Rhampholeon nalubaale, Hughes & Behangana & Lukwago & Menegon & Dehling & Wagner & Tilbury & South & Kusamba & Greenbaum, 2024

Hughes, Daniel F., Behangana, Mathias, Lukwago, Wilber, Menegon, Michele, Dehling, J. Maximilian, Wagner, Philipp, Tilbury, Colin R., South, Trisan, Kusamba, Chifundera & Greenbaum, Eli, 2024, Taxonomy of the Rhampholeon boulengeri Complex (Sauria: Chamaeleonidae): Five New Species from Central Africa’s Albertine Rift, Zootaxa 5458 (4), pp. 451-494 : 469-474

Rhampholeon nalubaale sp. nov. Hughes, Behangana, Lukwago, Kusamba, and Greenbaum

Goddess pygmy chameleon urn:lsid:zoobank.org:act:F997E4A5-298C-4137-9528-BF9A4DD04E3A

Synonymy.

Rhampholeon boulengeri — Schmidt 1919, de Witte 1965 (partim), Vonesh 2001, Kvift 2011, Tolley et al. 2013 (partim), Tilbury & Tolley 2015 (partim), Spawls et al. 2018 (partim), Tilbury 2018 (partim)

Rhampholeon sp. 2 — Hughes et al. 2018

Etymology. The specific epithet is derived from the Luganda word, nalubaale , which means a spirit of feminine qualities (i.e., goddess), and is also the name for Lake Victoria ( Kenny 1977).

Holotype. UTEP 22673 (field no. DFH 585 ), adult female, UGANDA, Western Region, Bunyoro sub-region, Masindi District, Budongo Central Forest Reserve , 01.72992° N, 31.55535° E, 1124 m elevation, 2 July 2015, collected by D.F. Hughes, W. Lukwago, and M. Behangana at night from forest vegetation about 1 m above the ground ( Fig. 10A ).

Paratype (topotype). Same collection details as holotype, two adult females, UTEP 22671–22672 (field nos. DFH 583–584 ) ( Fig. 10B–C ) .

Paratypes. Three adult females, UTEP 21693–21694 , 22670 (field nos. DFH 558–560 ), UGANDA, Western Region, Bunyoro sub-region, Masindi District, Budongo Central Forest Reserve , Sonso River , 01.71885° N, 31.54095° E, 1073 m elevation, 1 July 2015, collected by D.F. Hughes and W. Lukwago at night from forest vegetation about 1 m above the ground ( Fig. 10D ) .

Referred specimens. UTEP 21695–21697 (field nos. ELI 464–465 , EBG 2737 ) , UTEP 22744–22747 (field nos. ELI 466 , 479–481 ), DRC, South Kivu Province, Bizombo (03.02880° S, 28.28243° E, 1132 m elevation) (7 specimens) ( Fig. 10F ) . UTEP 21700 (field no. DFH 1101 ) and CAS 204371 (field no. JRV 450 ), UGANDA, Western Region, Kibale National Park, Ngogo , 00.49795° N, 30.42262° E, 1363 m elevation ( UTEP 21700 [ Fig. 10E ]), and Kanyawara, 00.56666° N, 30.35000° E, 1506 m elevation ( CAS 204371 ) (2 specimens) . UTEP 21691–21692 (field nos. CRSN HERP 2833 , 2837 ), DRC, Ituri Province, Bongobongo , 02.19766° N, 30.11468° E, 1258 m elevation (2 specimens) . UTEP 21698–21699 (field nos. MUSE 10178 , 10589 ), DRC, South Kivu Province, Kahuzi-Biega National Park, Ikundwe , 02.57567° S, 28.16142° E, 1137 m elevation ( UTEP 21698 ), and Kyasa, 01.75368° S, 27.61806° E, 975 m elevation ( UTEP 21699 ) (2 specimens) .

Diagnosis. Rhampholeon nalubaale sp. nov. is in the subgenus Rhinodigitum because of its distinctly bicuspid claws, prominent rostral process, smooth plantar surfaces, and phylogenetic placement, thus easily distinguishing it from the six species in the other two subgenera (i.e., Rhampholeon and Bicuspis ): R. gorongosae , R. marshalli , R. spectrum , R. spinosus , R. temporalis , and R. viridis . Rhampholeon nalubaale sp. nov. can be distinguished from all other Rhampholeon species by the following combination of traits: (1) lack of prominent mite pockets in the inguinal region distinguishes it from R. beraduccii , R. platyceps , R. chapmanorum , R. maspictus , R. tilburyi , R. bruessoworum , and R. nebulauctor ; (2) presence of prominent mite pockets in the axillary region distinguishes it from R. nchisiensis and R. acuminatus ; (3) distinct supra-orbital and canthal crests distinguishes it from R. hattinghi ; (4) geographic restriction in the Albertine Rift distinguishes it from R. uluguruensis , R. moyeri , R. colemani , R. sabini , R. rubeho , R. nicolai , R. waynelotteri , and R. princeeai ; (5) larger inter-limb length in females, genetic divergence, and non-overlapping elevational range at parapatric sites distinguishes it from R. boulengeri ; (6) larger mean body size, larger eye diameters, longer mouth, snout, inter-limb, and hind limb lengths in females distinguishes it from R. monteslunae sp. nov.; (7) slightly longer head, snout, and mouth lengths, and shorter inter-limb length in females distinguishes it from R. plumptrei sp. nov.; (8) slightly longer head, snout, and mouth lengths, larger eye diameters, and longer inter-limb and hind limb lengths in females distinguishes it from R. bombayi sp. nov.; (9) longer inter-limb, hind limb, and head lengths in females distinguishes it from R. msitugrabensis sp. nov.

Genetic differentiation and variation. A summary of pairwise sequence divergence for three DNA markers (16S, ND2, and RAG-1) among individuals of R. nalubaale sp. nov. and other Rhampholeon species is presented in Supplementary Material 1.

Description of holotype (UTEP 22673). Adult female, SVL 48.9 mm and TL 10.8 mm. Gravid (see Reproduction below). Body shape leaf-like. Casque flattened, with short head. Neck indistinct from head. Supra-orbital crests distinct with cluster of tubercles connected by a ridge with 14 tubercles across casque and 19 tubercles from peak-to-peak of crests. Rostral process 1.78 mm, composed of elongated tubercles. Temporal crest discrete with several enlarged tubercles extending posteriorly from mid-eye. Nares open in a posterior orientation. Canthal ridge consists of raised tubercles, one raised higher than others near snout. Ninety-eight upper and 94 lower labial tubercles present along tip of snout to rictus of mouth. Body covered in nearly homogenous, flattened tubercles. Crenulated dorsal crest, more prominent from mid-body to nape. Many enlarged conical tubercles present on limbs, tail, and lower dorsal flanks. Claws markedly bicuspid.

Coloration of holotype (in life). A photograph of the holotype is presented in Figure 10A . Background color tan with a yellow-orange hue. Top of head a whitish coloration. Head generally light tan and indistinct from body. Gular region white, which extends onto ventral area. One diagonal dark red line extends from near dorsal crest posteriorly to lateral flank with second line posterior, but faint. Tail a similar tan color as body. Several large tubercles on body and limbs white, especially towards ventral area. Largest body tubercle near neck dark brown. Limbs slightly darker brown color than body. Several light orange and yellow patches on body, especially along dorsal crest and near forelimb-nape region.

Variation. A summary of descriptive morphometrics for R. nalubaale sp. nov. is presented in Table 3 , comparative boxplots in Figure 4 , and measurements of the type specimens in Table 6 . Photographs displaying color variation in life are presented in Figure 10 . Morphological proportions are generally consistent with those of the holotype. Only females have been found. Relatively large species (mean SVL 49.4 mm, range 39.3–56.2 mm, n = 19) with a prominent rostral process (mean 1.5 mm, range 1.0– 1.9 mm, n = 19). Body coloration is consistently brown to tan, usually with red-orange hues. Most exhibited one, sometimes two, dark brown to red lines on the lateral flanks that extended diagonally from the dorsal crest toward the hind limbs, resembling veins of a leaf.

Reproduction. Five females were gravid ( UTEP 21691 , UTEP 21692 , UTEP 21698 , UTEP 22672 , and UTEP 22673 [holotype]). Gravid females had a mean SVL of 52.9 mm (48.9–56.2 mm) and a mean TL of 12.2 mm (10.8– 13.8 mm). These females were collected in January (n = 2) and July (n = 3). One female had a clutch size of 3 eggs ( Fig. 10B ). The smallest specimen examined ( UTEP 21694 ) was collected on 1 July 2015 with SVL 39.3 mm and TL 10.8 mm from Budongo Central Forest Reserve , Uganda.

Distribution, natural history, and conservation. Rhampholeon nalubaale sp. nov. is found in sub-montane forests at an elevation range from 513–1506 m. Specimens have been collected from Kibale National Park and Budongo Central Forest Reserve in Uganda, and Kahuzi-Biega National Park and Itombwe Natural Reserve in DRC. Vonesh (2001) recorded this species from Kibale National Park, where he found it to be the most commonly observed chameleon species relative to T. ituriensis and K. tolleyae , and was most often found on low shrubs. Extensive mark-recapture chameleon surveys in October 2018 by one of us (DFH) in Kibale National Park near Kanyawara Research Station across seven nights found just four females sleeping at a mean perch height of 375 mm (range 254–508 mm) and a mean perch diameter of 2.94 mm (range 1.79–4.67 mm). One female was gravid, and no individuals were recaptured across the seven consecutive survey nights. In fact, T. ituriensis was found to be much more common than R. nalubaale sp. nov. during those surveys with 33 individuals captured 42 times compared to the four individuals captured each once for the pygmy chameleon. We examined a specimen (UTEP 22673) under ultraviolet light and found that its facial tubercles fluoresced blue ( Fig. 11 ), indicating that they are of bony origin. Prötzel et al. (2018) found that this phenomenon of bone fluorescence is actually widespread in Chamaeleonidae , especially in species that live in forested habitats with relatively higher levels of ambient ultraviolet light. It is currently thought that chameleons that possess this trait have co-opted bone fluorescence for signaling between individuals ( Prötzel et al. 2018). We note that this is the first published account of fluorescence in the genus Rhampholeon , and while we did not examine other species under ultraviolet light, this has been observed in several other species of Rhampholeon (K.A. Tolley, pers. comm.); thus, we anticipate that most species in the genus will also exhibit this trait. The current range of R. nalubaale sp. nov. falls within the boundaries of at least two national parks and we suspect it may be present in other protected areas with suitable lowland forest habitat across the region. Budongo Central Forest Reserve and Itombwe Natural Reserve are also protected, but subjected to greater anthropogenic pressure relative to the national parks because they both allow some level of human use of the forests (Kujirakwinja et al. 2018; Lukwago et al. 2020) and law enforcement in the latter reserve is weak ( Greenbaum & Kusamba 2012; EG, pers. obs.).

Schmidt (1919) inspected a large collection of R. boulengeri from the Ituri Forest, DRC, housed at the American Museum of Natural History (AMNH), New York, which he noted were “all, curiously, females.” The collection included 61 specimens from Medje (Haut-Uele Province) and two specimens from Poko (Bas-Uele Province), both low-elevation villages in DRC. Based on Schmidt’s (1919) collection, Hall (1970) speculated that R. boulengeri (sensu lato) was a possible case of parthenogenesis in Chamaeleonidae , and to corroborate, he examined specimens at the Museum of Comparative Zoology (MCZ), Harvard. Hall (1970) examined at least four specimens (MCZ Herp R-53983–53986) from a different site in the Ituri Forest (Mayala [513 m elevation]) collected by C.J.P. Ionides and, by exposing their gonads, he found that these specimens were all females. We also concluded that these four specimens were females based recent photographs taken by the current collections manager at the MCZ, who likewise indicated that they are all females based on visual inspections of the specimens (S. Kennedy-Gold, pers. comm.). Hall (1970) also discussed other specimens in the MCZ collected from Central Africa that included males, such as those from Ja River and Kribi, Cameroon, and also from Idjwi Island, DRC. The Cameroonian specimens cannot be R. boulengeri because it is now restricted to the Albertine Rift, and thus they would be R. spectrum . The three Idjwi Island specimens (MCZ Herp R-47297–47299) were collected by Arthur Loveridge in 1939 and included at least one male (48 mm SVL and 16 mm TL) and one gravid female (47 mm SVL and 14 mm TL with 3 eggs) ( Loveridge 1942). A photograph of one of these specimens is provided by Loveridge (1942: Plate 5, Figure 1 ), which is clearly a male based on its long tail with an obvious hemipenal bulge. According to Loveridge (1944), the specimens collected on Idjwi Island were taken from near the Upper Mulinga River around 1981 m elevation. Based on the elevation at the collecting site and body sizes presented in Loveridge (1942), these Idjwi Island specimens would likely represent a different member of the R. boulengeri complex, probably R. bombayi sp. nov., as this species occurs in the region at other high-elevation sites where numerous males have been collected. Ultimately, Hall (1970) did not rule out parthenogenesis in R. boulengeri (sensu lato) because males possessed “greatly enlarged hemipenal swellings and much longer tails,” and thus he deemed sex-determination errors by Schmidt (1919) highly unlikely. Later, Kearney et al. (2009) dismissed the possibility of parthenogenesis in R. boulengeri (sensu lato) because the evidence of a sex-ratio bias was considered too weak, and no further evidence had come to light since Hall (1970).

Our findings for R. nalubaale sp. nov., where only females have been in collections from numerous lowland sites across the region (see Fig. 2 ; Table 3 ), nonetheless, extends Schmidt’s (1919) observation from the villages of Medje (715 m elevation) and Poko (634 m elevation). In contrast, at least two males have been found for all other species of the complex (see Tables 1–2 ), and for some species, just as many males have been collected as females, such as R. plumptrei sp. nov. Moreover, the level of intraspecific genetic divergence among samples of R. nalubaale sp. nov. was negligible to non-existent, even across vast geographic scales (some samples are separated by> 600 km straight-line distance), and was much lower than the ranges among samples of any other member of the R. boulengeri complex (excluding R. boulengeri [sensu stricto] with only four samples that have been sequenced from the same time and place). For example, using the most variable locus of Hughes et al. (2018), ND2, the range of intraspecific variation for R. nalubaale sp. nov. was 0.1–0.3% (n = 10), whereas the ranges for the other new species were much larger, especially for those species with comparably large geographic ranges: R. plumptrei sp. nov. (0.1–3.4%, n = 14), R. bombayi sp. nov. (0.1–4.4%, n = 12), R. msitugrabensis sp. nov. (2%, n = 2), and R. monteslunae sp. nov. (0.1–1.1%, n = 7).

Figures

FIGURE 1. Bayesian phylogeny of the Rhampholeon boulengeri complex from the Albertine Rift, CentralAfrica, adapted from Figure 4 of Hughes et al. (2018). Posterior probabilities ≥ 95% are denoted by filled circles adjacent to nodes.

FIGURE 2. Map of theAlbertine Rift, CentralAfrica, showing sampling localities for specimens of the Rhampholeon boulengeri complex examined in this study. For clarity, we show color-coded circles that indicate the number of specimens examined from that general locality. Underlined numbers indicate that a specimen from that area also included genetic data analyzed in Hughes et al. (2018). Two specimens (UTEP 21704–21705) from DRC not shown (see text for details). For a detailed map of localities representing R. boulengeri (sensu lato) see Tilbury (2018). The color scheme corresponds to clades of the species complex and is retained throughout all figures: Green = Rhampholeon sp. Itombwe (R. boulengeri); pink = Rhampholeon sp. 1 (R. plumptrei sp. nov.); blue = Rhampholeon sp. 2 (R. nalubaale sp. nov.); yellow = Rhampholeon sp. 3 (R. bombayi sp. nov.); purple = Rhampholeon sp. 4 (R. msitugrabensis sp. nov.); red = Rhampholeon sp. 5 (R. monteslunae sp. nov.).

FIGURE 4. Box plots showing variation in external traits of the Rhampholeon boulengeri complex from the Albertine Rift, Central Africa. Sample sizes for each species are denoted in the bottom right quarter. Males and females are separated to show degree of sexual-size dimorphism across members of the complex. All measurements are in mm. Plots show the median, 1st and 3rd quartiles, minimum and maximum inter-quartile ranges, and outliers. Refer to text for description of the linear measurements.

FIGURE 10. Photographs of various individuals of Rhampholeon nalubaale sp. nov. in life. (A)—Adult female holotype (UTEP 22673) from Budongo Central Forest Reserve, Uganda; (B)—Adult female paratopotype (UTEP 22671) with recently laid eggs from Budongo Central Forest Reserve, Uganda; (C)—Adult female paratopotype (UTEP 22672) from Budongo Central Forest Reserve, Uganda; (D)—Adult female paratype (UTEP 21694) from Budongo Central Forest Reserve, Uganda; (E)—Adult female (UTEP 21700) from Kibale Forest National Park, Uganda; (F)—Adult female (UTEP 21695) from Bizombo, DRC; (G)—Habitat view of the forest at Bizombo, DRC; (H)—Another habitat view of the forest at Bizombo, DRC.

FIGURE 11. Photographs illustrating bone fluorescence revealed by ultraviolet light exposure in Rhampholeon nalubaale sp. nov. (UTEP 22673) from the Albertine Rift, Central Africa.