Arthroleptis nyungwensis, Dehling, 2023

Dehling, J. Maximilian, 2023, A New Miniature Species of Arthroleptis (Anura: Arthroleptidae) from Nyungwe National Park, Rwanda, Diversity 15 (1104), pp. 1-16 : 3-11

publication ID	https://doi.org/ 10.3390/d15101104
DOI	https://doi.org/10.5281/zenodo.10165918
persistent identifier	https://treatment.plazi.org/id/03D95A2C-FFAB-DA4C-FE4B-845CFD173E02
treatment provided by	Julia
scientific name	Arthroleptis nyungwensis
status	sp. nov.

Treatment

Arthroleptis nyungwensis sp. nov.

Nyungwe Squeaker

urn:lsid:zoobank.org:act:E8F25561-AD7C-46D8-9107-73F6ED10799C

Arthroleptis sp. — Dehling & Sinsch 2023: 13 [17].

Holotype: ZFMK 104075 , adult male, from a small stream near Rukuzi (2.4635 S, 29.2293 E; 2200 m), Nyungwe National Park , Western Province, Rwanda, collected on 17 September 2014 by J. M. Dehling GoogleMaps .

Paratypes: ZFMK 104076 , adult male, from the type locality, collected in March 2013 by J.M. Dehling; GoogleMaps ZFMK 104077 , adult male, from Cyamudongo Forest (2.546 S, 28.989 E, about 2000 m), Western Province, Rwanda, collected 21 October 2018 by J.M. Dehling GoogleMaps ; SMNS 15743 and GoogleMaps 15744 , two subadult males, from the edge of Cyamudongo Forest (2.5378 S, 29.9942 E; 1830 m), Western Province, Rwanda, collected 14 June 2014 by J.M. Dehling GoogleMaps .

Referred material: JMD 599 , adult male, from the Kamiranzovu Waterfall Trail , appr. 1800 m a.s.l., Nyungwe National Park , Western Province, Rwanda, collected 25 September 2010 by J. M. Dehling .

Diagnosis: The species is assigned to the genus Arthroleptis for exhibiting the following morphological characteristics [28]: pedal webbing absent, median dorsal skin raphe present, third finger elongate in adult males, dermal spines present on third finger. The new species differs from all other members of the genus by the combination of the following characteristics: small size ( SVL of adult males 16.0– 16.5 mm); dorsal surfaces of head, trunk, and limbs and lateral surfaces of trunk finely shagreened; tympanum well visible externally; median lingual process absent; legs long, tibiotarsal joint reaching to eye; tibiofibular length equal to foot length; tip of third finger and tips of toes slightly enlarged; inner metatarsal tubercle very small and rounded, outer metatarsal tubercle absent; ventral colour reddish to orange with two slightly concave longitudinal yellow stripes and white dots; advertisement call consisting of single note, lasting 17.4 ± 6.4 [11–32] ms and dominant frequency at 5861 ± 188 [5531–6029] Hz; sequence of the 16S rRNA gene differing from available homologous sequences of other species by uncorrected p-distance of at least 4.6%.

Description of the holotype: Measurements of the holotype are provided in Table 1 View Table 1 . Very small (SVL 16.5 mm) adult male; body slender, widest at temporal region, slightly tapering to groin ( Figure 1A,B View Figure 1 ); limbs slender; head large (HL/SVL 0.37, HW/SVL 0.33), longer than wide (HW/HL 0.89); snout moderately long (SL/HL 0.41), wider than long (SL/EE 0.79); rostral tip rounded in both dorsal view and lateral view; canthus rostralis moderately distinct, straight between eye and nostril; loreal region oblique; nostrils rounded, directed laterally, situated about halfway between eye and tip of snout (EN/NS 0.97), separated from each other by distance much larger than distance between eye and nostril (NN/EN 1.68); eye directed anterolaterally, hardly protruding, projecting just beyond margins of head in dorsal view, relatively large (ED/HL 0.35), its diameter shorter than snout (ED/SL 0.84); dorsal surface of eye lids slightly above dorsal surface of head in lateral view; interorbital distance much wider than upper eyelid (IO/EW 1.61) and smaller than internarial distance (IO/NN 0.89); tympanum well visible externally, its annulus well defined; upper jaw with dentition; teeth on premaxilla larger than teeth on maxilla; choanae small, rounded, located far anterolaterally at anterolateral margin of roof of mouth, completely covered by maxillary bone, not visible in ventral view; vomer ridges and teeth absent; tongue long and moderately broad, posteriorly expanded, hardly bilobed, free distally for about two-thirds its length; median lingual process absent.

Dorsal surfaces of head, trunk, and limbs and lateral surfaces of trunk finely shagreened ( Figure 1 A View Figure 1 ); median skin raphe barely visible on dorsal side in preservative, only discernible on head surface; supratympanic region smooth with no dermal fold; ventral side of head smooth; vocal sac present; chest and anterior part of abdomen smooth, posterior part of abdomen weakly areolate; ventral side of limbs smooth ( Figure 1 B View Figure 1 ); short transverse fold above vent.

Forelimbs slender; hand small, but with very long third finger ( HND / SVL 0.42); few keratinous spines along lateral sides of third finger; tips of fingers not enlarged into small disc, except slightly in Finger III; relative length of fingers: I <IV <II <III; subarticular tubercles well developed, numbering one on Fingers I and II, three on Finger III and two on Finger 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; fingers without webbing; thenar tubercle small, low and oval; inner palmar tubercle large, low, and rounded, outer palmar tubercle absent.

Hind limbs slender, moderately long; heel reaching to level of eye when legs adpressed forwardly to body; crus moderately long ( TFL / SVL 0.42), slightly shorter than thigh ( TFL / THL 0.94); foot length about equal to crus length ( FOL / TFL 1.03); relative length of toes: I <II <VI <III <IV; toe tips slightly enlarged into small disks; subarticular tubercles singular, numbering one on Toes I and II, two on Toes III and V, and three on Toe IV; toes without webbing; inner metatarsal tubercle small, rounded and moderately prominent, about one-third length of metatarsus of Toe I; outer metatarsal tubercle indiscernible.

Colouration in life. Dorsal basic colouration light brown. Slightly darker brown pattern on head and trunk hardly discernible, consisting of dark transversal interorbital bar and faint broad longitudinal band along spine ( Figure 1 A View Figure 1 ). Top of head anterior to interorbital bar lighter brown. Dark brown stripe in straight line along ventral part of canthus rostralis from tip of snout to anterior edge of eye, continued downwardly curved from posterior edge of eye almost to arm insertion, just touching the posterodorsal edge of tympanum ( Figure 1 A View Figure 1 ). Lateral sides of head and trunk lighter, greyish to yellowish brown; dorsal side of upper arms and hands yellowish brown. Sides of head and forearm loosely, flanks more or less regularly and densely scattered with small white dots ( Figure 1 A View Figure 1 ). Base colour of ventral side yellowish brown with tiny dark brown speckles, most densely on ventral side of head; ventral side of head along the jaw and ventral parts of forelimbs darker reddish brown; ventral parts of leg and lateral sides of thigh dark red ( Figure 1 B View Figure 1 ); abdomen yellowish brown with two bright yellow longitudinal, slightly concave stripes, faintly merging with each other at posterior end ( Figure 1 B View Figure 1 ); small white dots on ventral side, few on forearm and thigh, densely on lateral sides of abdomen, around cloaca and on tarsus; irregularly shaped yellow flecks on abdomen ( Figure 1 B View Figure 1 ).

Colouration in preservative. Dorsal basic colouration faded to greyish brown. Darker greyish brown dorsal pattern more conspicuous than in life. Ventral colour faded to uniformly yellowish creme-coloured. Dark brown speckling more conspicuous than in life. Yellow colour pattern indiscernible.

Variation. The adult male paratypes match the male holotype in general appearance, proportions, colouration, and colour pattern. Mensural variation within the species is shown in Table 1 View Table 1 . The dorsal colour pattern was more conspicuous in life in one of the adult males ( JMD 599) and in the subadults ( Figure 1 C, E View Figure 1 ). In the subadult specimens, the sides of the head and the flanks were dark grey in life and there was a black stripe running in a straight line from the nostril to the anterior edge of the eye and slightly ventrally curved from the posterior edge of the eye above the tympanum to the level of the arm insertion; the venter was light yellow in the centre, darkening to dark yellow then orange on the edges, without the conspicuous yellow stripes ( Figure 1 E, F View Figure 1 ).

Bioacoustics. Series of advertisement calls of the holotype, two paratypes, another collected and two uncollected males were recorded at different ambient temperatures between 12 ◦ C and 20 ◦ C. Males called from the leaf litter on the forest floor during both night and day. The most-often-emitted vocalisation was a single note ( Figure 2 A View Figure 2 ), and I regard this as the advertisement call. The call was repeated in series at irregular intervals of 2.5– 8.8 s. In most recordings, the note appeared unpulsed or diffusely pulsatile, but in a few instances, two separate pulses were visible ( Figure 2 A View Figure 2 ). The note had a total duration of 17.4 ± 6.4 [11–32] ms ( N = 5 males). Individual pulses, when traceable, were separated by an interval of 1 ms duration and had an individual duration of 7 ms (first pulse) and 5 ms (second pulse ( Figure 2 A View Figure 2 ). There was no measurable frequency modulation in shorter notes of less than 20 ms and dominant frequency was at 5861 ± 188 [5531–6029] Hz. A fundamental was present at about 2950 Hz, and harmonics were present at 9000, 12,000, 15,000, and 18,000 Hz ( Figure 2 A View Figure 2 ). Prevalent bandwidth was 5400–6300 Hz. In a few longer notes of more than 30 ms, the dominant frequency increased from 5404 ± 30 [5383–5426] Hz in the first third of the note to 5598 Hz in the last third of the note.

One of the paratypes ( ZFMK 104077) was collected while duetting with another uncollected male. The two males emitted a second call type ( Figure 2 B, C View Figure 2 ). It was impossible to differentiate between the two males in the recording, and therefore the following description is based on all recorded calls. The second call type likewise contained a prominent last note lasting 21.4 ± 10.1 [11–39] ms with the dominant frequency increasing from 5175 ± 197 [4866–5469] Hz in the first third of the note to 5480 ± 130 [5167–5727] Hz in the last third of the note ( Figure 2 B, C View Figure 2 ). However, the main note was always initiated by a note group that had a much lower amplitude and was separated from the main note by an interval of 90.1 ± 13.6 [71–113] ms. The composition of the note group varied considerably. In about half of the recorded calls, it consisted of an uninterrupted series of 1–13 notes ( Figure 2 B View Figure 2 ), in the other half, two or three subgroups, each consisting of 1–3 notes, were separated from each other by intervals of 37.3 ± 22.1 [19–86] ms. As calls with both interrupted and uninterrupted pulse groups were recorded in quick succession, these differences were not attributable to the two different calling individuals. Individual notes within the (sub)groups were repeated at a rate of 58.6 ± 4.9 [47.6–62.5] per second, were weakly pulsatile, and had a duration of 8.8 ± 3.3 [4–14] ms. Amplitude increased from the first to the last note of the group ( Figure 2 B, C View Figure 2 ), going along with an increase in dominant frequency from 4658 ± 323 [4177–5124] Hz in the first note to 4944 ± 210 [4608–5254] Hz in the last note ( Figure 2 B, C View Figure 2 ). Whereas the interrupted and uninterrupted note groups sounded like a trill, in one case, two widely separated initial notes had a relatively high amplitude, giving the impression that the main note was rapidly repeated ( Figure 2 C View Figure 2 ). Total duration of the second call type was 209.1 ± 40.2 [139–285] ms.

On the same recording, a third call type was identified. It had been recorded a total of three times and was a brief whistle that consisted of a single pulsatile note, lasting 40, 44 and 74 ms. The dominant frequency was markedly modulated, increasing from 3760 ± 108 [3660–3875] Hz in the first third to 4205 ± 25 [4177–4220] Hz in the last third ( Figure 2 D View Figure 2 ).

Habitat and natural history: Calling males were observed in moist leaf litter of closed-canopy montane forest between 1800 and 2200 m a.s.l. Subadults were found at the forest edge in Cyamudongo Forest. The species is active at both night and day. The reproduction is unknown, but the species is suspected to deposit eggs in moist leaf litter and to undergo direct development without a tadpole stage.

Etymology: The species is named after Nyungwe Forest in southern Rwanda.

Distribution and Conservation: Despite intensive surveys in Nyungwe Forest and elsewhere in Rwanda [17,29], the species is currently known from only a few localities in the western part of Nyungwe Forest and in Cyamudongo Forest ( Figure 3 View Figure 3 ). I propose the species to be classified as “Near Threatened” according to the criteria established by the International Union for Conservation of Nature ( IUCN) [7] in both the global Red List and the Rwandan national Red List [17].

Phylogenetic relationships: The phylogenetic tree resulting from the ML analysis was well supported by nonparametric bootstrap values ( Figure 4 View Figure 4 ). All samples of Arthroleptis nyungwensis formed a clade that was weakly supported as being sister to a clade containing two deeply divergent clades assigned to A. schubotzi , one from Rwanda ( A. schubotzi A), the other from Bwindi, Uganda ( A. schubotzi B). The three clades are all from montane forests in the central and northern Albertine Rift. They were sister to a clade containing A. xenodactyloides and A. xenochirus ( Figure 4 View Figure 4 ), two species that are distributed from Angola to southern DRC, southern Tanzania and northwards to Kenya. Another sequence assigned to Arthroleptis xenodactyloides was resolved as sister to all aforementioned clades, suggesting that the identification of the source specimens of these three latter sequences need to be revised. The third Rwandan species, A. adolfifriederici , is only distantly related to A. nyungwensis and A. schubotzi and appears to be most closely related to A. tanneri from the Usambara Mountains in Tanzania ( Figure 4 View Figure 4 ). The samples of A. nyungwensis differed from each other by 0.00–0.54% and from samples of all other species by at least 4.6% in uncorrected p-distance. Samples of A. schubotzi A from Rwanda differed from the sample of A. schubotzi B from Uganda by 5.6%.

Morphological comparison: The very small size ( SVL of adult males 16.0– 16.5 mm) distinguishes A. nyungwensis sp. nov. from the other species in the wider region that are larger, i.e., A. adolfifriederici : males 27.6–32.0 mm; A. francei Loveridge, 1953 : male 32 mm; A. phrynoides (Laurent, 1976) : male 20.4 mm; A. reichei Nieden, 1911 : males to 30 mm; A. schubotzi : males 19.9–21.2 mm (including Schoutedenella discodactyla Laurent, 1954 with males 17.5–19 mm); A. spinalis Boulenger, 1919 : male 21.4 mm; A. stenodactylus Pfeffer, 1893 : males to 33 mm; A. xenochirus Boulenger, 1905 (including Schoutedenella globosa de Witte, 1921 as well as A. lameeri de Witte, 1921 and Schoutedenella muta de Witte, 1933 ; see also [5]): males with enlarged third finger 16.5–24 mm; A. xenodactylus Boulenger, 1909 : males to 26 mm; A. xenodactyloides Hewitt, 1933 : males to 25 mm. The very small inner metatarsal tubercle distinguishes the new species from all remaining species with large, elongate, prominent inner metatarsal tubercle that is about two-thirds the length of the first metatarsus, i.e., A. loveridgei de Witte, 1933 (also outer palmar tubercle present, ventral side of thigh coarsely granular, discs of toes strongly enlarged vs. outer palmar tubercle absent, thigh smooth, discs of toes slightly enlarged); A. sylvaticus ( Laurent, 1954) (also discs of toes strongly enlarged vs. slightly enlarged); and A. xenochirus Boulenger, 1905 (also venter uniformly off-white, throat grey in males vs. venter reddish to orange with longitudinal yellow stripes and white dots, throat yellowish brown with tiny dark brown speckles). Arthroleptis fichika Blackburn, 2009 and A. kidogo Blackburn, 2009 are known only from females that are much smaller ( SVL 13.5–14.2 mm and 13.9–14.1 mm, respectively) than the new species, and differ in having a dappled ventral colour pattern [7].

Morphological differentiation between the similarly sized species of Arthroleptis from the Albertine Rift is hampered by the shortage of external diagnostic characters, especially in preserved specimens, in combination with the briefness of the original descriptions that specify only a handful of characteristics, some of which are not diagnostic. In addition, the whereabouts and the identity of the types of several species described by Laurent [3,16] are currently vague. The life colouration can be a useful character to easily distinguish between species if it is thoroughly documented. The distributional range of Arthroleptis nyungwensis sp. nov. overlaps with that of A. schubotzi in western Rwanda, although the two species are usually found in different habitats. The Rwandan specimens match the types of A. schubotzi and the types of its junior synonym Schoutedenella kivuensis de Witte, 1941 , very well. Arthroleptis schubotzi (males 19.9–21.2 mm, male syntype of S. kivuensis 19.8 mm; females 21.1–21.6 mm; female holotype currently 19.2 mm, previously measured 21 mm [13] and 20 mm [20], female syntype of S. kivuensis 20.6 mm) is significantly larger than A. nyungwensis sp. nov. (males 16.0– 16.5 mm), has relatively shorter legs ( TFL / SVL 0.36–0.41 vs. 0.42–0.46 in A. nyungwensis ), a relatively larger tympanum ( TD / EYE in adult males>0.60 vs. <0.48), a relatively shorter head ( HL / SVL 0.31–0.33 vs. 0.35–0.37), and its dorsum is granular, covered with small, low tubercles, especially in males ( Figure 5 View Figure 5 ; vs. dorsum finely shagreened). It is most easily distinguished from A. nyungwensis sp. nov. (venter reddish to orange with longitudinal yellow stripes and white dots, Figure 1 View Figure 1 ) by its conspicuous ventral pattern consisting of an off-white background with dark reticulation, with the ventral side of the head having a higher proportion of dark pattern than the breast and abdomen in females and the gular region of males being black with few whitish flecks, and bright red thighs ( Figure 5 View Figure 5 ). This colour pattern was also described in the female holotype of A. schubotzi [20] and described and depicted for the types of Schoutedenella kivuensis [15]. There are a number of similarly sized, but poorly defined taxa from eastern DRC that are only known from the type series [3,16] and whose taxonomic status is doubtful. A very similar ventral colour pattern to A. schubotzi is present in the types of Arthroleptis mossoensis ( Laurent, 1954) , Schoutedenella discodactyla (currently considered a junior synonym of A. schubotzi ) and A. pyrrhoscelis Laurent, 1952 , and these taxa are readily distinguished from A. nyungwensis sp. nov.: Arthroleptis mossoensis was described from Murugaragara, Mosso, Territoire de Rutana, Burundi, at an altitude of 1200 m, based on a single female ( SVL 22.4 mm) that remains the only specimen of the species ever collected. It further differs from A. nyungwensis sp. nov. in its short hindlimbs ( TFL / SVL 0.36 vs. 0.42–0.46), the tibio-tarsal articulation only reaching the shoulder (vs. reaching the eye). Arthroleptis pyrrhoscelis from the Kabobo Plateau in eastern DRC is similar in size (male types 15.1–16.2 mm) to A. nyungwensis sp. nov., but has shorter hindlimbs, the tibiotarsal joint reaching only to tympanum (vs. to eye). The posterior part of the abdomen and the ventral side of the thighs are coarsely granular (vs. weakly areolate), an outer palmar tubercle and several prominent metacarpal tubercles are present (vs. absent), and the inner metatarsal tubercle is large, elongate and prominent (vs. small and rounded). Schoutedenella discodactyla from Lutunguru in the North Kivu Province of DRC (currently referred to A. schubotzi ) differs by its markedly dilated discs of fingers and toes (vs. tip of third finger only and tips of toes slightly enlarged). Arthroleptis vercammeni ( Laurent, 1954) from Mwana in eastern DRC is a very small species ( SVL of males 13–15 mm, of females 15–17 mm [3]) and thus even smaller than A. nyungwensis sp. nov. (males 16.0– 16.5 mm), the throat is blackish in males (vs. yellowish brown with tiny dark brown speckles), the tibia is noticeably longer than the foot ( TFL / FOT 1.10–1.25 vs. 0.97–1.03 in A. nyungwensis ), and the tips of fingers and toes are clearly dilated [3] (vs. tip of third finger only and tips of toes slightly enlarged). Arthroleptis hematogaster ( Laurent, 1954) is a poorly known species from the South Kivu Province in eastern DRC. The species is similar in size (only known male 16.5 mm), but is reported to have a uniform ventral colouration varying from orange-red to blood-red [3] (vs. yellowish brown) and lacks the distinct two longitudinal yellow ventral stripes and the white dots on venter, arms and thighs that are present in A. nyungwensis sp. nov., the foot is relatively shorter with FOL/SVL 0.38–0.41 (vs. 0.43–0.45), and finger tips and toe tips are strongly enlarged (vs. slightly enlarged).

Bioacoustic comparison: The advertisement calls of only about half the species of Arthroleptis are known [1]. The advertisement call of Arthroleptis nyungwensis sp. nov. (single note, 17.4 ± 6.4 [11–32] ms duration, dominant frequency at 5861 ± 188 [5531–6029] Hz; Figure 2 View Figure 2 ) differs from all described calls of its congeners. The call of one of the two other species of Arthroleptis recorded from Rwanda, A. adolfifriederici , is similar in consisting of a single, brief (52–65 ms) note, but has a much lower dominant frequency of about 2900 Hz [17]. The known advertisement calls of the phylogenetically closely related species differ markedly from the call of A. nyungwensis sp. nov., i.e., A. xenochirus : high-pitched trill, seven notes, repeated at a rate of 15/s, dominant frequency at 4600 Hz [22]; A. xenodactylus : brief whistle, duration 50 ms, repeated two or three times per second, dominant frequency at 6400–7000 Hz [22]; A. xenodactyloides : single note, 88–95 ms, repeated at an interval of 340–390 ms, composed of three pulses, each lasting 16–24 ms, dominant frequency at 6300–6500 ms [30]; brief, cricket-like chirp, consisting of three brief clicks, dominant frequency at 5500 Hz [22]; call duration 0.05– 0.1 s, repeated every 0.3– 0.7 s, dominant frequency 5.2–6.4 kHz, 2–4 pulses [31].

Based on observations of males of its junior synonym Schoutedenella kivuensis , the call of A. schubotzi has been described onomatopoeically as “cri-cri, cri-cri” and characterized as “extremely piercing and very characteristic cry, absolutely similar to that of S. globosa ” [= A. xenochirus ], “quite comparable to the ‘song’ of our cricket, but much louder” [15]. This was subsequently cited as a “harsh series of double chirps” [1,22]. The call description agrees with the results of the analysis of call recordings of A. schubotzi from Rwanda [17]: call duration 246–429 ms, 5–6 notes, each lasting 23–29 ms and composed of three pulses, internote interval 34–40 ms, dominant frequency 4331–4450 Hz. The advertisement call of males assigned to A. schubotzi from Kibale National Park, Uganda, differs from the advertisement call of Rwandan specimens in consisting of only either two or three notes, the first two being separated from each other by an interval of 80 [59–98] ms, the second and third by an interval of 94 [84–113] ms; in having a slightly higher dominant frequency of 4661 [4462–4892] Hz; and in a briefer call duration of 158 [92–273] ms [32]. The advertisement calls of both populations assigned to A. schubotzi differ from the advertisement call of A. nyungwensis .