Common name

Hughes, Daniel F., Kusamba, Chifundera, Behangana, Mathias & Greenbaum, Eli, 2017, Integrative taxonomy of the Central African forest chameleon, Kinyongia adolfifriderici (Sauria: Chamaeleonidae), reveals underestimated species diversity in the Albertine Rift, Zoological Journal of the Linnean Society 181, pp. 400-438 : 418-423

Common name : Tolley’s forest chameleon.

Holotype: UTEP 21490 (field no. ELI 2755 ), adult female, UGANDA, Western Region, Kigezi sub-region, Kabale District, Bwindi Impenetrable National Park , near Ruhija village , 01°2′54.096″S 29°46′36.624″E, 2284 m elevation, 26 May 2014, collected at night from natural vegetation along a roadside near Institute for Tropical Forest Conservation ( ITFC) by C. Kusamba, M.M. Aristote and W.M. Muninga ( Fig. 8E).

Paratopotypes: Same collection details as holotype, two adult females, UTEP 21486 (field no. ELI 2754 ) and UTEP 21487 [field no. ELI 2788 (28 May 2014)], collected at night from forest edges c. 3 m above ground along a road to ITFC, and one adult male, UTEP 21488 (field no. ELI 2756 ), collected at night with aid of stick from c. 5 m above ground in sleeping perch of tree behind ITFC (main office) by D.F. Hughes, K.A. Tolley, S. Davies and A.A. Turner .

Paratype: One adult male, UTEP 21489 (field no. ELI 2827 ), UGANDA, Western Region, Rwenzururu sub-region, Kasese District, near Rwenzori Mountains National Park , Ruboni village , 00°20′58.992″N 30°1′47.028″E, 1655 m elevation, 31 May 2014, collected at dusk from c. 3 m above ground in sleeping perch of vegetation (secondary forest) in front of the Ruboni Community Hotel by D.F. Hughes, E. Greenbaum and M. Behangana .

Referred specimens: One adult female [ CAS 176920 (field no. JVV-1367)], UGANDA, Western Region, Kigezi sub-region, Kabale District, Bwindi Impenetrable National Park , Mubwindi Swamp , c. 120 m south of swamp, 2133 m elevation, 01°4′12″S, 29°45′0″E, 9 December 1990, collected c. 60 cm above ground on fern by J.P. O’Brien and J. V . Vindum . Three adult females [ CAS 201593–95 (field nos. JVV-4058–59, 4577)], UGANDA, Western Region, Kigezi sub-region, Kabale District, Bwindi Impenetrable National Park , ITFC near Ruhija village , 2362 m elevation, 1°2′47.8″S, 29°46′28.5″E, 12 September 1996 ( CAS 201593–94 ) and 18 October 1996 ( CAS 201595 ), collected at night c. 3 m above ground on road-cut vegetation ( CAS 201593–94 ) and c. 2 m above ground in bush ( CAS 201595 ) by J. V . Vindum ( CAS 201593–94 ), and R . C. Drewes and J. V . Vindum ( CAS 201595 ) .

Diagnosis: Kinyongia tolleyae sp. nov. can be distinguished from all other Kinyongia species by the following combination of traits: (1) lack of rostro-nasal ornamentation in both sexes; (2) moderate body size (mean SVL = 56.6 mm); (3) anterior dorsal keel with 5–10 conical tubercles; (4) casque slightly elevated above the nape; (5) two smooth, expanded areas present on the casque that appear bilobed when viewed from above; (6) absence of both a gular and ventral crest; (7) 13–17 upper and 14–16 lower labials; (8) tail length longer than SVL in both sexes; (9) parietal crest with several slightly raised tubercles that fork towards the snout; (10) background coloration of the body in adult females is generally light green to yellow-green; background coloration of the body in adult males is generally light brown with anteriorly positioned green patches and peach speckling near the head; (11) large dark brown patches with white centres are present on the lateral flanks of adult females and these lateral patches are typically oriented with a larger patch positioned anteriorly and sometimes a second smaller patch positioned posteriorly from mid-body; (12) areas of darker brown pigment cover the cloacal region and extend distally onto hidden parts of the hind limbs and tail in adult females; (13) interstitial skin between the tubercles on the body is generally white and sometimes green for both sexes; (14) a brown stripe passes through the middle of the eye and extends from the canthal ridge to the temporal crest, and the eye skin above and below the stripe is powder blue/teal, gradually dissipating dorsally and ventrally; (15) the top of the head is somewhat darker green than elsewhere; (16) gular region and ventral portions of the body are distinctly off-white.

Differential diagnosis: A medium-sized forest chameleon that is distinguished from most other congeners by the absence of a rostral process in both sexes ( K. asheorum , K. boehmei , K. carpenteri , K. fischeri , K. magomberae , K. matschiei , K. msuyae , K. multituberculata , K. oxyrhina , K. tavetana , K. tenuis , K. uluguruensis , K. uthmoelleri , K. vanheygeni , K. vosseleri and K. xenorhina ). The new species can be distinguished from K. adolfifriderici by its larger snout length and more upper (13–17 vs. 10–14) and lower (14–16 vs. 12–15) labials. The new species can be distinguished from K. rugegensis sp. nov. by the presence of two distinctly expanded and smooth portions of the upper casque (bilobed appearance), slightly smaller head width, fewer upper labials (13–17 vs. 16–18), and smaller fleshy papillae medial to rotulae on hemipenis. The new species can be distinguished from K. itombwensis sp. nov. by its larger snout length, slightly larger forelimbs and casque–eye distance and generally more conical tubercles on the dorsal crest (5–10 vs. 6–7). The new species can be distinguished from K. mulyai and K. excubitor by the presence of a dorsal crest with 5–10 conical tubercles and marked mitochondrial sequence divergence. The new species can be distinguished from K. gyrolepis by a smaller mean body size (56.6 mm vs. 67.3 mm) and current distribution in moist Afromontane rainforest.

Genetic differentiation and variation: Summary of pairwise sequence divergence for each molecular marker (16S, ND2 and RAG 1) among individuals of K. tolleyae sp. nov. and other species of Kinyongia endemic to the AR are presented in Table S2. For the ND2 locus, p -distances among K. tolleyae sp. nov. samples ranged from 0.0 to 1.4%.

Description of holotype: Adult female, SVL 52.9 mm and TL 75.6 mm. Four rounded ovarian follicles present (see Reproduction in the following text). Casque slightly elevated above nape. Posterior apex of casque present, overhanging nape. Two distinct expanded areas of flattened tubercles present on top of casque, bilobed appearance. Neck distinct from head. Parietal crest consists of four discrete, enlarged tubercles extending posteriorly as a ridge to apex of casque. Supra-orbital ridges mostly smooth and one larger conical tubercle near dorsal posterior margin of orbit present. Temporal crest consists of three enlarged tubercles extending posteriorly from mid-eye and ascending posteriorly along ridge of casque to apex. Nares open laterally and posteriorly. Canthal ridge consists of five raised tubercles descending from eye towards snout. Fifteen upper and 16 lower labials present along tip of snout to posterior margin of orbit. No gular or ventral crests present. Nine raised conical tubercles present on anterior portion of dorsal crest, absent near mid-body. Tail and lateral flanks smooth. Body covered in nearly homogenous, flattened tubercles. Some larger polygonal tubercles present dorsally on flanks. Rosette patches of smaller tubercles on ventral portion of body. Mostly enlarged flattened tubercles present on outer portions of limbs. Claws typical of Kinyongia species.

Coloration of holotype (in ethanol): Photographs of the body and head detail of the holotype (in preservative) are presented in Fig. 10. The background coloration is various shades of blue with darker grey-blue areas covering some dorsal parts of the body and tail. The venter, beginning below the nape and extending near the cloacal region, is a pink to off-white coloration. Patches of lighter blues are present behind the eye, near commissure of the mouth, side and top of the casque, sides of the tail and parts of the hind limbs. A large portion, about midway on the tail, is off-white. The axillary and inguinal regions are lighter blue-green than elsewhere on the body. The soles of the feet are yellowish-white.

Coloration of holotype (in life): A photograph of the holotype (in life) is presented in Fig. 8E. The following description is based on colour photographs of the holotype, which were taken when the animal was in a slightly defensive display with overall darker body colour ( Fig. 8E). See Diagnosis of K. tolleyae sp. nov. for description of more normal coloration, and see photos of other individuals in various physiological states ( Fig. 8). The top of the head is covered in dark brown tubercles with black interstitium. The head is lighter in colour beginning below the temporal crest to canthal ridge, and covered in light brown and yellowish-green tubercles with off-white interstitium. At mid-eye, there is a dark brown lateral stripe that connects the coloration on the canthal ridge to the temporal crest. The eye skin is dark brown and resembles that of the top of head. Labial scales are heterogeneous in colour with hues of red. The gular region is off-white, and this coloration extends across the venter and parts of the tail. Areas of darker brown pigment cover the cloacal region, hidden parts of the hind limbs and part of the tail. Area below jaw on gular is peach colour. The background coloration of the body is greenish-brown with off-white to green interstitium. The ventral flanks are adorned with a large dark patch of coloration, positioned slightly anterior from mid-body. The centre of the patch is lighter than the black edges, and almost orange in colour. Several faint dark brown vertical bands begin on the dorsal keel and quickly fade ventrally, not to reach mid-body. Smaller body tubercles form rosettes, with light green colour filling spaces between tubercles. Tubercles near axillary and inguinal regions, and hidden parts of the limbs, are white with flecks of green. The dorsal crest is ornamented with darker tubercles than elsewhere and this pattern extends onto the tail. The posterior third of the tail is darker green than the rest of the tail, and faint vertical dark brown bands are present, especially towards the distal end of the tail.

Hemipenis: Hemipenal drawings and description are based on specimen UTEP 21488. Line drawings depicting the general hemipenis morphology of K. tolleyae sp. nov. are presented in sulcal and lateral views ( Fig. 7B). The hemipenis of this new species is very similar to that of K. rugegensis sp. nov., except that it possesses smaller fleshy papillae medial to each large rotulae. See Hemipenis of K. rugegensis sp. nov. for description of hemipenis morphology.

Variation: Descriptive morphometrics of K. tolleyae sp. nov. are presented in Table 5 and a summary of mean measurements in Table 3. Chameleon photographs displaying colour variation in life are presented in Fig. 8. Morphological proportions in paratopotypes and paratypes are generally consistent with those in the holotype. Males and females have similarly sized tails [M: 65.0 ± 1.1 (64.2–65.8 mm, n = 2); F: 70.7 ± 5.9 (64.0– 75.6 mm, n = 7)] (P> 0.05), but males have smaller body sizes [M: 50.1 ± 2.2 (48.5–51.6 mm, n = 2); F: 58.4 ± 4.9 (51.5–66.2 mm, n = 7)] (P = 0.03). Males have overall brown background coloration with green pigmented patches anteriorly, in contrast to the light green background coloration of females, which are largely devoid of brown pigment. Females possess a dark patch (sometimes two) of coloration on the lateral flanks of the body with a lighter centre, whereas males do not possess this feature. When agitated, the lateral patches, eye skin and dorsal region of the head became dark ( Fig. 8E).

Reproduction: The female holotype ( UTEP 21490) with SVL 52.9 mm and TL 75.6 mm collected on 26 May 2014 was in the early stages of folliculogenesis. This individual contained four slightly enlarged ovarian follicles (completely rounded) with mean diameter (in mm) 5.22 ± 0.22 (5.03–5.52). Exact follicular measurements were as follows: 5.25 W; 5.03 W; 5.52 W; 5.09 W. This individual had moderate fat bodies. A female paratopotype ( UTEP 21487 ) with SVL 60.0 mm and TL 75.4 mm collected on 28 May 2014 was gravid. This individual contained five oviductal (shelled) eggs with mean dimensions (in mm), length 14.05 ± 0.33 (range: 13.75–14.44) and width 7.46 ± 0.1 (range: 7.32–7.59). Exact measurements of eggs were as follows: 14.44 L × 7.59 W; 14.38 L × 7.44 W; 13.88 L × 7.32 W; 13.82 L × 7.51 W; 13.75 L × 7.45 W. This individual had minor fat bodies. A paratopotype ( UTEP 21486 ) with a smaller body size ( SVL 51.5 mm and TL 64.3 mm) collected on 28 May 2014 was not gravid, as evidenced by the largest ovarian follicles measuring <2 mm in diameter and lacking yolk. This individual had extensive fat bodies. Two other paratopotype females ( CAS 201593 – SVL 59.5 mm and TL 64.8 mm; CAS 201594 – SVL 59.9 mm and TL 75.6 mm) collected on 12 September 1996 were gravid. Clutch characteristics were not measured for these individuals. From a small sample, the temporal incidence of gravidity in females at Bwindi Impenetrable National Park seems to correspond with the two annual peaks in precipitation for this region (i.e. March–May and October–November), which is a common phenomenon among chameleon species ( Tilbury, 2010). We speculate that egg production may not occur during only one rainy period per year or females may produce two clutches per year. More investigation with a larger sample is warranted to determine the seasonal reproductive cycle for females of this new species .

All males had darkly pigmented testes (i.e. black coloration). All collected males were sexually mature. One male paratopotype ( UTEP 21488 ) with SVL 48.5 mm and TL 64.2 mm collected on 26 May 2014 had enlarged testes. The right testis of this individual measured 6.24 mm in length and 4.91 mm in width. This individual had minor fat bodies. A male paratype ( UTEP 21489 ) with SVL 51.6 mm and TL 65.8 mm collected on 31 May 2014 also had enlarged testes. The right testis of this individual measured 6.65 mm in length and 4.93 mm in width. Fat bodies for this individual were moderate .

Diet: Three specimens examined for gut contents had identifiable remains of arthropod prey items, one specimen had an empty stomach ( UTEP 21487) and one specimen had only a bolus of unidentifiable remains surrounded by a white mucus membrane ( UTEP 21488). The stomach of one female ( UTEP 21490) contained Mantodea, Araneae , Hymenoptera, Diptera, Hemiptera and Coleoptera. A second female ( UTEP 21486) stomach contained Araneae and Hymenoptera . A male ( UTEP 21489) stomach contained Diptera.

Distribution and natural history: Kinyongia tolleyae sp. nov. is found in moist Afrotemperate montane and sub-montane forests at an elevation range from 1655 to 2362 m. Most specimens were collected from forest edges within Bwindi Impenetrable National Park. Several specimens were found on sleeping perches relatively high in the canopy (c. 5 m above ground) and some were found lower (c. 2 m above ground). One specimen ( UTEP 21489) was collected from secondary forest on disturbed vegetation (c. 2.5 m above ground) near the Ruboni Community Hotel just outside of Rwenzori Mountains National Park. The presence of this species at two disjunct mountain blocks suggests a recent forest connection between these areas and increases the likelihood that this species is more widespread than currently known. For example, Vonesh (2001) recorded Chamaeleo (= Kinyongia ) adolfifriderici from Kibale National Park in Uganda, which is less than 50 km from Rwenzori Mountains National Park, and thus the observation was potentially this new species. We speculate that K. tolleyae sp. nov. may also occur in other montane protected areas with suitable forest habitat near these two sites (e.g. forest reserves contiguous with Queen Elizabeth National Park and Mgahinga Gorilla National Park). Both collected males seemed sexually mature, and four female specimens were gravid. To the best of our knowledge, no juveniles have been detected to date. Behaviour and activity patterns are basically unknown, but likely similar to that of K. adolfifriderici ( Tilbury, 2010) . Intersexual interactions were observed among a few specimens before preservation. When a male was placed in the presence of two females, male body colour became milky white, regions on the head greener, powder-blue eye skin became much more striking and distinct diamond patterns suddenly

*Enlarged ovarian follicles present in body cavity of specimen. Eggs and CTD were not evaluated for CAS specimens.

formed on the tail. Whereas female background colour turned a rich green, ventral portions of the body became noticeably whiter and the lateral body patches became marked with a brown hue at the edges and the centre became a purer white ( Fig 8D). For a detailed list of lizard species present at the type locality, see Drewes & Vindum (1998). Other species collected from Rwenzori Mountains National Park comprised typical AR lizard fauna and some endemic species, including Adolfus jacksoni , Kinyongia carpenteri , K. xenorhina , Leptosiaphos meleagris , Rhampholeon boulengeri , Trioceros ellioti , T. johnstoni and T. rudis .

Conservation: Bwindi Impenetrable National Park and Rwenzori Mountains National Park are wellestablished members of the protected area network in the AR. These areas constitute some of the few remaining portions of intact Afromontane forests in the Kigezi Highlands. Nevertheless, these forests face similar anthropogenic threats to other protected areas across the region. The current range of K. tolleyae sp. nov. falls within the boundaries of these two protected areas and we suspect it may be present in nearby protected areas with suitable habitat.

Etymology: The specific epithet is named in honour of Krystal A. Tolley for her substantial contributions to chameleon biology, with the Latin suffix – ae to denote feminine genitive singular. To date, Krystal has participated in the description of 12 new chameleon species, published copious primary research articles on chameleons covering a remarkable breadth of subjects and coauthored (or edited) two important books on chameleons ( Tolley & Burger, 2007; Tolley & Herrel, 2013).