Brookesia micra, Frank Glaw & Jörn Köhler & Ted M. Townsend & Miguel Vences, 2012

Frank Glaw, Jörn Köhler, Ted M. Townsend & Miguel Vences, 2012, Rivaling the World’s Smallest Reptiles: Discovery of Miniaturized and Microendemic New Species of Leaf Chameleons (Brookesia) from Northern Madagascar, PLoS ONE 7 (2), pp. 1-24 : 16-17

Brookesia micra sp. n.

ZooBank LSID: urn:lsid:zoobank.org:act:D1A239D6-93E8-4C34-A428-F79A2C8B6405

Remark.—This species has been considered before as Brookesia sp. ‘‘Nosy Hara’’ [ 7].

Holotype.— ZSM 2181/2007 (FGZC 1271), adult male (hemipenes everted), collected on Nosy Hara island , 12°14'40"S, 49°0 0'30"E, ca. 10–20 m a.s.l., Antsiranana Province, northern Madagascar, on 7 March 2007 by H. Enting, F. Glaw and J. Köhler.

Paratypes.— ZSM 2180/2007 (FGZC 1270), ZSM 2182/2007 (FGZC 1275), juveniles, ZSM 2183/2007 (FGZC 1278), ZSM 2185/2007 ( FGZC 1280 ), adult males (hemipenes everted), ZSM 2184/2007 (FGZC 1279), ZSM 2186–2187/2007 (FGZC 1281– 1282), adult females, all with same data as holotype ; UADBA uncatalogued ( FGZC 1830 ), male, ZSM 1507 /2008 ( FGZC 1831 ), male (not examined morphologically), UADBA uncatalogued ( FGZC 1833 ), female, ZSM 1509 /2008 ( FGZC 1834 ), adult female, ZSM 1510 /2008 ( FGZC 1832 ), juvenile, all collected at small stream on Nosy Hara , 12°14'59"S, 49°0 0'28"E, 12 m a.s.l., Antsiranana Province, northern Madagascar, on 22 February 2008 by F. Glaw and J. Köhler.

Diagnosis.— A member of the Brookesia minima group based on small body size (SVL<20 mm) and molecular phylogenetic relationships. Brookesia micra is distinguished from all other members of the group by a shorter relative tail length (tail length/SVL 0.37–0.49 versus 0.49–0.92), and by orange coloured tails in life in adults (vs. inconspicuous brownish colour). In addition, from B. confidens by a smaller adult male size (SVL 15.1– 15.3 mm vs. 18.3–20.1 mm), supranasal cone present (vs. absent), and hemipenis with comb-like apical structure (vs. narrow without ornaments); from B. dentata by probably smaller adult body size (no measurements of male B. dentata available); from B. exarmata by smaller adult body size (female SVL 18.7–19.9 vs. 25.7–26.5, no male measurements available for B. exarmata ); from B. karchei by smaller size (female SVL 18.7–19.9 vs. 30.7, no male measurements available for B. karchei ); supraocular cone absent (vs. present); from B. minima by presence of a pelvic spine (vs. absent or indistinct pelvic spine), and hemipenis with comb-like apical structure (vs. balloon-like without ornaments); from B. peyrierasi by a smaller adult male size (SVL 15.1–15.3 mm vs. 19.1–27.4 mm), and hemipenis with comb-like apical structure (vs. bilobed with four spines on each lobe); from B. ramanantsoai by a smaller adult male size (SVL 15.1–15.3 mm vs. 21.7 mm), supraocular cone absent (vs. present in some specimens), and hemipenis with comblike apical structure (vs. baloon-like without ornaments); from B. tristis by a smaller adult male size (SVL 15.1–15.3 mm vs. 18.0– 18.2 mm), and hemipenis with comb-like apical structure (vs. small papillae on apex not arranged comb-like); and from B. tuberculata by supraocular cone absent (vs. present), and hemipenis with comb-like apical structure (vs. crown-like structure). For a distinction from B. desperata , described below, see the diagnosis of this species. Referencing a fragment of the 16S rRNA gene, B. micra shows an uncorrected pairwise divergence of 6.8% to its sister clade ( B. tristis + B. desperata ), and divergences>7.2% to all other species of the B. minima group.

Description of holotype.— Adult male in good state of preservation ( Fig. 7 ; Supporting Information S1). Both hemipenes everted. Measurements in Table 2. Head with lateral crest starting at median level at the posterior edge of eye; prominent orbital crests; a weak crest at the posterior edge of the head, that forms a weakly developed dorsal helmet; a pair of low indistinct parasagittal crests slightly converging before terminating at the lateral crest; three similar-sized pointed tubercles on each side of posterior crest, one at termination point of lateral crest, one at termination point of parasagittal crest, and a one between parasagittal and lateral crests; one pointed tubercle on lateral surface of head, below lateral crest in temporal region; orbital crest denticulated; no supraocular cone recognizable; supranasal cone small; head longer (4.5 mm) than wide; chin and throat without longitudinal rows of slightly enlarged tubercles. Dorsal surface of body without a vertebral ridge or keel; 11 dorsolateral pointed tubercles form a complete longitudinal line on the body; most posterior (11th) pointed dorsolateral tubercle being largest, above insertion point of hindlimb; pointed dorsolateral tubercles almost equally spaced, pointing out almost perpendicularly from body; slightly enlarged, rounded tubercles form curved transversal crests on either side of the vertebral line between 1 st and 10th dorsolateral pointed tubercles; slightly enlarged scales forming four parallel longitudinal rows on dorsal surface of tail; no well-defined dorsal pelvic shield in sacral area; scattered enlarged rounded tubercles on the lateral surface of body; venter without enlarged tubercles; no pointed tubercles around cloaca; no enlarged tubercles on lateral or ventral surfaces of tail. After almost four years in ethanol, back, flanks, dorsal surfaces of limbs and anterior part of tail uniformly dark grey-brown; posterior part of tail beige; neck grey; throat and venter light grey.

Variation.— For morphological measurements and proportions see Table 2 and Supporting Information S1. In preservative, ZSM 2185/ 2007 and 2188 /2007 have a greyish dorsal surface of head and neck and a slightly lighter vertebral region. The throat is uniformly dark brown (ZSM 2187/ 2007 and 2184 /2007) or beige with brown spots (ZSM 2185/2007, 2188/2007, and 1509/2008). The tail base of the males is only slightly more thickened than in the females. In life, most individuals with dorsal colouration of head, dorsum and tail light grey, lateral parts of the tail more yellowish becoming orange posterior to the tail base. Lateral parts of the body brown, with few dark brown spots; limbs almost uniformly dark brown. This pattern is likely to refer to a stress colouration. When unstressed, most parts of the body dark brown, except a beige area on the head anterior to the eyes. Tail base dark brown, orange in the middle and yellowish posteriorly. Colour and pattern of juveniles resemble those of adults and they can also show the stress colouration, but tails are slightly less colourful than in adults and usually do not show bright orange colour.

Genital morphology.— Everted hemipenes of this species are available for three specimens (holotype ZSM 2181/2007, paratypes ZSM 2183/2007, ZSM 2185/2007). Each hemipenis is an elongated, relatively wide tubular structure. Apex and truncus are devoid of any ornaments. In the holotype, hemipenis length is 2.4 mm and maximum hemipenis width is 0.9 mm. When fully everted, the most characteristic feature is the apex which is a flat surface distally forming a symmetrical comb of six large, rounded papillae, of which the two inner ones are largest, followed by the two intermediate ones, whereas the outer ones are merely two slightly elevated knobs, recognizable only in fully everted organs. In general, this comb of papillae is not visible in hemipenes that are not fully everted, different from the spines of, e.g., B. peyrierasi that typically are also visible in incompletely everted organs. All three examined specimens have one hemipenis fully everted, the second one only partially everted. The organs are largely transparent, and the central retractor muscles can be easily seen through the outer hemipenial integument ( Fig. 6 ).

Etymology.— The species epithet is a latinized derivation from the Greek word ‘‘MIKRóz’’ (mikros), meaning ‘‘tiny’’ or ‘‘small’’ and referring to the extremely diminutive body size. It is used as an invariable noun in apposition.

Distribution.— Only known from two sites (see localities in type series) on the small island of Nosy Hara, northern Madagascar (e.g. Fig. 8D ). Remarkably, no Brookesia species was recorded during intensive herpetological surveys of Nosy Hara, nearby islands and the adjacent mainland [ 40], suggesting that B. micra might be difficult to record.

Natural History.— B. micra was found during the day active on the ground in a mosaic of eroded limestone boulders and dry forest leaf litter, and at night roosting on branches in very low vegetation (ca. 5–10 cm above the ground). In contrast to B. tristis and B. confidens its occurrence was not remarkably patchy.

Figures

Figure 6. Hemipenes of species in the Brookesia minima group. The photos show for each species, a general view of the organs and a close-up. For B. desperata, the inset picture shows a non-turgid everted hemipenis where the two apex projections are very prominent. Note that also several other of the shown preparations are not fully turgid, especially in B. ramanantsoai and B. micra. In two other species (B. confidens and B. tristis) the shown hemipenes might not be fully everted. doi: 10.1371 / journal. pone. 0031314. g 006

Figure 7. Dorsal, lateral and ventral views of preserved male holotypes of newly described species. Scale bar equals 5 mm. doi: 10.1371 / journal. pone. 0031314. g 007

Figure 8. Brookesia micra sp. n. from Nosy Hara, northern Madagascar. (A) adult male on black background, showing orange tail colouration; (B) juvenile on finger tip; (C) juvenile on head of a match; (D) habitat along a small creek on western flank of Nosy Hara, where part of the type series was collected. doi: 10.1371 / journal. pone. 0031314. g 008