chifundera Kusamba and Félix I. Alonda ( Figs. 8D–F , 12A–B ).

Paratopotype. UTEP 20806 (field no. ELI 606 ) , adult male, collected with the holotype.

Referred specimens. Specimens with an asterisk were not included in morphological analyses due to poor quality of preservation, lack of a voucher, or unavailability of specimen(s): UTEP 20807–08 (field nos. ELI 644 , 649 ), vicinity of Kalundu (03.15552° S, 28.42108° E, 1482 m), South Kivu Province, DRC ; UTEP 20809 , 22422 (field nos. ELI 669–70 ), Baraka , near shore of Lake Tanganyika (04.10832° S, 29.09705° E, 777 m), South Kivu Province, DRC ; UTEP 20810–11 (field nos. EBG 1316 , 1319 ), vicinity of Irangi (01.8873° S, 28.4495° E, 820 m), South Kivu Province, DRC ; UTEP 22423 (field no. MUSE 10192 ), Kahuzi-Biega National Park , Nanwa (02.362138° S, 28.192589° E, 1566 m), South Kivu Province, DRC ; UTEP 22424 (field no. MUSE 10137 ), Itombwe Plateau , Mbandakila (03.47937° S, 28.413049° E, 1135 m), South Kivu Province, DRC ; RMCA 77-020 -B-133–136* (four specimens), Itombwe Plateau , Tubutubu (2300 m), South Kivu Province, DRC ; RMCA 77-020 -B-89–92 (field nos. MF 14–15 [two specimens]), Kitutu (ca. 03.28° S, 28.11° E, 700 m), South Kivu Province, DRC ; RMCA 77-020 - B-0069–71 (1 specimen), Itula (ca. 03.27° S, 28.12° E, 650 m), South Kivu Province, DRC ; RMCA 77-020 -B-0081–83, 77-20-B-0086, Kamituga (ca. 03.54° S, 27.69° E, 1050 m), South Kivu Province, DRC ; RMCA 77-020 - B-0072–73 (1 specimen), Mwana (ca. 03.15° S, 28.47° E, 1650 m), South Kivu Province, DRC ; UTEP 22417 (field no. CRSN 2773 ), Toyokana (02.02734° N, 030.06653° E, 1294 m), Ituri Province, DRC; (field no. EPLU 395 *, photo and tissue only) , ca. 0.5 km E of Epulu, near Mt. Mbiya (01.39594° N, 28.58093° E, 755 m), Ituri Province, DRC ; UTEP 22416 (field no. DFH 247 ), Bwindi Impenetrable National Park , Buhoma (00.99045° S, 29.61884° E, 1523 m), Western Region, Uganda; (field nos. DFH 1102–03 * photos and tissues only) , Kibale Forest National Park , Ngogo Research Center (00.49795° N, 30.42262° E, 1363 m), Western Region, Uganda ; CAS 202032–36 , Bwindi Impenetrable National Park , Buhoma rd., 2 km S (by rd.) of Bizenga River (01.00975° S, 29.620694° E), Western Region, Uganda ; CAS 202133 , Bwindi Impenetrable National Park , small tributary to Ishasha River (00.905° S, 29.704972° E, 1280 m), Western Region, Uganda ; CAS 202109 , Bwindi Impenetrable National Park , Bizenga River at Buhoma rd. (00.99275° S, 29.615722° E), Western Region, Uganda ; CAS 256035 *, Bwindi Impenetrable National Park , rd. north of Ruhija, Western Region, Uganda ; CAS 256128–31 *, Mabira Forest Reserve , marshy area adjacent to unpolluted stream (0.4508° N, 32.9493° E, 1121 m), Mukono District, Central Region, Uganda .

Diagnosis. The species is referred to the genus Afrixalus for 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 18.9–22.2 mm, in females 20.8–25.7 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. fulvovittatus (males 23–27 mm, females 25–28 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, females 32–35 mm), A. paradorsalis (males 28–34 mm, females 32–35 mm), A. septentrionalis (males 19–21 mm), A. vittiger (males 22–25 mm, females 25–28 mm), and A. wittei (males 27–30 mm, females 29–33 mm); and larger size than A. delicatus (males 15–19 mm, females 17–22 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 showing 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 ). It is most similar to A. phantasma sp. nov. but differs from this species in being smaller (Table 1) and showing an overall darker coloration and more contrasting dorsal pattern that is obvious even in preserved specimens ( Figs. 7–8 , 12 ). It is readily distinguished from A. phantasma sp. nov. by the more extensive hand and toe webbing ( Fig. 8E–F ).

Description of holotype. Measurements of the holotype are provided in Table 2 . Body very slender, widest at temporal region, slightly tapering to groin ( Fig. 8D–F ); head small (HL/SVL 0.31, HW/SVL 0.31), about as long as wide (HW/HL 0.99); snout relatively long, rounded in dorsal view and in lateral profile, slightly wider than long; canthus rostralis hardly discernible, slightly concave between eye and nostril in dorsal view; loreal region oblique; nostrils rounded, directed anterolaterally and slightly dorsally; situated much closer to tip of snout and to eye, separated from each other by distance about equal to distance between eye and nostril (IN/EN 1.02); eye directed anterolaterally, strongly protruding, very large (ED/HL 0.39), its diameter shorter than snout (ED/SL 0.90); interorbital distance much wider than upper eyelid (IO/EW 1.61) and wider than internarial distance (IO/IN 1.31); 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 heartshaped, longer than broad, bilobed for about one-fourth of its length, free distally for about two-thirds 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; tiny pointed, widely scattered tubercles on dorsum, more numerous posteriorly than anteriorly; supratympanic fold absent; few tubercles at rear end of mandible without pointed 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. 8E ); chest smooth, abdomen weakly areolate; ventral side of limbs smooth; short transverse fold above vent.

Forelimbs slender; hand large (HaL/SVL 0.28); 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 II 2-/3- III 2.25/2 IV; thenar tubercle oval, small and very low, about one-fourth length of metacarpal of Finger I; inner palmar tubercle and outer palmar tubercle very low, small, rounded, almost indiscernible.

Hind limbs slender, moderately long; heel reaching to level of eye when legs adpressed forwardly to body; crus moderately long (TibL/SVL 0.44), slightly shorter than thigh; heels not touching each other when knees flexed and thighs held perpendicularly to median plane; foot subequal in length to crus (FoL/TibL 0.94); 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 1.5/2+ II 1+/2+ III 1+/2+ IV 2/1+ V ( Fig. 8E ); inner metatarsal tubercle moderately prominent, elongated, about half 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 brown with more or less regular, locally more densely clustered dark brown speckling; distinct dark brown transverse stripe between upper eyelids, another less distinct one in scapula region, and another narrow one at level of anterior end of pelvis; dorsal skin of thigh largely unpigmented with only a broad stripe of widely scattered brown pigmentation; distinct dark brown band along canthus, continuing behind eye on both sides of trunk to level of pelvis; tubercles below eye and in tympanic region at rear end of jaw white; dark brown stripe running diagonally on middle of tibia, forming interrupted, inverted U-shaped band together with pelvic spots when legs folded against body; skin of ventral side of head, trunk and limbs largely unpigmented and translucent; gular gland bright yellow; fingers and toes yellow ( Fig. 12 ). During day, basic dorsal coloration light brown; dark brown dorsal speckles, spots and stripes in more pronounced contrast to basic coloration, more distinctly visible.

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

Variation. The paratypes match the holotype in general appearance and proportions. Coloration and color pattern varies from light-cream to yellowish-orange with a few relatively large and darker blotches and vermiculation, light speckling and indistinct dorsolateral stripe to an almost reticulated pattern of contrasting bright and dark elements with a broad and conspicuous brown dorsolateral band ( Fig. 12 ). Pedal webbing variation is I 1.5[100]/2+[100] II 1+[100]/2+[100] III 1 +[50],1.25[50]/2+[100] IV 2 [100]/1+[100] V.

Bioacoustics. The advertisement call and other vocalizations are unknown.

Ecology and natural history. We collected males and females in swamps in forest openings and near forest edges ( Fig. 11B ), from vegetation at the edge of streams (or on vegetation overhanging them) in forest, and from non-forest vegetation near the shore of Lake Tanganyika. Egg deposition has not been observed and tadpoles are unknown. An adult male (CAS 256035) was found in Bwindi Impenetrable National Park ( Uganda) ca. 2 m above ground in a tree fern “either calling or moving to a calling site (similar to ‘running’ of Kassina )” (D. Blackburn, in litt., 22 July 2021). Laurent (1955) noted the species from transitional forest. In his paper on amphibians of Virunga National Park, Laurent (1972) noted the species is most commonly found in swamps with herbaceous vegetation in secondary forest, and more rarely, in primary forest. Laurent (1982) noted that, in general, the species is common in the foliage of shrubs in dense forests. He also recorded it from “une mare sombre” (i.e., a dark pond) in syntopy with Chiromantis at Kitutu ( DRC), marshes where it reproduces by sticking its eggs under the leaves of fountain grass ( Pennisetum, Shabunda , DRC), a shaded bank of a pond in syntopy with Hyperolius “ tuberculatus ” (likely H. hutsebauti sensu Bell et al. 2017 ) and H. frontalis ; the center of this pond had reeds harboring H. kivuensis and Afrixalus orophilus (Shabunda, DRC). Laurent (1983:352) listed the species (along with Phrynobatrachus petropedetoides and Hyperolius frontalis ) from “shadowy puddles of the thick transition forest.”

Etymology. The species epithet is the Latin adjective “ lacustris ,” meaning belonging to or dwelling in lakes; in allusion to the distribution of the new species in the region of the African Great Lakes.

Distribution and conservation. The species is distributed from lowland rainforest of the Congo Basin at 460 m (Omaniundu, DRC, Laurent 1982) to transitional forests of the Albertine Rift at 1650 m (Mwana, DRC) and east as far as Mabira Forest, Uganda (1121 m). As shown in Figure 5 , the species has a relatively large distribution, including several national parks and protected areas (e.g., Virunga National Park, Bwindi Impenetrable National Park), and thus is not likely to be threatened based on a limited distribution. Using GeoCAT, its extent of occurrence is estimated as 409,238 km ² and its area of occupancy as 160 km ² ( Bachman et al. 2011). We therefore classify this species as Least Concern according to the IUCN Red List criteria ( IUCN 2021).

Four specimens (RMCA 77-020-B-133–136) from Tubutubu, Itombwe Plateau (2300 m) are problematic because they are morphologically consistent with A. lacustris , but they were collected from a substantially higher elevation than all other known specimens. Coordinates for Tubutubu provided by RMCA (4° S, 28.933° E) suggest the locality is east of the highest point of the plateau at an elevation of about 1400 m on Google Earth. Although it is possible that the specimens were collected at the latter elevation, Laurent (1982) mentions bamboo forest as the habitat, which usually occurs at the highest elevations of the Itombwe Plateau ( Doumenge 1998). No clarity is offered by Laurent (1964), because he does not mention any Afrixalus in his study of the ecology and distribution of amphibians of the Itombwe Plateau. Given this conflicting information, we do not include the Tubutubu specimens in our current understanding of the elevational distribution of A. lacustris (see gray triangle in Fig. 5 ).

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 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.

FIGURE 12. Photos of Afrixalus lacustris sp. nov. in life. Adult male holotype (UTEP 20805), from the vicinity of Kalundu (03.15552° S, 28.42108° E, 1482 m), South Kivu Province, DRC in dorsal (A) and (B) ventral views, adult female (UTEP 20809) from Baraka, near shore of Lake Tanganyika, South Kivu Province, DRC (C), adult female (EPLU 395) from Epulu, Ituri Province, DRC (D), adult male (UTEP 22417) from Toyokana, Ituri Province, DRC (E), individual of unknown sex (DFH 1102) from Ngogo Research Center, Kibale Forest National Park, Western Region, Uganda (F). All photos taken the morning after capture.