A New Black-Bellied Snake (Pseudoxyrhophiinae: Liophidium) from Western Madagascar, with Notes on the Genus Pararhadinaea

Amphibia-Reptilia 30 (2009): 173-183

A new black-bellied snake (Pseudoxyrhophiinae: Liophidium) from western Madagascar, with notes on the genus Pararhadinaea

Michael Franzen1, Julia Jones2, Achille P. Raselimanana3,ZoltánT.Nagy4, Neil D’Cruze5, Frank Glaw1, Miguel Vences6,∗

Abstract. We describe Liophidium maintikibo, a new species of pseudoxyrhophiine snake from the dry deciduous forest of Kirindy, western Madagascar. The new species is related to Liophidium therezieni but differs by a lower number of ventral scales and several details of colouration. Its ventral scales have a large central black patch which is missing from the subcaudals. This predominantly black ventral side is similar to that of another enigmatic Malagasy snake, Pararhadinaea melanogaster, for which we here present evidence for two new locality records, Ankarana and Daraina in northern Madagascar. The phylogenetic relationships of P. melanogaster (the sole representative of a monotypic genus) have so far not been clariﬁed. Similarities to Liophidium maintikibo may indicate afﬁnities to Liophidium,butP. melanogaster differs from this new species by a lower number of ventrals, subcaudals, number of maxillary teeth and by a different dorsal colouration.

Keywords: Liophidium maintikibo sp. n., Liophidium therezieni, Madagascar, molecular relationships, new distribution records, Pararhadinaea melanogaster, Squamata: Serpentes: Lamprophiidae.

Introduction Boettger, 1898, may also be related to Li- ophidium. This genus has been reviewed by The genus Liophidium Boulenger, 1896, cur- Domergue (1984b) who also described a sub- rently contains eight species of small terres- species of P. melanogaster, P. m. marojejyen- trial snakes, including seven Malagasy taxa and sis and a new species that he assigned to one endemic of Mayotte in the Comoro is- the genus as Pararhadinaea albignaci. Sub- lands. Species of the genus are morphologi- sequently, Raxworthy and Nussbaum (1994) cally rather similar. Liophidium has not been placed Pararhadinaea near Pseudoxyrhopus subjected to a comprehensive revision since and Heteroliodon. This view was rejected by the work of Domergue (1984a) who described Cadle (1999) who also stressed that Liophidium three new species (L. apperti, L. therezieni, is only weakly deﬁned among the Pseudoxyrho- L. chabaudi). pus group and that monophyly within Lio- A recent molecular study (Glaw et al., phidium 2007) suggests a relationship between Lio- is poorly corroborated (Cadle, 1999: phidium and species of Liopholidophis Moc- 435-436). Cadle (1999) transferred the sec- quard, 1904. The monotypic Pararhadinaea ond species of Pararhadinaea as Exallodon- tophis albignaci to a newly described, monotypic genus, leaving P. melanogaster (including 1 - Zoologische Staatssammlung München, Münchhausen- its subspecies marojejyensis) as the sole repre- str. 21, 81247 München, Germany 2 - School of the Environment and Natural Resources, Ban- sentative of the genus. gor University, LL57 2UW, Wales The present study contributes to the sys- 3 - Départment de Biologie Animale, Université d’Anta- tematics of Liophidium by describing a new nanarivo, BP 906, Antananarivo, 101 Madagascar 4 - Royal Belgian Institute of Natural Sciences, rue Vautier species from Kirindy forest in western Mada- 29, B-1000 Brussels, Belgium gascar which is clearly assigned to this genus 5 - The World Society for the Protection of Animals, 89 Al- by molecular data. We compare the new species bert Embankment, London, SE1 7TP, United Kingdom Liophidium 6 - Technical University of Braunschweig, Zoological Insti- to its presumed closest relative, tute, Spielmannstr. 8, 38106 Braunschweig, Germany therezieni,aswellastoPararhadinaea melano- ∗Corresponding author; e-mail: [email protected] gaster and provide data on newly collected

Table 1. Voucher specimens and GenBank accession numbers of the snakes included in the molecular analysis.

Species Sample Locality information Voucher specimen GenBank ID accession no.

Dromicodryas bernieri J91 Ifaty UADBA (FGMV 2000-517) AY188014 Dromicodryas quadrilineatus J66 Sambava not collected AY188015 Thamnosophis lateralis J93 near Mantasoa UADBA (FGMV 2000-36) DQ979977 Thamnosophis stumpffi J331 Nosy Be ZSM 579/2001 DQ979986 Exallodontophis albignaci Z2220 Andasibe UADBA (ZCMV 2220) EU394724 Liopholidophis sexlineatus J98 Mandraka UADBA (FGMV 2000-38) AY188024 Liopholidophis dimorphus F491 Montagne d’Ambre ZSM 252/2004 DQ979980 Pseudoxyrhopus ambreensis J102 Montagne d’Ambre not collected AY188035 Liophidium chabaudi Tp844 not available not available EU394721 Liophidium torquatum J84 Montagne d’Ambre not collected AY188023 Liophidium torquatum J307 Ranomafana (Vohiparara) ZSM 691/2003 DQ979984 Liophidium vaillanti B27 near Kirindy not collected EU394720 Liophidium vaillanti B32 near Kirindy not collected DQ979995 Liophidium therezieni M07-2 Montagne des Français ZSM 2053/2007 EU394722 Liophidium maintikibo M07-3 near Kirindy ZSM 2052/2007 EU394723 Liophidium rhodogaster J304 Ranomafana NP ZSM 784/2003 DQ979978 Liophidium rhodogaster F466 Montagne d’Ambre ZSM 238/2004 EU394719 Liophidium rhodogaster F467 Montagne d’Ambre UADBA (FGZC 467) DQ979992 specimens of both these poorly known snake Phylogenetic reconstructions were carried out using species. PAUP* 4b10 software (Swofford, 2002). We performed parsimony analyses with 2000, and maximum likelihood heuristic searches with 100 bootstrap replicates, respectively. In the data set including outgroups, 410 of the total Materials and methods 1117 characters were parsimony-informative, and a single most parsimonious tree was found. For maximum likelihood The snakes were generally anaesthetized by injection with analysis, the nucleotide substitution model HKY + I + G chlorobutanol, fixed in either formalin or 95% ethanol, was selected using the Akaike information criterion (AIC). and subsequently stored in 70% ethanol. Muscle tissue Bayesian analyses of phylogenetic inference (BI) were car- samples were taken either from freshly killed snakes or ried out using MrBayes v3.1.2 (Ronquist and Huelsenbeck, from ethanol-fixed specimens 1-2 years after collection 2003) running 2×106 generations under the HKY + I + G and preserved in 98% ethanol. Measurements were taken substitution model selected by the software MrModeltest to the nearest millimeter with a caliper or a ruler. We (Nylander, 2004). In BI, the first 25% of the trees (5000 follow Cadle (1996) regarding the terminology of meris- trees) were discarded, and the remaining 15 000 trees were tic and mensural data. Ventral scales were counted with- evaluated. out preventrals. Institutional abbreviations are: Museum New sequences determined in this study were deposited National d’Histoire Naturelle, Paris (MNHN); Naturhis- in GenBank under the accession numbers EU394719- torisches Museum, Wien (NMW); Forschungsinstitut und EU394724. Data on voucher specimens and Genbank ac- Naturmuseum Senckenberg, Frankfurt am Main (SMF); cession numbers are given in table 1. Material used for mor- Université d’Antananarivo, Département de Biologie An- phological comparisons is listed in the appendix. Pararhad- imale (UADBA); Zoologische Staatssammlung München inaea was omitted from genetic analyses since we had no (ZSM). tissue samples available. A standard method was used for total genomic DNA extraction (Sambrook, Fritsch and Maniatis, 1989). The complete cytochrome b gene was amplified with primers Results L14910, L14919 and H16064 (Burbrink, Lawson and Slowinski, 2000; modified by de Queiroz, Lawson and Liophidium maintikibo sp. n. (figs 1-3) Lemos-Espinal, 2002), and directly sequenced with L14903 (a 5 end of L14910), L-410 and H-391 (Nagy et al., 2003). Pararhadinaea/Liophidium sp.“Kirindy”Ð Glaw All sequences were checked for their quality by eye, and for their mitochondrial origin (i.e., they were translated to and Vences (2007): 430-431. amino acids and checked for stop codons as well as for higher substitution rates in third positions which is typical Holotype. ZSM 2052/2007, collected near Ki- ◦ ◦ for coding sequences). Sequences were aligned manually. rindy research station (20 03 S, 44 39 E), el- A new black-bellied snake (Pseudoxyrhophiinae: Liophidium) 175

Figure 1. Liophidium maintikibo sp. n. (holotype, ZSM 2052/2007), drawing of head in (a) dorsal and (b) lateral view. Scale bar represents 1 mm.

Figure 2. Holotype of Liophidium maintikibo (ZSM 2052/2007) in life. evation below 100 m, about 60 km north of Morondava (district of Morondava, region of

Menabe, Toliara Province), western Madagas- Figure 3. Holotype of Liophidium maintikibo (ZSM car, by Julia Jones on 20 November 2004. 2052/2007) in life, ventral side. 176 M. Franzen et al.

Diagnosis. Liophidium maintikibo sp.n.dif- per and lower dark margins of lateral band nar- fers from the only Comoran species L. may- row (vs. equivalent lines broad), dorsolateral ottensis by 17 rows of dorsal scales (vs. 19) stripe absent or weak (vs. dorsolateral stripe and from the Malagasy species (which all share broad), gular region heavily mottled with dark 17 rows of dorsal scales) as follows: from L. ap- brown markings (vs. gular region with sparse perti, L. chabaudi, L. rhodogaster, L. torquatum dark markings), light ventral colouration bright and L. trilineatum by the lack of a loreal scale yellow in life (vs. light ventral colouration pink- and the presence of only seven upper labials, ish white in life), ventral scales with a median with upper labials 3 + 4 touching the eye (vs. 8 oval blotch, forming one broad mid-ventral line upper labials, 4+5 touching the eye). Moreover, (vs. ventral scales mostly with two lateral mark- it differs from the above mentioned species (ex- ings, forming two indistinct lateral rows), sub- cept L. rhodogaster) by a higher number of ven- caudals immaculate (vs. subcaudals with lateral tral scales and by a different dorsal colouration markings). (5 dorsal stripes vs. 0, 1 or 3 stripes; except The new species differs from the two taxa L. apperti). of the morphologically similar genus Pararhad- From the remaining Liophidium with seven inaea (P. melanogaster melanogaster, P. m . upper labials and no loreal scale L. maintikibo marojejyensis) by a higher number of ventral sp. n. differs from L. vaillanti by fewer ventral scales (193 vs. 147-180), a higher number of scales (193 vs. 220-255) and colouration (e.g., subcaudals (56 vs. 41-45), a high number of presence of a light nuchal band, lack of a broad maxillary teeth (23 vs. 13-14) and by a differ- and well deﬁned light lateral band, presence of ent colouration (presence of a light nuchal band a broad longitudinal mid-ventral stripe of oval and no well deﬁned strongly contrasting light blotches). It also differs from L. vaillanti by and dark stripes). a smaller total length (255 mm vs. max. 858 Description of holotype. Probably adult, sex mm, see comments on earlier available names unknown, in good state of preservation. Snout- below). vent length 205 mm, tail length 50 mm (to- The new species resembles its apparent sister tal length 255 mm; tail length 19.6% of total taxon Liophidium therezieni in most characters. length). Head length 7.4 mm, head width 3.8 It differs from the latter by having fewer ven- mm; eye large, 1.1 mm in diameter, pupil round. tral scales (193 vs. 218-235, table 2) and in sev- Ventral scales 193, three preventrals; cloacal eral aspects of the dorsal and ventral coloura- plate divided; subcaudal pairs 56. Dorsal scales tion: upper labials predominantly dark, mostly smooth, no apical pits; in 17-17-15 longitudinal with a small light marking each (vs. upper labi- rows; scale row reduction from 17 to 15 at level als light, with sparse dark markings), broad dark of ventral 119. Rostral scale broad, reaching lateral band (vs. no distinct lateral band), up- onto the dorsal side of head. Internasals and pre-

Table 2. Mensural and meristic data of Liophidium therezieni. ToL – total length; SVL – snout-vent length; TL – tail length; V – ventrals; SC – subcaudals; HL – head length; HW – head width; ED – eye diameter; HT – holotype; PT – paratype (data from Domergue, 1984).

Locality Sex ToL SVL TL TL/ToL V SC HL HW ED ED/HL

MNHN 1982.444 (HT) Forêt d’Anatelo 697 588 109 0.16 229 58 18.5 11.3 2.4 0.13 MNHN 1978.1425 (PT) Forêt d’Anatelo 560 469 91 0.16 233 56 – – – – UADBA (FGZC 1717) Montagne des Français 704 610 94 0.13 235 46 17.8 10.5 2.3 0.13 ZSM 2053/2007 Montagne des Français 473 395 78 0.17 219 55 12.5 6.7 1.6 0.13 ZSM 1612/2008 Ampombofofo 637 557 80 0.13 235 52 13.9 7.6 1.8 0.13 UADBA 00726 not available 598 506 92 0.15 218 51 – – – – ZSM 1613/2008 Baie des Sakalava juv. 400 345 55 0.14 234 50 9.7 5.3 1.4 0.14 A new black-bellied snake (Pseudoxyrhophiinae: Liophidium) 177 frontals nearly quadratic. Loreal absent. Preocu- dorsolateral stripe on dorsal scale rows 4-7, lars single, two postoculars. Supraoculars elon- and a diffuse dark vertebral stripe (3 dorsals gate, posteriorly reaching to the posterior mar- wide), composed of tiny irregularly shaped dark gins of the postoculars. Frontal scale elongate, markings on each scale. triangular. Parietals triangular, very broad; ante- Ventrals creamish white; a large black and rior outer margins reaching down to the upper somewhat irregularly shaped oval patch at cen- portions of the lower postoculars. Upper labi- ter of each scale; the large patches form a broad als 7/7 but on left side an interspersed addi- mid-ventral longitudinal stripe, reaching from tional scale between upper labials 2 and 3; up- the first onto the penultimate ventral; ultimate per labials 3-4 in contact with eye. Lower labials ventral, cloacal plate and subcaudals without 8/8, the first pair in contact behind the mental, black central markings. Lateral edges of ven- 1-4 touching an anterior genial, 4-5 touching a trals with tiny irregular dark markings, forming posterior genial. Genials elongate, longer than a diffuse longitudinal stripe; lateral markings on broad; anterior genials broader than posterior. subcaudals broad, covering the entire outer mar- Almost all head shields (except parietals) with gins of each scale. tiny irregularly distributed papillae; on frontal The overall dorsal life colouration appeared scales only in irregular rows at the posterior to be reddish brown (based on slides taken in margins. the field, see also fig. 6, p. 431 in Glaw and We were not able to examine the dentition of Vences, 2007). The lightly coloured areas at the the new species comprehensively due to the del- snout were creamish beige, the nuchal band and icate nature of the only known specimen. How- the light portions of the ventral side were bright ever, we counted at least 23 maxillary teeth on yellow in life. the right maxilla, and noticed a small diastema, Habitat. The holotype was collected during probably due to missing teeth. the day near a dirt road in the forest of Kirindy. After approximately three years in preser- The vegetation at Kirindy consists of semi- vative overall ground colouration brown with open, deciduous dry forest. The snake was col- small light and dark mottlings and longitudi- lected as it crossed a sandy path at 7.00 a.m. nal stripes. Dorsal head colouration brown, with small and partly diffuse dark vermiculations. Molecular relationships. The molecular tree Rostral, internasals, anterior 4/5 of prefrontals presented here (fig. 4) is based on cytochrome b and most of the supraoculars creamish white DNA sequences of most Malagasy Liophidium to light brown with some diffuse darker shades species, and only misses L. apperti and L. tri- and irregularly distributed tiny dark spots. Dark lineatum. Monophyly of the included species of dorsal head colouration posteriorly gradually the genus is confirmed and strongly supported. fading into a white, three dorsals wide nuchal The sister group of Liophidium (made up by band that ventrally connects with the white belly the genus Liopholidophis; see Glaw, Nagy and colouration. Nuchal band posteriorly sharply Vences, 2007; Glaw et al., 2007) is not sup- edged by a three dorsals wide dark brown collar. ported, and the same is true for other inter- Lateral sides of the head dark brown; each up- generic relationships, indicating that inclusion per labial with an irregular, somewhat centered of additional markers (Glaw et al., 2007) is nec- large white marking. Gular region heavily mot- essary to resolve these aspects of the topology. tled with irregular large white and dark brown Exallodontophis albignaci, for which molecu- markings. lar data are here included for the first time, The dorsal colouration consists of a dark does not appear to be closely related to nei- lower lateral stripe with slightly darker upper ther Pseudoxyrhopus nor Liophidium and its and lower edges on dorsal scale rows 1-3, a light isolated position receives no relevant support. 178 M. Franzen et al.

Figure 4. Maximum likelihood tree based on cytochrome b sequences of species of Liophidium and other pseudoxyrhophiine snakes. Numbers above branches are (from left to right) support values from bootstrap analyses (parsimony, 2000 replicates; maximum likelihood, 100 replicates) and Bayesian posterior probabilities. Two species of Dromicodryas were used as outgroup (not shown).

Within Liophidium, L. rhodogaster is placed as 1958; Glaw and Vences, 1994). We have re- most basal species, L. chabaudi is placed sister examined the types of both taxa and conclude to L. torquatum and L. maintikibo sister to L. that they strongly differ from L. maintikibo.The therezieni. Hence, although several basal rela- holotype of Idiophis vaillanti var. extensa (SMF tionships among genera are not sufficiently re- 17152) has a high number of ventral scales solved, the tree shows that Liophidium main- (250), three longitudinal rows of oval blotches tikibo is firmly nested within Liophidium and on the ventral side and a dorsal colouration that closely related to L. therezieni. The molecular consists of five well-defined narrow dark lon- differentiation between these two species is of gitudinal lines alternating with strongly con- of 11.8% uncorrected p-distance, at a similar trasting lightly coloured longitudinal bands. The level as between other well-established species two syntypes of Wernerodakaria subpunctata of pseudoxyrhophiine snakes. (NMW 16860:1-2, female, male) also have high Earlier available names. Besides current spe- numbers of ventral scales (240 and 228, respec- cies as listed in the diagnosis, two nomina tively), are much larger than L. maintikibo (total exist in the genus Liophidium that need to length 858 and 725 mm, respectively) and each be considered as possible earlier names of possess a dorsal coloration of well-defined lon- Liophidium maintikibo, namely Idiophis vail- gitudinal dorsal lines and bands, including five lanti var. extensa Boettger, 1913 (type local- narrow dark lines, a light broad lateral band, and ity: “Madagaskar”), and Wernerodakaria sub- a greyish broad vertebral band. punctata (Werner, 1925) (substitute name for Dakaria subpunctata according to Williams and Etymology. The species name is used as a Wallach, 1989; type locality “Dakar, Senegam- noun in apposition and is composed of the bien” [in error]), both currently seen as ju- Malagasy adjectiv “mainty”, meaning black, nior synonyms of Liophidium vaillanti (Guibé, and “kibo”, meaning venter. It refers to the large A new black-bellied snake (Pseudoxyrhophiinae: Liophidium) 179 black central markings on the ventral scales of Orangea region). All new localities are between the new species. 20 and 230 m elevation. Meristic and mensural data of the new spec- Distribution. Liophidium maintikibo is only imens are presented in table 2. The new spec- known from the type locality. However, Mori imens resemble the holotype of L. therezieni and Ikeuchi (2006: 42) depicted a snake from in most characters (see also table 2): Body Ampijoroa (Mahajanga province, approx. 570 approximately as high as wide; head slightly km northeast of Kirindy) as a juvenile of L. wider than neck. Pupil round. Anterior edges torquatum. This individual resembles the holo- of internasals and posterior edges of prefrontals type of L. maintikibo in most aspects of the dor- rounded, convex. Loreal absent. Preocular sin- sal and ventral colouration and may also repre- gle, two postoculars. Temporals 1+2+3onboth sent this new species. sides. Usually 7/7 upper labials, with 3-4 touching the eye; two individuals (ZSM 2053/2007, New data on Liophidium therezieni ZSM 1613/2008) with a 7/6 constellation (fu- sion of right upper labials 5 + 6). Lower labi- We obtained five new specimens of Liophid- als 8/8, the first pair in contact behind the men- ium therezieni, mainly during extensive sur- tal, 1-4 touching an anterior genial, 4-5 touch- veys of the amphibians and reptiles of the ing a posterior genial. Genials slightly longer Montagne des Français area and the Ampom- than broad; anterior genials broader than poste- bofofo region north of Anjiabe by volonteers rior. Dorsal scales smooth, in 17-17-17 rows at of Frontier-Madagascar (e.g., D’Cruze et al., midbody. Cloacal plate divided. See table 2 for 2007). All individuals were captured in more additional mensural and meristic data. or less disturbed dry deciduous forests, either Life colouration (based on slides taken in the in limestome (Tsingy) dry forest (Montagne des field, see also fig. 5): Ground colouration of the Français) or within dense scrub forest on heav- heads in all specimens light brown, dorsally and ily overgrown coastal dunes (Baie des Sakalava, laterally dusted with dark brown, forming an in-

Figure 5. Liophidium therezieni from Baie des Sakalava (ZSM 1613/2008), showing similarities in dorsal colouration to L. maintikibo. 180 M. Franzen et al. distinct dark head cap. The head cap covers the men of P. melanogaster marojejyensis, from the upper portions of all upper labials, preoculars, Marojejy Massif in the North East (but see Ca- postoculars, the frontal, supraoculars, and the dle, 1999: 440, for problems with this locality). parietals. A distinct cream patch covers the ros- This prompted us to examine further material tral, nasal, internasals as well as the prefrontals, of P. melanogaster to assess its morphological and a thin black postocular bar extends from variability. Two specimens of this species were the anterior of the eye to the anterior of upper available to us, both collected by APR and col- labial 7. The remaining portions of the upper leagues in northern Madagascar, and both con- and lower labials are immaculate white. A dis- stituting new locality records for the species. tinct cream nuchal collar (3 dorsals wide) bor- UADBA 18586 (Ankarana Special Reserve; dered by thin black lines is also present. Ground see Appendix for comprehensive collection colouration of dorsal scale rows light brown ex- data): snout-vent length 247 mm, tail length cluding the first three rows immediately fol- 43 mm (total length 290 mm); small rostral lowing the light nuchal collar which share the (not visible from above), quadratic internasals; dark brown colouration of the head cap. Dor- no loreal; prefrontals larger than internasals; sum with five dark longitudinal lines: a broad supraoculars large, roughly oval in shape; 7/7 lateral band on dorsal scale rows 1-3 (with scale upper labials (3 + 4 in contact with eye); one row 3 distinctly darker), a dark dorsolateral line preocular, 3/2 postoculars; 1 + 2 + 3 tempo- on dorsal scale row 6 and a middorsal line on rals; head as broad as body (head width 5.1 scale row 9, which is distinctly darker than the mm; head length 9.3 mm); eye small, 0.8 mm other lines. The longitudinal lines start immedi- in diameter (9% of head length); 17 dorsals, ately behind the nuchal band and extend along 180 ventrals, cloacal plate divided, 42 subcau- the entire length of the body, gradually fading dal pairs. This specimen is reproduced in fig. 6, on the anterior of the body and tail. Ground and has also been shown by Glaw and Vences colouration of ventral surfaces of the head, neck (2007). UADBA 30054 (Andranotsimaty forest, and body creamish white-grey, slightly irides- Daraina Conservation Site) is a juvenile with cent. Ventral surface of head dusted in places a damaged head in poor state of preservation: with dark grey. Venter and underside of tail usu- snout-vent length 86.5 mm, tail length 29.5 mm ally with two complete lateral rows (incomplete (total length 116 mm), 17 dorsals, 187 ventrals, in the juvenile ZSM 1613/2008) and one in- cloacal plate divided, ca. 45 subcaudal pairs. complete median row of irregular dark mark- This specimen was collected under a rotten log ings. in the morning around 10:00 a.m. within open canopy dry transitional semi-deciduous forest. New data on Pararhadinaea melanogaster The habitat was intensively disturbed by artisan The new species described above, Liophidium gold extraction and cattle grazing. When uncov- maintikibo, bears a few characters, especially ered, the snake tried to escape by burrowing into the black colour on ventrals but not on sub- the sandy soil. caudals, that superficially resembles an enig- The dorsal colouration of both specimens matic species of pseudoxyrhophiine snake from consists of two whitish, two light brown and Madagascar, Pararhadinaea melanogaster. Be- three dark brown stripes: the first dorsal scale side a specimen with the unprecise local- row is creamish white with tiny faint brown ity information “Madagascar” (the holotype of markings; a dark brown lower lateral stripe on Rhabdotophis subcaudalis Werner, 1909), this dorsal scale rows 2, 3 and the lower half of species was so far known only from the type row 4; a thin white line on the upper half of specimen from Nosy Be in the Sambirano re- dorsal scale row 4 and the lower half of row gion of Madagascar, and from the type speci- 5; a narrow dark brown stripe on the upper A new black-bellied snake (Pseudoxyrhophiinae: Liophidium) 181

Figure 6. Pararhadinaea melanogaster from Ankarana in life (UADBA 18586). half of dorsal row 5 and lower half of row 6; acters (Cadle, 1999: table 5), i.e., number of two broad light brown to creamish paravertebral maxillary teeth (Liophidium 26-33; Pararhad- stripes on dorsal scale rows 6-8; a dark brown inaea 13-14) and size of dentary teeth (Lio- vertebral line on dorsal scale rows 8 and 9. The phidium: all dentary teeth subequal; Pararhad- ventrals are creamish white, each with a large, inaea: posterior dentary teeth larger and more centered, oval, black patch that covers most of robust than anterior; less than 10 anterior den- the scale. The dark blotches form a row from tary teeth). The comparably large number of the first onto the penultimate ventral. Ultimate at least 23 maxillary teeth in L. maintikibo is ventral, cloacal plate and subcaudals without nearly within the above given range for Lio- black central markings. phidium and clearly outside of the range of Pararhadinaea. Molecular data also place L. maintikibo near L. therezieni, and close to other Discussion species such as L. torquatum, which have unan- imously been assigned to the genus Liophidium Liophidium maintikibo resembles Pararhadi- (e.g., Guibé, 1958; Domergue, 1984a; Ziegler naea melanogaster (including P. m. maroje- et al., 1996; Cadle, 1999; Glaw and Vences, jyensis) in several external characters: small to- 2007). Nevertheless, the formal allocation of tal length (up to 290 mm in P. melanogaster), L. maintikibo to Liophidium remains somewhat a similar number of ventral and subcaudal scales provisional due to the lack of L. trilineatum (147-180 ventrals and 41-45 subcaudals in P. Boulenger, 1896 (the type species of Liophid- melanogaster), lack of a loreal scale, only seven ium according to Williams and Wallach, 1989) upper labials, a dorsal pattern of five dark lon- and Pararhadinaea melanogaster in the molec- gitudinal stripes, a belly pattern consisting of a ular analysis. single row of large dark patches from the first to Liophidium maintikibo is currently known the penultimate ventral and an immaculate ven- from a single specimen, L. therezieni from seven tral tail. specimens, and Pararhadinaea melanogaster Cadle (1999) already stressed the close re- from five specimens. In almost all cases only a lationships of Liophidium and Pararhadinaea. single specimen of these species was collected Both genera mainly differ in dentition char- from one locality. Nevertheless, our data indi- 182 M. Franzen et al. cate that the extent of occurrence of these snakes Domergue, C.A. (1984b): Notes sur les serpents de la région is not necessarily small. P. melanogaster and malgache. 4. Le genre Pararhadinaea Boettger, 1898. Descriptions d’une espèce et d’une sous-espèce nou- L. therezieni may in fact occur across northern velles. Bull. Mus. Natn. Hist. Nat., Paris 6: 149-157. Madagascar, and L. maintikibo (if the Ampi- Glaw, F., Vences, M. (1994): A Fieldguide to the Amphib- joroa locality is confirmed) across a wide range ians and Reptiles of Madagascar, 2nd Edition. Köln, Vences and Glaw Verlag. in the West and North West. Whether the ex- Glaw, F., Vences, M. (2007): A Field Guide to the Am- treme rareness of captures reflects real rareness phibians and Reptiles of Madagascar, 3rd Edition. Köln, of these snakes in their environments or secre- Vences and Glaw Verlag. tive habits remains to be studied. Glaw, F., Nagy, Z.T., Franzen, M., Vences, M. (2007): Mole- cular phylogeny and systematics of the pseudoxyrhophiine snake genus Liopholidophis (Reptilia, Colubridae): evolution of its exceptional sexual dimorphism and de- Acknowledgements. We are grateful to Ruth Kühband- scriptions of new taxa. Zoologica Scripta 36: 291-300. ner who prepared the drawings and to Ivan Ineich, Gun- Glaw, F., Nagy, Z.T., Vences, M. (2007): Phyloge- ther Köhler and Franz Tiedemann for the loan of or access netic relationships and classification of the Malagasy to type specimens. Josef Friedrich Schmidtler kindly trans- pseudoxyrhophiine snake genera Geodipsas and Comp- ported material to Munich. We thank Frontier-Madagascar sophis based on morphological and molecular data. (The Society for Environmental Exploration) for the per- Zootaxa 1517: 53-62. manent loan of specimens collected during various surveys Guibé, J. (1958): Les serpents de Madagascar. Mem. Inst. and especially Steven Megson for his invaluable help in Sci. Madagascar 12: 189-260. the field. We are also grateful to the Malagasy authorities Mori, A., Ikeuchi, I. (2006): A Photographic Guide to the for issuing research and export permits. The new species Reptiles and Amphibians of Ampijoroa. Kyoto Univer- was found during a Tropical Biology Association Course sity, Université d’Antanarivo, ANGAP, Durrell Wildlife held in Kirindy Forest. We thank Rosie Trevelyan and Pi- Conservation Trust. otr Lukasik. ZTN acknowledges the financial support of the Nagy, Z.T., Joger, U., Wink, M., Glaw, F., Vences, M. Synthesys programme (6th FP of the EC). (2003): Multiple colonization of Madagascar and Soco- tra by colubrid snakes: evidence from nuclear and mitochondrial gene phylogenies. Proc. Roy. Soc. Lond. B 270: 2613-2621. References Nylander, J.A.A. (2004): MrModeltest v2. Program distributed by the author. Uppsala University, Evolutionary Bi- Burbrink, F.T., Lawson, R., Slowinski, J.B. (2000): Mito- ology Centre. chondrial DNA phylogeography of the polytypic North Raxworthy, C.J., Nussbaum, R.A. (1994): A review of the American ratsnake (Elaphe obsoleta): a critique of the Madagascan snake genera Pseudoxyrhopus, Pararhad- subspecies concept. Evolution 54: 2107-2118. inaea and Heteroliodon (Squamata: Colubridae). Misc. Cadle, J.E. (1996): Snakes of the genus Liopholidophis Publ. Mus. Zool. Univ. Michigan 182: I-IV + 1-37. (Colubridae) from eastern Madagascar: new species, Ronquist, F., Huelsenbeck, J.P. (2003): Mrbayes 3: Bayesian revisionary notes and estimate of phylogeny. Bull. Mus. phylogenetic inference under mixed models. Bioinfor- Comp. Zool. 154: 369-464. matics 19: 1572-1574. Cadle, J.E. (1999): The dentition, systematics, and phy- Sambrook, J., Fritsch, E.F., Maniatis, T. (1989): Molecular logeny of Pseudoxyrhopus and related genera from Cloning: A Laboratory Manual. Cold Spring Harbor, Madagascar (Serpentes: Colubridae), with descriptions NY, Cold Spring Harbor Laboratory. of a new species and a new genus. Bull. Mus. Comp. Swofford, D.L. (2002): PAUP*. Phylogenetic Analysis Us- Zool. 155: 381-443. ing Parsimony (*and other Methods), Version 4. Sunder- D’Cruze, N., Sabel, J., Green, K., Dawson, J., Gardner, C., land, Massachusetts, Sinauer Associates. Robinson, J., Starkie, G., Vences, M., Glaw, F. (2007): Williams, K.L., Wallach, V. (1989): Snakes of the World. The first comprehensive survey of amphibians and rep- Volume I. Synopsis of Snake Generic Names. Malabar, tiles at Montagne des Français, Madagascar. Herp. Con- Krieger Publishing Company. serv. Biol. 2: 87-99. Ziegler, T., Vences, M., Glaw, F., Böhme, W. (1996): de Queiroz, A., Lawson, R., Lemos-Espinal, J.A. (2002): Remarks on the genital morphology of the Malagasy Phylogenetic relationships of North American garter snake genus Liophidium (Reptilia, Serpentes, Colubri- snakes (Thamnophis) based on four mitochondrial dae). Acta Biol. Benrodis 8: 157-159. genes: how much DNA sequence is enough? Mol. Phyl. Evol. 22: 315-329. Domergue, C.A. (1984a): Notes sur les serpents de la ré- Appendix: Comparative material examined gion malgache. 3. Description de trois espèces nouvelles rapportées au genre Liophidium Boulenger, 1896. Bull. Liophidium therezieni: MNHN 1982.444 (holotype of Mus. Natn. Hist. Nat., Paris 5: 1109-1122. Liophidium therezieni), male, Antsiranana prov., Foret A new black-bellied snake (Pseudoxyrhophiinae: Liophidium) 183 d’Anatelo (Ankarana), coll. Y. Therezien, 14.02.1966; Liophidium vaillanti: NMW 16860:1 [female], NMW ZSM 2053/2007, female, Antsiranana prov., Montagne des 16860:2 [male] (syntypes of Wernerodakaria subpunctata), ◦ ◦ Français at 12 19.59 S, 49 20.60 E, 232 m elevation, coll. “Dakar, Senegambien” (in error), coll. Zechmeister; SMF K.G. Green, P. Cowling and several Frontier volunteers, 17152 (lectotype of Idiophis vaillanti var. extensa), male, 24.01.2006; UADBA uncatalogued (field number FGZC “Madagascar”, coll. A. Voeltzkow, 1906. 1717), female, Antsiranana prov., Montagne des Français, Pararhadinaea melanogaster: UADBA 18586, adult, “Frontier base camp” approximately 1.5 km (air distance) Antsiranana prov., Ankarana Special Reserve, “American ◦ ◦ SW of Andavakoera at 12 19.948 S, 049 21.156 E, 200 Camp”, 2.6 km E Andrafiabe at 12◦55.9S, 49◦03.4E, 30 m elevation, coll. E. Randriamalala, 10.02.2006; ZSM m elevation, coll. A.P. Raselimanana and M. Razafimpa- 1612/2008 (field number FGZC 1911), female, Antsiranana hanana, 24.01.2001; UADBA 30054 (field number APR prov., Ampombofofo region north of Anjiabe, “Frontier 06386), juvenile, Antsiranana prov., Diana region, Am- ◦ ◦ base camp” at 12 05.528 S, 049 19.485 E, 28 m elevation, bilobe district, Andranotsimaty forest (Daraina Conserva- coll. R. Devas, 10.08.2006; ZSM 1613/2008 (field number tion Site) at 13o10.7S, 49o42.0E, 150 m elevation, coll. A. FGZC 1841), juvenile, Antsiranana prov., Baie des Sakalava Raselimanana, 1994. ca. 5 km SE of Ramena at 12◦16.338S, 49◦23.237E, 25 m elevation, coll. S. Megson, 25.02.2008; UADBA 00726 Received: April 18, 2008. Accepted: December 12, 2008. (field number APR 03026), female, no locality data available.