Calumma roaloko, Proetzel, David, Lambert, Shea M., Andrianasolo, Ginah Tsiorisoa, Hutter, Carl R., Cobb, Kerry A., Scherz, Mark D. & Glaw, Frank, 2018

Proetzel, David, Lambert, Shea M., Andrianasolo, Ginah Tsiorisoa, Hutter, Carl R., Cobb, Kerry A., Scherz, Mark D. & Glaw, Frank, 2018, The smallest ' true chameleon' from Madagascar: a new, distinctly colored species of the Calummaboettgeri complex (Squamata, Chamaeleonidae), Zoosystematics and Evolution 94 (2), pp. 409-423 : 410-415

Calumma roaloko sp. n.

Holotype.

KU 343178 (field number SML 213), adult male in a good state of preservation with incompletely everted hemipenes (Fig. 3), collected on January 12th, 2016 by Shea M. Lambert, Carl R. Hutter, Kerry A. Cobb and Ginah Tsiorisoa Andrianasolo in mid-altitude rainforest, locally known as Inaroka (ca. 19.0050°S, 48.4613°E, ca. 1100 m a.s.l., Fig. 4) near Vohidrazana, Alaotra-Mangoro Region, in central-eastern Madagascar.

Paratypes.

ZSM 244/2018 (KU 343177, field number SML 210), subadult male, same locality and collectors as holotype; KU 343168 (field number SML 177), adult female, UADBA-R uncatalogued (KU 343176, field number SML 178), subadult male, and UADBA-R uncatalogued (KU 343167, field number SML 166), subadult female, all three collected on December 28th, 2015 (SML 166) and December 29th, 2015 (SML 177, 178) by Shea M. Lambert, Carl R. Hutter, Kerry A. Cobb and Ginah Tsiorisoa Andrianasolo in mid-elevation rainforest, locally known as Analambalo (ca. 18.9659°S, 48.4888°E, ca. 1100 m a.s.l., Figs 4-6) near Vohidrazana, Alaotra-Mangoro Region, in central-eastern Madagascar.

Diagnosis.

Calumma roaloko sp. n. is a member of the phenetic C. nasutum species group ( Prötzel et al. 2016), on the basis of the presence of a soft, dermal unpaired rostral appendage, absence of gular and ventral crests, and heterogeneous scalation on the lower arm, consisting mostly of tubercles of 0.4-0.7 mm diameter. With 44.5-45.6 mm SVL and 85.5-93.7 mm total length in adult specimens it is currently the smallest known species in the genus Calumma . The body of the chameleon is uniquely two-colored with beige/white on the ventral and bright green on the dorsal half. Furthermore, it is characterized by a prominent and distally rounded rostral appendage, occipital lobes that are slightly notched, a distinctly elevated rostral crest, absence of a dorsal crest (or presence of at most two cones) in both sexes, absence of axillary pits, and a unique skull morphology.

Calumma roaloko sp. n. differs from C. fallax , C. gallus , C. nasutum , C. peyrierasi , C. vatosoa and C. vohibola of the C. nasutum group by the presence of occipital lobes; from C. boettgeri , C. gehringi , C. guibei , C. lefona , C. linotum and C. juliae in the generally smaller body size with a maximum SVL of 45.6 mm and a maximum TL of 93.7 mm (vs. a range of SVL maxima in the former species of 49.1-59.6 mm and TL maxima of 98.7-126.1 mm), and a straight-lined dorsal margin of the supralabial scales vs. serrated (character 'en dents de scie’ in Angel 1942); additionally from C. gehringi , C. guibei , and C. lefona in the slightly notched occipital lobes of 0.2-0.4 mm (vs. clearly notched with 0.5-1.8 mm) and in the absence of frontoparietal fenestra; from C. boettgeri by the large juxtaposed tubercle scales on the extremities (vs. isolated from each other).

From the most similar taxon Calumma uetzi , C. roaloko sp. n. differs in the absence of a dorsal crest or presence of at most two cones (vs. presence of 5-14 cones), absence of a temporal crest (vs. presence of 1-2 temporal tubercles), greater number of supralabial scales (13 vs. 10-12) and infralabial scales (12-14 vs. 11-12), a longer rostral appendage in adult males of 5.2 mm with large tubercle scales (vs. 3.8 mm, small and smooth tubercle scales; note: n = 1 each), and less heterogeneous scalation on the head with diameter of largest scale in temporal region of 0.6-0.7 mm (vs. 1.0-1.3 mm). The osteology of the skull is similar in both species; C. roaloko sp. n. differs from C. uetzi only in the absence of elevated protuberances at the anterior end of the maxilla that characterize the skull of male C. uetzi . Calumma roaloko sp. n. furthermore differs from all other species by distinct differences in the mitochondrial genes ND2 and COI and a unique two-colored life-coloration.

Description of the holotype.

Adult male (Figs 3, 5b) in a good state of preservation; mouth slightly open; both hemipenes incompletely everted; SVL 45.6 mm, tail length 48.1 mm, for further measurements see Table 1; distinct and elevated rostral ridges that form a concave cup on the snout and fuse on the anterior snout at the base of a tapering, laterally compressed dermal rostral appendage that projects straight forward over a length of 5.2 mm with a diameter of 2.6 mm, rounded distally; 13 infralabi al and 13 supralabial scales; supralabials with a straight dorsal margin; no supra-orbital crest; distinct lateral crest running horizontally; no temporal crest; indistinct parietal crest; occipital lobes clearly developed and slightly notched (0.4 mm); casque raised; dorsal crest absent, only two single cones 0.7 and 1.1 mm from the base of the notch between the occipital lobes; no caudal crest; no traces of gular or ventral crest. Body laterally compressed with fine homogeneous scalation, slightly more heterogeneous on the extremities and head region; limbs with rounded tubercle scales with maximum of 0.7 mm diameter; heterogeneous scalation on the head with largest scale on temporal region with diameter of 0.7 mm; 16 large, oval tubercle scales (diameter>0.3 mm) on the right side of the rostral appendage; no axillary or inguinal pits.

Skull osteology of the holotype.

Description based on a micro-CT scan (Fig. 1a, b). Skull length 12.1 mm; snout-casque length 14.5 mm; maxillae dorsolaterally forming ridges-externally seen as rostral crest; narrow paired nasals tightly bordering anteriorly and separating frontal from maxillae; anterior tip of frontal exceeding more than half of the naris; prefrontal fontanelle and naris separated by contact of prefrontal with maxilla; frontal and parietal smooth with few tubercles; frontal with a width of 3.2 mm (26.4% of skull length) at border to prefrontal, extending to 4.5 mm (37.2%) at border to postorbitofrontal; broad parietal tapering more or less constantly from a width of 4.7 mm (38.8%) at the border to frontal and still broad at midpoint at 2.7 mm (22.3%) until it meets the squamosals, then narrowing to a tip; posterodorsally directed parietal in broad lateral contact with the squamosal; squamosal thick with a few tubercles. For further measurements, see Table 2 and also Suppl. material 3 for a 360° video of the skull. The skull of Calumma roaloko sp. n. shows notable similarity to C. uetzi except for the shape of the maxilla.

The micro-CT scan uncovered a worm-like structure that lies curled and fractured in the throat and proceeds posteriorly into the chameleon’s body presumably via the esophagus. We suppose that this shows an endoparasite trying to leave the dying chameleon after the processing, but note that it is remarkably strongly mineralized.

Coloration of the holotype in preservative.

The body of the holotype in preservative (Fig. 3) is of gray and blue/violet color; the rostral appendage and the head are dark brown with a beige stripe from the snout tip via the supralabial scales to the ventral margin of the occipital lobes and a dark blue temporal region; broad lateral stripe on the body violet with a diffuse net-like pattern, tubercles on extremities also violet; ventral half of the body and inner side of extremities beige-white, dorsal margin of the body and tail of same dark brown color as the head.

Variation.

The four paratypes agree well with the holotype in most characters of morphology and osteology. However, all four paratypes have more tubercle scales on rostral appendage on right side (28-33 vs. 16) and all paratypes lack a parietal crest (vs. indistinctly present); dorsal crest absent in UADBA-R (KU 343167), KU 343168, and UADBA-R (KU 343176). In osteology of the skull the only other micro-CT scanned specimen (the female KU 343168; Fig. 1c, d, Suppl. material 4) differs by the fused prefrontal fontanelle and naris, and the slightly narrower parietal with 34.8% of skull length at postorbitofrontal border (vs. 38.8%) and 19.1% of skull length at midpoint (vs. 22.3%). Both osteological characters can be attributed to sexual dimorphism or intraspecific variation.

Coloration in life.

Based on observations and photographs of the type specimens (Figs 5-7) the species is sexually dichromatic, with males showing a body coloration with an olive green to bright green dorsal half of the body and beige to white ventral half that is continuing on the tail. Females are generally brown and tan or cream ventrally. Both sexes can display a netlike pattern caused by skin between scales in dark brown or beige. Extremities indistinct brown or beige; throat and upper labial scales beige in both sexes; rostral appendage of same brown color as the upper head region, can turn violet in males (Fig. 6a), as well as the eyes, with a beige line on ventral side; in females the appendage can turn yellowish (Fig. 7); dark lateral stripe from the base of the appendage crossing the eyes and ending at the occipital lobes; cheek region highlighted in bright green in the males, continued anteriorly to the base of the appendage.

Hemipenial morphology.

The hemipenes of the three male specimens (the holotype KU 343178, UADBA-R (KU 343176), and ZSM 244/2018) are not completely everted and consequently we can only provide a preliminary and possibly incomplete description. On the asulcal side of the truncus the hemipenis shows large calyces with smooth ridges. The apex is ornamented with two pairs of rotulae, which are larger on the sulcal side (with 12-14 tips) and with 8-10 tips on asulcal side. In the holotype KU 343178 and UADBA-R (KU 343176) there is a small peak between the lobes on the posterior side that might be the tip of a cornuculum ( Prötzel et al. 2017), but this interpretation is in need of confirmation due to the incomplete eversion of the hemipenes. The top of the apex has a papillary field of several fleshy papillae.

Available names.

There are no available names that could be attributed to a species of the C. nasutum group with occipital lobes.

Etymology.

The specific epithet " roaloko " is a combination of the Malagasy words “roa” meaning “two” and “loko” meaning “color”, in reference to the characteristic two-toned body colorations of males (green and white) and females (brown and tan) of this species. The epithet is to be treated as an invariable noun in apposition.

Natural history.

The specific natural history of C. roaloko sp. n. is little-known, but assumed to be similar to other small-bodied Calumma . As with other C. nasutum group species, individuals of C. roaloko sp. n. were encountered sleeping at night on leaves (Fig. 7) or small branches, and most often spotted ~2-5 m above the ground. Calumma roaloko sp. n. may be restricted to higher-elevation habitats, as it has only been found at ca. 1100 m a.s.l., although this is difficult to determine with certainty as most forests below ~1000 m a.s.l. in the area have been cleared. Interestingly, it is known from only two sites, both on the periphery of the forest fragment, and characterized by qualitatively more degraded habitat and/or secondary forest growth as compared to two sites located with more intact primary forest, where it was not encountered (Fig. 4). In summary, either C. roaloko sp. n. may have a higher detection probability in disturbed habitats, and/or may be out-competed in primary forest by close relatives (e.g., C. nasutum complex species that we found in all four sites). Several specimens were observed to have small red acarid ectoparasites (visible on the hindlimb in Fig. 6a).

Distribution.

Given current evidence, the distribution of C. roaloko sp. n. is potentially restricted to a small fragment (~300 km2) of mid-elevation rainforest that lies outside of nearby Analamazaotra Special Reserve and Andasibe-Mantadia National Park in central-eastern Madagascar (Fig. 4), but within the Réserve de Ressources Naturelles du Corridor Ankeniheny-Zahamena newly protected area. However, we believe that C. roaloko sp. n. may still be discovered in nearby areas, including Andasibe-Mantadia National Park, although it has never been found over dozens of surveys in nearby protected areas over the last century, including our own surveys (Hutter, Lambert, Scherz, Prötzel, Glaw, etc. unpubl. data). It is also possible that C. roaloko sp. n. could be found in other smaller and more fragmented forests located to the west of the type locality of C. roaloko sp. n., south of the city of Moramanga, but recent work in one remnant forest fragment in that area discovered C. juliae there, and no specimens of C. roaloko sp. n. were found ( Prötzel et al. 2018).

Suggested Conservation Status.

The ~300 km2 fragment of mid-elevation rainforest from which C. roaloko sp. n. is known is managed by several local government councils, and has recently been established as a new protected area ( Réserve de Ressources Naturelles du Corridor Ankeniheny-Zahamena) within the scope of the expansion of Madagascar’s national parks ( Gardner et al. 2018). Forest in this area is dramatically fragmented and its area is decreasing. We suggest to evaluate the species as Endangered under the IUCN Red List criterion B1 (Extent of occurrence <5000 km2) subcriteria a (severely fragmented or known from fewer than five threat-defined locations) and b(iii) (continuing decline in the area, extent, and/or quality of habitat). However, potentially suitable habitat for C. roaloko sp. n. also exists in other nearby protected areas (Andasibe-Mantadia, Analamazaotra) and private reserves (Vohimana). Although field surveys to these areas have not yet uncovered C. roaloko sp. n., they have revealed the presence of several other undescribed species of amphibians and reptiles, found originally in the same forest fragment as C. roaloko sp. n. (Hutter, unpubl. data). Furthermore, current evidence suggests that C. roaloko sp. n. is amenable to disturbed habitat (see Natural History). As such, the conservation status of C. roaloko sp. n. as suggested herein may need revision pending future survey work, particularly in nearby protected areas.