Remarkable records of amphibians and reptiles on Madagascar s central high plateau
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1 Tropical Zoology 20: 19-39, 2007 Remarkable records of amphibians and reptiles on Madagascar s central high plateau F. Andreone 1, M. Vences 2, F. Glaw 3 and J.E. Randrianirina 4 1 Museo Regionale di Scienze Naturali, Via G. Giolitti 36, Torino, Italy ( f.andreone@libero.it) 2 Division of Evolutionary Biology, Zoological Institute, Technical University of Braunschweig, Spielmannstr. 8, Braunschweig, Germany ( m.vences@tu-bs.de) 3 Zoologische Staatssammlung, Münchhausenstr. 21, München, Germany ( Frank.Glaw@zsm.mwn.de) 4 Parc Botanique et Zoologique de Tsimbazaza, BP 4096, Antananarivo 101, Madagascar ( randrianirina_herpeto@yahoo.fr) Received 12 May 2005, accepted 31 August 2006 We present data on the herpetofauna from the high plateau of Madagascar, based upon recent survey work and analysis of the literature. We visited several sites during a field survey of the critically endangered harlequin mantella, Mantella cowani Boulenger 1882, in the Antoetra and Antratrabe regions. The habitats of the high lands are currently quite altered and only a few spots present a certain degree of forest coverage. At these sites, we discovered several taxa that were little known thus far, not yet recorded for central Madagascar, or possibly still undescribed. M. cowani was found at four sites, although with differences in abundance. Other remarkable species are the frogs Boophis ankaratra Andreone 1993, B. elenae Andreone 1993, and B. rhodoscelis Boulenger 1882, as well as the possibly new species Boophis sp. 2 (aff. boehmei Glaw & Vences 1992), B. sp. 1 (aff. ankaratra), and Gephyromantis sp. (cf. plicifer Boulenger 1882). A further search for M. cowani was also done in the Ambatodadama area (near Antsirabe), where it was formerly known, based upon specimens housed in the Paris Museum. We did not confirm this species at this site, but we found Mantella betsileo (Grandidier 1872): this is the first recent record for this species from a highaltitude locality in central Madagascar, indicating that its type locality ( Pays Betsileo ) is not erroneous, as formerly believed. Most of the species found on the high plateau are typical of eastern rainforests, but evidence from the studied sites confirms that the original zoological assemblages from the high plateau have undergone a marked decline. The giant snake Acrantophis dumerili Jan 1860 was found at Antoetra and near Antsirabe, representing important range extensions. At Antoetra, we also found Pseudoxyrhopus imerinae (Günther 1890), which is the third known locality for this species. In the collection of the Turin museum, we found a further specimen of this rare snake, collected at Andrangoloaka at the end of the 19th century. key words: Amphibia, Reptilia, high plateau, biodiversity, Madagascar.
2 20 F. Andreone et alii Introduction Material and methods Results Discussion Herpetofauna composition on the high plateau DNA barcoding Biodiversity conservation Acknowledgements References Appendix INTRODUCTION The herpetofauna of Madagascar has been the object of considerable attention, underlined by the high number of recently published papers dealing with surveys, taxonomic revisions or conservation. Much of this research focused on species from primary habitats, i.e. rainforests and deciduous forests, repeatedly indicated as the most endangered ecosystems of the Grand Île. Although the focus of these contributions was often oriented towards defining conservation priorities, little attention has been paid to the fauna present in the residual forest parcels on the high plateau. Much of the central portion of Madagascar is heavily spoiled, due to human activity, which has caused the deforestation of this large area. Only a few forest parcels are still present on the high plateau, mainly surrounded by savannas and eroded landscapes that prevent the genetic exchange of populations of these forested islands. Due to this general alteration and generally limited attractiveness of the landscape, a poor local biodiversity has usually been assumed and few studies have dealt with the herpetofauna living on the high plateau or its relevance for the assessment of conservation priorities. Recently, we visited some high plateau sites with the aim of verifying the presence and status of populations of one of the most endangered Madagascan frog species, the harlequin mantella, Mantella cowani Boulenger 1882 (Andreone & Randrianirina 2003, Andreone et al. 2005). On this occasion, we gathered new information about the presence of other amphibian and reptile species. In the present note, we summarize the main biogeographical and biological data obtained during this survey, present a species list, comment on little known species, and discuss the possible threats to biodiversity conservation. MATERIAL AND METHODS Visited sites The surveys were carried out in 2003 and 2004 at some high plateau localities, mainly chosen because of the possible presence of Mantella cowani: (1) Soamazaka (also known as Soamahazaka; Antoetra Firaisana, Ambositra Fivondronana, Fianarantsoa Faritany), m a.s.l., S, E; visited between January This site is close to the village of Antoetra (about 2 km), and for this reason it has been intensively visited by local people to collect M. cowani (Biodev International 1996). The habitat consists of a degraded savanna, crossed by small streams with extensive grass meadows and scattered Eucalyptus trees.
3 Amphibians and reptiles from Madagascar 21 (2) Vohisokina (also known as Vohitsokina, administrative data as for [1]), m a.s.l., S, E; January 2003; savanna dominates the hilly area, while a stream with some scattered trees represents the habitat where we found the Mantella cowani population. This stream is bordered by a very narrow band of presumably original vegetation. (3) Farihimazava (also known as Farimazava, Amparimazava, or Ampasimpotsy, administrative data as for [1]), m a.s.l., S, E, 30 January-3 February This site consists of an original plateau rainforest of undetermined extension, and nearby degraded fields subjected to slash and burn agriculture, with maize, potatoes and manioc cultivations. (4) Vatolampy (also known as Maromanoa, administrative data as for [1]), m a.s.l., S, E; 3 February A montane heathland, characterized by large boulders, with percolating water. (5) Antratrabe (also known as Rianabe, Antakasina Firaisana, Ambatolampy Fivondronana, Antananarivo Faritany), S, E, m a.s.l., 9-12 February This site includes an ecotonal ridge between a fragmented forest and nearby savanna-like fields devoted to cattle pasturage and a river which forms a series of waterfalls. As usual in this area, the river is surrounded by a narrow forest band. (6) Ambatodradama (locally known as Beanjombona, Mandoto Firaisana, Antsirabe Fivondronana, Antananarivo Faritany), 925 m a.s.l., S and E; October This is an altered site with scattered gallery forests along the streams and many traveller s palms. Sites 1-4 will hereafter be pooled as Antoetra, while site 5 will be named Tsinjoarivo- Antakasina and site 6 Ambatodradama. A few more specimens were obtained from two other forest sites. They were collected by local guides, unfortunately without any data except for the local name of the sites. For this reason we do not know the metric distance or the habitat characteristics of these sites. They are: (1) a site in the Antoetra region (named Bedilolo, approximately 2 hr walking from Soamazaka), and (2) an unnamed site approximately 3 hr walking from Antratrabe. Most of the visited sites are not explicitly cited in relevant publications regarding the herpetofauna from the high plateau, although the general Antoetra denomination, found several times in the scientific literature, likely refers to some of our visited localities (sites 1-4). In particular, the Farihimazava Forest was likely the typical site for Brookesia antoetrae Brygoo & Domergue 1971, currently considered a synonym of B. thieli Brygoo & Domergue 1969 (Raxworthy & Nussbaum 1995). Moreover, some of the already known sites for Mantella cowani correspond to those we visited. For example, the Farihimazava site was cited by Biodiv International (1996) and RAkotomavo (2001). The Antratrabe site corresponds to some already reported findings and provenance localities of M. cowani given (although vaguely) by local collectors, who used to refer to it as Ankaratra area or Tsinjoarivo. The site (6) largely corresponds to the historical Betafo and Ambatodradama localities, referable to specimens housed in the Muséum National d Histoire Naturelle of Paris (Vences et al. 1999). Research and collecting techniques Amphibians and reptiles were collected by the following techniques: (1) opportunistic searches, following paths and inspecting small streams, marshes, stone walls and heaths during the day and overnight, (2) detection and tape recordings of the advertisement calls (for amphibians), with subsequent bioacoustic analysis, (3) pitfall trapping, with the installation of pitfalls and drift fences, which allowed the capture of the most secretive and fossorial amphibians and reptiles. Some of the individuals were collected as vouchers, and are now housed in the herpetological collections of Museo Regionale di Scienze Naturali (MRSN, MRSN-FAZC, and MRSN- RJS), the Université d Antananarivo, Département de Biologie Animale (UADBA), the Zoological Museum Amsterdam (ZMA), and the Zoologische Staatssammlung, München (ZSM). A list of voucher specimens is provided as an Appendix.
4 22 F. Andreone et alii Faunal comparison We compared the faunal assemblages at the newly visited sites with information on high plateau sites that could be extracted from the literature and museum collection analysis. We followed the area delimitations of Madagascar s high plateau, as provided by Raxworthy & Nussbaum (1996a), including the areas with an elevation > 800 m. Since our survey was carried out at some sites of the central portion of the high plateau, we explicitly excluded from our comparison the northernmost sites (i.e. the Tsaratanana Massif) and the southernmost sites (i.e. the Andohahela Massif). Thus, for comparison we included the following data: (1) Andringitra Massif and nearby areas (Raxworthy & Nussbaum 1996b, Raselimanana 1999), (2) Ankaratra Massif and nearby areas (Vences et al. 2002), (3) Ambohitantely Forest (Vallan 2000, 2003), (4) Itremo Massif (unpublished data of M. Vences and D.R. Vieites, and data summarized in Glaw & Vences 1994). Furthermore, we also present data for another high plateau forest, (5) Andrangoloaka, near Mantasoa Lake, using the information provided with the specimens that are currently preserved in MRSN, and referring to captures obtained at the end of the 19th century (Peracca 1892, 1893) and partly published by Gavetti & Andreone (1993). This was a typical high plateau forest, likely in continuity with the large Mandraka Forest. At that time, the site was at least partly covered by a plateau rainforest, of which there are now only a few remnants. Nowadays this name refers to a small forested parcel near Mantasoa Lake, an artificial basin created in the 1930s. According to Cadle (1996a, 1996b), the site co-ordinates are S, E (Moramanga Fivondronana, Toamasina Faritany). Recently (January 2000), one of us (F. Andreone) visited the area (at S, E) and found that a very small portion of the Andrangoloaka Forest still exists, although it is greatly reduced. Fig. 1 is an overall map of Madagascar, including the main localities cited in the text. Taxonomic determination and nomenclature Species determination was based on a comparison with other preserved material, mainly housed in the reference collections of the authors institutions. For the amphibians, we also compared the acoustic recordings with our reference call collection. Finally, we compared the DNA from ethanol-fixed tissues with an available reference database (Vences et al. 2005). Muscle tissue samples were taken from freshly collected specimens and preserved in 98% ethanol. DNA was extracted using different standard protocols and a fragment of the mitochondrial 16S rrna gene was amplified using the primers 16Sa-L and 16Sb-H of Palumbi et al. (1991). After purification (Qiagen kits), the fragments were resolved on automated DNA sequencers (ABI 377 and ABI 3100). Sequences were validated and aligned with the software Sequence Navigator (Applied Biosystems), and deposited in Genbank (accession numbers of newly obtained sequences from Antoetra specimens: AY324817, AY848078, AY AY848117, AY848122, AY AY848133, AY848208, AY AY848222, AY AY848272, AY848380, AY848415, AY848418, AY AY848438, AY848469, AY AY848554, AY AY848573, AY848589, AY848590, AY848591, AY AY848602, AY848616, AY848617, AY AY883991, AY883994, AY883995). For the taxonomy and nomenclature, we followed Glaw & Vences (1994) and recent literature, such as the new mantellid classification provided by Glaw & Vences (2006). For the gender of the chameleon named Calumma, we followed Lutzmann & Lutzmann (2004) in considering it neuter. RESULTS In total, we recorded 49 species (Table 1), of which 42 were found at Antoetra, 21 at Antratrabe and 14 at Ambatodradama. Clearly, these numbers are not exhaus-
5 Amphibians and reptiles from Madagascar 23 Fig. 1. The map of Madagascar, with the localities visited during the survey work (in black), and those cited in the text of relevant literature (in grey).
6 24 F. Andreone et alii Table 1. List of the species found during the survey work on the central high plateau of Madagascar. HYPEROLIIDAE Antoetra Antratrabe 1S 2S 3S 3F 4S 4F 5 Ankaratra 1 Heterixalus betsileo Heterixalus rutenbergi PTYCHADENIDAE 3 Ptychadena mascareniensis MANTELLIDAE Ambatodradama Ambohitantely Andringitra Ivohibe Itremo Andrangoloaka 4 Boophis ankaratra ? 5 Boophis elenae + 6 Boophis goudoti Boophis marojezensis + 8 Boophis microtympanum Boophis rhodoscelis Boophis sp. 1 (aff. ankaratra) + 11 Boophis sp. 2 (aff. boehmei) Boophis tephraeomystax + 13 Gephyromantis sp. 1 (aff. blanci) 14 Gephyromantis sp. (aff. plicifer) + 15 Guibemantis liber Mantella baroni Mantella betsileo + 18 Mantella cowani Mantidactylus alutus Mantidactylus brevipalmatus Mantidactylus curtus Mantidactylus femoralis (continued)
7 Amphibians and reptiles from Madagascar 25 Table 1. (continued) Antoetra Antratrabe Ankaratra Ambatodradama Ambohitantely Andringitra Ivohibe Itremo Andrangoloaka 23 Mantidactylus lugubris Mantidactylus cowani + 25 Mantidactylus zipperi Blommersia kely Spinomantis peraccae MICROHYLIDAE 28 Platypelis pollicaris Plethodontohyla notosticta + 30 Plethodontohyla tuberata + + CHAMAELEONIDAE 31 Calumma brevicorne Calumma gastrotaenia Calumma nasutum Calumma oshaughnessyi Furcifer campani Furcifer lateralis Furcifer willsii + + GEKKONIDAE 38 Phelsuma barbouri SCINCIDAE 39 Amphiglossus sp. (aff. macrocercus) Mabuya madagascariensis OPLURIDAE 41 Oplurus quadrimaculatus GERRHOSAURIDAE 42 Zonosaurus ornatus (continued)
8 26 F. Andreone et alii Table 1. (continued) Antoetra Antratrabe Ankaratra Ambatodradama Ambohitantely Andringitra Ivohibe Itremo Andrangoloaka BOIDAE 43 Acrantophis dumerili + + COLUBRIDAE 44 Geodipsas infralineata Liopholidophis lateralis Liopholidophis sexlineatus Madagascarophis colubrinus Mimophis mahfalensis + 49 Pseudoxyrhopus imerinae + + The list reports those species recorded at sites 1-5 (shaded in grey), and their occurrence at other comparative sites (Ankaratra, Ambohitantely, Andringitra, Itremo, Andrangoloaka). At each of these sites, many other species have been recorded that were not found in the present survey and are not included in the table. The occurrence of Boophis goudoti, Mantidactylus curtus, M. brevipalmatus, and M. zipperi at Andringitra Massif is given in a preliminary way. Most of the populations attributed to these species and coming from this massif appear to be already sufficiently differentiated to warrant another specific attribution. Snake specimens of Madagascarophis from Andringitra and Antoetra belonged to M. meridionalis, but records from other localities have not been reliably identified so far. (?) The record of Boophis ankaratra at Andrangoloaka is provided in a preliminary way, since the collected specimen only partially matches the known colouration of the species. 1, Soamazaka; 2, Vohisokina, 3, Farihimazava; 4, Antratrabe; 5, Ambatodradama; Ankaratra, Ankaratra Massif (according to Vences et al. 2002), Ambohitantely, Ambohitantely Forest (Vallan 2000, 2003; M. Vences & F. Glaw unpubl. obs.); Andringitra-Ivohibe, Andringitra Massif, Ivohibe Forest, and connecting corridor (Raselimanana 1999), Itremo, Itremo Massif (M. Vences unpubl. obs.) Andrangoloaka, Andrangoloaka Forest (Gavetti & Andreone 1993; F. Andreone unpubl. obs., and unpubl. historical catalogues). Occurrence in forest (F) and savanna (S) is also given.
9 Amphibians and reptiles from Madagascar 27 tive herpetofaunal inventories but give indications about the relative community diversity. Some of the amphibian and reptile species found during our survey are new records for the high plateau, while others represent a significant range extension of the known distribution area. In fact, of the total number of species found at Antoetra, 20 were known from the Ankaratra region, 28 from the Andringitra Mas- Fig. 2. Some of the most remarkable amphibians and reptiles from the visited high plateau sites. (A) Gephyromantis sp. 2 (aff. plicifer), Antratrabe Forest (MRSN A2243); (B) Boophis rhodoscelis, Antratrabe (MRSN-FAZC 11584); (C) Boophis sp. 1 (aff. ankaratra), Farihimazava Forest, Antoetra region (MRSN A2274); (D) Acrantophis dumerili, Soamazaka, Antoetra region (specimen housed in the Université d Antananarivo, Département de Biologie Animale); (E) Pseudoxyrhopus imerinae from Vohisokina, Antoetra region (MRSN R2215); (F) Pseudoxyrhopus imerinae from Vohisokina, Antoetra region (MRSN R2215), ventral side.
10 28 F. Andreone et alii sif, 20 from Ambohitantely, 13 from Itremo and 18 from Andrangoloaka. For several of the remaining species, the present finding represents a novel distribution record for the whole plateau area, and often a considerable range extension. Here we give some additional information on the most relevant taxa. In Fig. 2 we report some remarkable species found during the survey, while Fig. 3 includes photographs of four individuals of Mantella cowani and putative hybrids. Gephyromantis sp. 2 [aff. plicifer (Boulenger 1882)] At Farihimazava, we found some individuals of a Gephyromantis that are very similar to those from Ranomafana and Andohahela attributed to Gephyromantis plicifer (Fig. 2A). According to Vences & Glaw (2001), the most relevant characters to distinguish G. plicifer from the similar G. luteus (Methuen & Hewitt 1913) and G. sculpturatus (Ahl 1929) are (1) its large body size, and (2) extent of the femoral glands. The analysed individuals (MRSN A2243 and A2244) reached respectively 44.2 and 36.1 SVL, and their femoral glands measured 10.2 and 9.3 (length) and 5.5 and 4.3 mm (width), and thereby agree with individuals from Ranomafana and Andohahela. However, there were distinct genetic differences (8% uncorrected pairwise sequence divergence in the 16S rrna gene), suggesting that they may represent another, still unidentified, species. Fig. 3. (A) The individual of Mantella cowani found at Antratrabe (MRSN A3200); (B-D) three putative hybrids Mantella cowani Mantella baroni from Farihimazava, Antoetra region (not collected).
11 Amphibians and reptiles from Madagascar 29 Mantella baroni Boulenger 1888 The species was found at Farihimazava, where it hybridises with M. cowani (Chiari et al. 2005). The Farihimazava area is also remarkable in being the highest currently known site (1400 m a.s.l.) for this species. It was also found at two further sites which unfortunately are not identifiable by geographical coordinates. They are Bedilolo, near Soamazaka (Antoetra), and the site about 3 hr walking from Antratrabe. Mantella betsileo (Grandidier 1872) Two individuals of this species (MRSN A ) were found in the Ambatodradama area. This finding represents an important novelty in terms of geographic distribution, since the type specimens come from Pays des Betsileos, an indication that refers to the central-southern area of Madagascar, in Fianarantsoa Province (Vences et al. 1999), not far from the newly discovered locality. Previously, no M. betsileo population has been recorded in the eastern forests south of Nosy Boraha Island. The collecting site of the two specimens is near Ambatodradama Antsirabe in Imerina country (Antananarivo Province), and marks the only contemporary finding of M. betsileo on Madagascar s high plateau. This finding suggests that the type locality of this species is not erroneous and thus might help to clarify the nomenclature and identity of M. betsileo. Mantella cowani Boulenger 1882 This is considered the most endangered frog species of Madagascar, since its distribution area is limited to a few high plateau localities and until recently subject to intense collecting for the pet rade (Andreone & Randrianirina 2003, Andreone et al. 2005, Andreone et al. 2006). Here we confirm its presence in two areas: one around Antoetra and the other at Antratrabe. The single specimen collected at the latter locality was characterised in having the spots at the attachment of legs shading to orange (Fig. 3A), and not bright red as in specimens from other populations. This locality (Antratrabe) was already known by local collectors and exporters, and was vaguely named (e.g. Tsinjoarivo, Tsinjoarivo-Antakasina, Ankaratra), but had not been confirmed by any survey or voucher specimen. We were unable to confirm the presence of the species at two other sites reported in the literature and supported by voucher specimens at the Muséum National d Histoire Naturelle, Paris, namely Betafo-Ambatodradama and Itremo. The environmental conditions at all the visited sites where the species was confirmed were quite similar, consisting of a montane savanna, mostly of anthropogenic origin. The harlequin mantella was present in low densities (from single individuals to less then 30 specimens found at Vohisokina during 5 days of research) along streams and wet stone walls with percolated water. In general, it was very secretive, hiding in the crevices and cavities along the streams, from which the males emitted their calls. At Farihimazava, M. cowani was syntopic with M. baroni: specimens chromatically attributable to M. cowani, as well as putative hybrids were also observed (Fig. 2B-D). The hybrids showed a different degree of intergradation in colouration between the parental species. Some individuals had a general colour pattern more typical of M. cowani,
12 30 F. Andreone et alii with black dorsum and relatively small axillary and inguinal yellow or orange spots. Other individuals had the spots more yellowish or greenish, instead of red, as in M. cowani. Some other individuals were more similar to M. baroni, lacking the frenal stripes. Irregular and atypical light (yellowish) spots were sometimes present on the head, under the eyes. A detailed genetic analysis of this population has been provided elsewhere (Chiari et al. 2005), while more detailed information on demography, age structure and morphometry will be provided in forthcoming papers. Mantidactylus zipperi Vences & Glaw 2004 Two individuals (MRSN A2337 and A2295) came from Farihimazava forest. They agree with the original description of this species (Vences & Glaw 2004) which was until recently included within Mantidactylus albofrenatus (Müller 1892). This locality represents a new record for this little known terrestrial frog. Boophis ankaratra Andreone 1993 Some individuals of a small green Boophis Tschudi 1838 were heard and/or observed at the visited Antoetra sites, in residual vegetation formations along streams in open areas. At Soamazaka and Vohisokina, we tape-recorded the calls, which fit perfectly with the acoustic repertoire of B. ankaratra from the typical site (Manjakatompo). Boophis sp. 1 (aff. ankaratra Andreone 1993) At Farihimazava, we also heard several calls in open areas that were similar to the typical B. ankaratra call. Unfortunately, we were not able to collect any of these specimens. On the other hand, we recorded, observed, and photographed some individuals of a small green Boophis within the forest at Farihimazava, which, at a first glance, was not similar to B. ankaratra. The calls of these individuals were not the fast croaking ones characteristic of B. ankaratra, but were slower and trilling. Although a detailed analysis of this call type is beyond the scope of the present paper, the individuals from the Fahirimazava forest (but not those from the open areas that were ascribed to B. ankaratra) were considered as belonging to a still undescribed species. The analysed individuals and associated tissue samples (MRSN A ) showed a 2.3% sequence divergence from B. ankaratra (12 mutations) and 3.3% divergence from B. schuboeae Glaw & Vences 2002 (18 mutations), suggesting that this might be a separate taxonomic unit, here named Boophis sp. 1. Finally, at Antakasina, we tape-recorded and collected a specimen (MRSN A2274) that matched B. ankaratra. Boophis elenae Andreone 1993 At Farihimazava, we found and tape-recorded a male of this species, which until now was only reliably known for the Ranomafana and Ifanadiana areas (Andreone 1993). The Antoetra area represents the northernmost record of the
13 Amphibians and reptiles from Madagascar 31 species. The DNA sequence of the specimen from Antoetra (MRSN A2296) agreed (0% sequence divergence) with others from Maharira Forest (next to Ranomafana), close to the type locality of this species (M. Vences unpublished). According to our current knowledge, B. elenae is a complex of at least two divergent species of great morphological similarity; one with a series of horizontal reddish-brownish stripes on the iris (as the holotype of B. elenae), the other with a dirty grey-brown-reddish iris. The Antoetra specimen genetically agrees with the typical B. elenae. Boophis sp. 2 (aff. boehmei Glaw & Vences 1992) Boophis boehmei was formerly known from a few eastern localities (e.g. Andasibe, Ankeniheny and Ambalamarina; Glaw & Vences 1994). The DNA sequences of the Antoetra specimens showed differences from those from Andasibe, as well as from those of the morphologically similar B. rufioculis Glaw & Vences 1997 from its type locality (An Ala). They were similar to some sequences from Ranomafana assigned to B. boehmei (ZMA 20193) (3 mutations, 0.5% divergence) but strongly divergent from others (ZMA and UADBA 20702, 20703, 20705, 20708) (9%) and from typical boehmei (about 7%). This suggests the presence of at least one probably two new species in the central-eastern region and indicates a need for taxonomic revision of this species complex. Boophis microtympanum (Boettger 1881) The DNA sequences of B. microtympanum from Antoetra showed a relevant differentiation from those of the Ankaratra Massif (1.7% divergence), but were similar to other populations from relatively low altitudes at Ranomafana and Cirque Namoly, Andringitra. This suggests a process of altitudinal gradient speciation in this species that requires further study. Boophis rhodoscelis (Boulenger 1882) This is a poorly known species. We found specimens at two of the visited localities (Farihimazava and Antratrabe) outside the rainforest. These specimens (MRSN A2292, A2319) agree genetically (0% divergence) with those from Vohiparara (next to Ranomafana) which are characterized as B. rhodoscelis, especially by a greyish marbling on the throat and (less developed) on the belly. Heterixalus rutenbergi (Boettger 1881) Despite the attractive colouration which makes this high plateau species easy to recognize, it was until recently known from only a few localities. Because it is a non-forest species, H. rutenbergi has not been recorded in most highland herpetological surveys, which did not focus on unforested areas. The known localities (according to Raharivololoniaina et al. 2003) are besides Antratrabe Ambohitantely, Mantasoa, Ambatolampy, Tsinjoarivo and Ambatofitoharanana.
14 32 F. Andreone et alii Calumma brevicorne (Günther 1879) This chameleon was found at two of the visited forest sites, namely Farihimazava (MRSN R2098) and Antratrabe (MRSN R2314). Both specimens appeared to belong to the nominal subspecies and did not present the divided occipital lobes described for the subspecies C. b. tsarafidyi Brygoo & Domergue 1970, whose collecting locality (Tsarafidy Forest, Ambohimasoa) is not far from Antoetra. Acrantophis dumerili Jan 1860 Although this boa is usually known from western and arid localities, as reported by Vences & Glaw (2003), we observed it on two occasions. The first refers to an individual obtained via local collectors, who likely collected it in open habitats near Soamazaka (Fig. 2D). The second specimen was found at Amboloandro (Ambatondradama, near Antsirabe; photographed by J.E. Randrianirina). These findings represent the easternmost and northernmost localities in eastern Madagascar. Pseudoxyrhopus imerinae (Günther 1890) This colubrid snake was thus far known from only a few specimens. Raxworthy & Nussbaum (1994) reported: (1) four specimens coming from Madagascar, (2) the holotype (provenance given as in the forest district east of Imerina, Madagascar ), (3) a specimen from Ananokely, Ankaratra, and (4) a specimen from Mont Ibity, 2200 m. Thus, only two precise localities were known for this apparently rare species, characterised and distinguished from the other Pseudoxyrhopus Günther 1881 by having 19 scale rows at midbody (versus 21-25). During our former surveys at Ankaratra (Vences et al. 2002) and Mt. Ibity (M. Vences et al. unpublished 2003), we did not find this species. Hence the collection of one specimen at Vohisokina/Antoetra (MRSN R2215) represents a remarkable observation and the first photographic documentation of a living specimen (Fig. 2E). The individual is a female of 454 mm total length (weight 50 g), found next to a small stream in open grassland (hr 17.30) while preying upon eggs laid by a lizard, presumably Oplurus quadrimaculatus Duméril & Bibron 1851 (10 eggs, MRSN- FAZC 11427). As seen in Fig. 2E-F, the living specimen had a light-brownish back with five longitudinal blackish lines, the middorsal being wider than the others and more shading towards brownish. The head is darker, with a whitish stripe bordered in black, running from the jaw articulation to the posterior edge of the eye (4th supralabial). The 1st, 2nd, and 3rd supralabials are lighter than the other scales of the head, with a blackish pattern on the lower parts. The ventral parts of the body are dark-greyish-bluish, mottled with black and pink. While analysing the Pseudoxyrhopus specimens housed in the historical collection at Turin Museum, we found another specimen fitting the meristic and morphometric characters of P. imerinae. This specimen (MZUT R1665) was obtained from Andrangoloaka and included in the collection under the name P. quinquelineatus (Günther 1881) (Elter 1982). Surprisingly, two other specimens, instead attributed to P. imerinae (erroneously given as P. imerina by Elter 1982), turned out to belong to P. quinquelineatus. We suspect that this reflects mislabelling, and that initially the three specimens were correctly assigned. For a rapid comparison, we report
15 Amphibians and reptiles from Madagascar 33 Table 2. Morphological and meristic characters of Pseudoxyrhopus imerinae and P. quinquelineatus housed in the Turin Museum. Species P. imerinae P. quinquelineatus Acronym and museum number MRSN R2215 MZUT R1665 MZUT R MZUT R Sex Total length Tail length (trun-cated) (truncated) Head width Head length Neck width Eye horizontal diameter Distance eye snout tip Supraoculars 1/1 1/1 1/1 1/1 Preoculars 1/1 1/1 1/1 1/1 Primary temporals 1/1 1/1 1/1 1/1 Secondary temporals 2/2 2/2 2/2 2/2 Tertiary temporals 3/3 3/3 3/3 2/2 Loreal 1/1 1/1 1/1 1/1 Scales surrounding the parietals * 10/10 10/10 11/11 11/11 Scales surrounding the eye 6/6 6/6 6/6 6/6 Postoculars 2/2 2/2 2/2 2/2 Supralabials 8/8 8/8 8/8 8/8 Supralabials in contact with the eye 4th and 5th 4th and 5th 4th and 5th 4th and 5th Infralabials 9/10 9/9 9/9 9/9 Infralabials in contact with anterior inframaxillary scales Dorsals at forebody, midbody and precloacal zone * 5/4 4/4 4/4 4/4 19/19/17 19/19/17 21/21/19 21/21/19 Ventrals Anal Divided Undivided Divided Divided Subcaudals * Dorsal colouration * Brownish Brownish Width of mid-dorsal (3rd) line * Larger and lighter Larger and lighter Belly colouration * Blackish Blackish Brownyellowish Same width and same colour Brownyellowish Same width and same colour Yellowishunpigmented Yellowishunpigmented Metric measurements in mm (precision: 0.1 mm). Paired values separated by a slash indicate left and right measurements. Asterisked values indicate the parameters that are likely diagnostic for specific recognition. the main morphometric and meristic characters of the new specimens in Table 2. MZUT R1665 is similar in scalation to the newly captured specimen, with 19 scales at midbody, and with colouration that was probably similar when freshly obtained
16 34 F. Andreone et alii but is now a little bit faded. The two P. quinquelineatus specimens are much more yellowish, and with a light-yellowish venter (versus blackish in P. imerinae), although presumably collected on the same occasion. MZUT R has a light dorsum with five contrasting brownish lines, more or less of the same width, while MZUT R has less visible dorsal lines. Both specimens have 21 scale rows at midbody. Whether P. imerinae and P. quinquelineatus are distinct species is debatable, taking into consideration the overall similarity in morphology and habitat. However, the scalation at midbody (19 scales in P. imerinae versus 21 in P. quinquelineatus), the number of scales around parietals (10 versus 11), and the colouration differences (black belly versus light belly) support their specific distinctness. DISCUSSION Herpetofauna composition on the high plateau The amphibians and reptiles found at Antoetra and Antratrabe represent a typical montane herpetofauna, with many species already known from other plateau habitats (Raxworthy & Nussbaum 1996a, 1996b). This faunal assemblage is also similar to that of the eastern rainforests but appears to be impoverished, likely as a consequence of the deforestation and habitat alteration occurring on the high plateau and of the absence of species that are ecologically restricted to lower elevations. In fact, species typical of rainforest were found only in the forest fragments of Farihimazava and Antratrabe. The forest species we recorded during our survey were: Boophis elenae, B. marojezensis Glaw & Vences 1994, B. sp. 2 (aff. boehmei), Mantidactylus femoralis (Boulenger 1882), Gephyromantis sp. 1 [aff. blanci (Guibé 1974)], G. sp. 2 (aff. plicifer), Guibemantis liber (Peracca 1893), M. opiparis (Peracca 1893), M. peraccae (Boulenger 1896), Platypelis pollicaris Boulenger 1888, Calumma brevicorne, C. gastrotaenia (Boulenger 1888), C. nasutum (Duméril & Bibron 1836), C. oshaughnessyi (Günther 1881). Throughout the survey, we never found these species in open areas without forest coverage, and thus we consider them as good indicators of the persistence of the original forest. The species more typical of montane savannas and gallery habitats along the streams were a more adaptable assemblage: Heterixalus betsileo (Grandidier 1872), H. rutenbergi, Boophis microtympanum, Mantella cowani, Mantidactylus alutus (Peracca 1893), M. brevipalmatus Ahl 1929, M. kely Glaw & Vences 1994, Ptychadena mascareniensis (Duméril & Bibron 1841), Plethodontohyla tuberata (Peters 1883), Furcifer campani (Grandidier 1872), F. lateralis (Gray 1831), Phelsuma barbouri Loveridge 1942, Mabuya madagascariensis Mocquard 1908, Oplurus quadrimaculatus, Liopholidophis lateralis (Duméril & Bibron 1854), L. sexlineatus (Günther 1882), and Pseudoxyrhopus imerinae. Because of their association with open environments, we consider these species primarily forest edge or grassland-specialized, as stressed by Raxworthy & Nussbaum (1996b). The only species found both in open habitat (savannas) and in forest was Mantidactylus curtus (Boulenger 1882). A similar situation was also observed for Mantella baroni at Farihimazava. There, this frog was particularly abundant in the forested area, but also occupied on a cultivated field near the forest itself. Some other species were found only in open areas, but are known from rainforest sites
17 Amphibians and reptiles from Madagascar 35 elsewhere: Boophis ankaratra, Boophis goudoti, B. rhodoscelis, M. lugubris (Duméril 1853), Furcifer willsii (Günther 1890), Amphiglossus cf. macrocercus (Günther 1882), Zonosaurus ornatus (Gray 1831), Geodipsas infralineata (Günther 1882). For these species the lack of observations in the rainforest sites of the high plateau was likely due to surveying deficiencies: we consider them primarily adapted to forest habitats, but capable to some extent of colonising open habitats a certain distance from the real forest, often following the vegetation bordering watercourses (Andreone & Randrianirina 2000). DNA barcoding Our genetic data corroborated the utility of DNA barcoding for rapid assessments of herpetofaunal biodiversity (Vences et al. 2005). Indeed, these data indicated a number of species (especially Boophis sp. 1 and Gephyromantis sp. 1) that require of more in-depth taxonomic evaluation and may represent new, undescribed species. In contrast, Antoetra specimens of other frog species were genetically very similar to supposed conspecific populations, and thus the DNA data added reliability to the records. Besides the ones listed above, this refers to Boophis marojezensis (almost identical to Ranomafana populations), B. goudoti Tschudi 1838, Blommersia kely (less than 1% divergence from Ankaratra populations), M. brevipalmatus (a single mutation compared to Ankaratra specimens). For Mantidactylus curtus, the phylogeographic situation turned out to be very complex, and further studies are required to sort out the taxonomy of this species. Biodiversity conservation Conservation concerns regarding the herpetofauna of the visited high plateau sites are similar to those already stressed for the Ankaratra and Ambohitantely assemblages (Vences et al. 2002, Vallan 2003). In particular, persistence of the forest fragments, even of small size, may be of considerable value for the survival of many species. Moreover, the size of these fragments plays a significant role in determining the diversity of the hosted fauna, and below a certain limit we cannot be certain of mid- or long-term stability of the community and species richness. Thus, any conservation measure, also taking into consideration the needs of local communities (wood, space for cultivations and cattle), should probably be addressed primarily to large fragments with streams hosting a significant herpetofaunal diversity. The Farihimazava forest is one of these priority forest fragments, and a certain effort is urgently needed to assure its conservation. The presence of the critically endangered frog Mantella cowani is another conservation priority at the visited sites (Andreone et al. 2006). Further research is necessary to get a more comprehensive vision of the distribution and occurrence of the species in the residual forest fragments and in peculiar habitats, such as montane moorlands. Considering the strong genetic differentiation detected in several of the studied amphibian species, we believe that sites of the plateau contain a reasonable number of regionally and altitudinally endemic species, some still undescribed. Therefore, taxonomic work is crucial to more precisely assess and compare the biodiversity at different sites, and to propose pertinent conservation actions.
18 36 F. Andreone et alii Acknowledgements The study on the high plateau of Madagascar was made possible by funding provided by several organisations to which we are extremely grateful: DAPTF-IUCN for the seed grants that allowed us to start the Arovy ny sahona gasy project, the Wildlife Conservation Society, the Istituto Oikos, the North American Amphibian Center, and the Nando Peretti Foundation which financed our latest research. Thanks also to BIOPAT, and Gondwana Conservation and Research. Many people helped us during our stay in Madagascar: G. Aprea, O. Behra, P. Bora, E.J. Edwards, T. Halliday, M. Hatchwell, F. Rabemanjara. V. Mercurio and M. Favelli helped with the measurements and setting of the specimens. W. Böhme, A. Dubois, and A. Ohler kindly allowed the loan of specimens housed in Bonn and in Paris. We are indebted to the Malagasy authorities for the necessary permits and export authorisations. M. Largen and D. Vallan acted as referees on a first version of this paper, making useful suggestions and remarks. REFERENCES Andreone F Two new treefrogs of the genus Boophis (Anura: Rhacophoridae) from central-eastern Madagascar. Bollettino del Museo Regionale di Scienze Naturali di Torino 11 (2): Andreone F., Cadle J.E., Glaw F., Nussbaum R.A., Raxworthy C.J., Vallan D. & Vences M Species review of amphibian extinction risks in Madagascar: conclusions from the Global Amphibian Assessment. Conservation Biology 19 (6): Andreone F., Mercurio V. & Mattioli F Between environmental degradation and international pet trade: conservation strategies for the threatened amphibians of Madagascar. Natura Società Italiana di Scienze Naturali e Museo Civico di Storia Naturale di Milano 95 (2): Andreone F. & Randrianirina J.E Biodiversity, rainforests and herpetological communities in Madagascar: what about differences between amphibians and reptiles?, pp In: Lourenço W. & Goodman S.M., Edits. Diversity and endemism in Madagascar, Mémoires de la Societé de Biogéographie. Andreone F. & Randrianirina J.E It s not carnival for the harlequin mantella! Urgent actions needed to conserve Mantella cowani, an endangered frog from the high plateau of Madagascar. Froglog 59: 1-2. Biodev International Étude de la distribution et des niveaux de populations de deux espèces de Mantella commercialisees de Madagascar. CITES Bureau Netherlands. Cadle J.E. 1996a. Snakes of the genus Liopholidophis (Colubridae) from eastern Madagascar: new species, revisionary notes, and an estimate of phylogeny. Bulletin of the Museum of Comparative Zoology 154: Cadle J.E. 1996b. Systematics of snakes of the genus Geodipsas (Colubridae) from Madagascar, with descriptions of new species and observations on natural history. Bulletin of the Museum of Comparative Zoology 155: Chiari Y., Andreone F., Vences M. & Meyer A Genetic variation of an endangered Malagasy frog, Mantella cowani, and its phylogeographic relationship to the widespread M. baroni. Conservation Genetics 6: Elter O La collezione erpetologica del Museo di Zoologia dell Università di Torino. Cataloghi V, Museo Regionale di Scienze Naturali di Torino, (1981) 116 pp. Gavetti E. & Andreone F. 1993, Revised Catalogue of the Herpetological Collection in Torino University. I. Amphibia. Cataloghi X. Museo Regionale di Scienze Naturali di Torino, Torino, 143 pp. Glaw F., & Vences M A fieldguide to the amphibians and reptiles of Madagascar. Second edition, including freshwater fish and mammals. Cologne: Vences und Glaw Verlag.
19 Amphibians and reptiles from Madagascar 37 Glaw F. & Vences M Phylogeny and genus-level classification of mantellid frogs (Amphibia, Anura). Organisms, Diversity & Evolution 6: Lutzmann N. & Lutzmann H Das grammatikalische Geschlecht der Gattung Calumma (Chamaeleonidae) und die nötigen Anpassungen einiger Art- und Unterartbezeichnungen. Reptilia 9 (4): 4-5. Palumbi S.R., Martin A., Romano S., McMillan W.O., Stice L. & Grabowski G The Simple Fool s Guide to PCR, Version 2.0. Privately published document compiled by S. Palumbi. Department of Zoology, Honolulu University. Peracca M.G Descrizione di nuove specie di Rettili e Anfibi di Madagascar. Bollettino dei Musei di Zoologia e di Anatomia Comparata della R. Università di Torino 7: 1-5. Peracca M.G Descrizione di nuove specie di Rettili e Anfibi di Madagascar. Bollettino dei Musei di Zoologia e di Anatomia Comparata della R. Università di Torino 8: Raharivololoniaina L., Vieites D.R., Glaw F. & Vences M Larval stages, habitat and distribution of the hyperoliid frog Heterixalus rutenbergi (Boettger, 1881). Alytes 21 (1-2): Rakotomavo E., Étude de la filière Mantella de Madagascar. Antanarivo: Office National pour l Environnement. Raselimanana A.P Le herpetofaune, pp In: Goodman S. & Rasolonandrasana B.P.N., Edits. Inventaire biologique de la réserve spéciale du pic d Ivohibe et du couloir forestier qui la relie au Parc national d Andringitra. Récherches pour le Développement, (Sciences Biologiques) 15: Raxworthy C.J. & Nussbaum R.A A review of the Madagascan snake genera Pseudoxyrhopus, Pararhadinaea, and Heteroliodon (Squamata: Colubridae). Miscellaneous Publications, Museum of Zoology, University of Michigan 182: Raxworthy C.J. & Nussbaum R.A Systematics, speciation and biogeography of the dwarf chameleons (Brookesia; Reptilia, Squamata, Chamaeleontidae) of northern Madagascar. Journal of Zoology, London 235: Raxworthy C.J. & Nussbaum R.A. 1996a. Montane amphibian and reptile communities in Madagascar. Conservation Biology 10: Raxworthy C.J. & Nussbaum R.A. 1996b. Amphibians and reptiles of the Réserve Naturelle Intégrale d Andringitra, Madagascar: a study of elevational distribution and local endemicity. In: Goodman S.M., Edit. A floral and faunal inventory of the eastern slopes of the Réserve Naturelle Intégrale d Andringitra, Madagascar: with reference to elevational variation. Fieldiana Zoologica (n.s.) 85: Vallan D Influence of forest fragmentation on amphibian diversity in the nature reserve of Ambohitantely, highland Madagascar. Biological Conservation 96: Vallan D Consequences of rain forest fragmentation for herpetofauna: a case study from Ambohitantely, pp In: Goodman S.M. & Benstead J.P., Edits. A natural history of Madagascar. The University of Chicago Press. Vences M., Andreone F., Glaw F., Raminosoa N., Randrianirina J.E. & Vieites D Amphibians and reptiles of the Ankaratra Massif: reproductive diversity, biogeography and conservation of a montane fauna in Madagascar. Italian Journal of Zoology 69: Vences M. & Glaw F Systematic review and molecular phylogenetic relationships of the direct developing Malagasy anurans of the Mantidactylus asper group (Amphibia, Mantellidae). Alytes 19: Vences M. & Glaw F Phylogeography, systematics and conservation status of boid snakes from Madagascar (Sanzinia and Acrantophis). Salamandra 39 (3/4): Vences M. & Glaw F Revision of the subgenus Chonomantis (Anura: Mantellidae: Mantidactylus) from Madagascar, with description of two new species. Journal of Natural History 38: Vences M., Glaw F. & Böhme W A review of the genus Mantella (Anura, Ranidae, Mantellinae): taxonomy, distribution and conservation of Malagasy poison frogs. Alytes 17 (1-2): Vences M., Thomas M., van der Meijden A., Chiari Y. & Vieites D.R Comparative performance of the 16S rrna gene in DNA barcoding of amphibians. Frontiers in Zoology 2: article 5.
20 38 F. Andreone et alii APPENDIX List of voucher specimens. Asterisks (*) indicate the specimens analysed for DNA. Abbreviations for collections: MRSN = Museo Regionale di Scienze Naturali, Torino (Italy); MRSN-FAZC and MRSN-RJS, Franco Andreone Zoological Collection, Torino (Italy); MZUT = Museo di Zoologia dell Università di Torino (collection now housed at MRSN); UADBA, Université d Antananarivo, Département de Biologie Animale, Antananarivo (Madagascar); ZMA, Zoological Museum Amsterdam, Amsterdam (The Netherlands); ZSM, Zoologische Staatssammlung München. Abbreviation of localities are given between parentheses: A = Antratrabe; ADK = Andrangoloaka; ADR = Ambatodradama; B = Bedilolo; F = Antoetra, Farihimazava; IT = Itremo, S = Antoetra, Soamazaka; V = Antoetra, Vohisokina; VT = Antoetra, Vatolampy. AMPHIBIA Hyperoliidae Heterixalus betsileo MRSN A2409 (F) Heterixalus rutenbergi MRSN A2290 (A); ZSM 789/2001 (IT) Ptychadenidae Ptychadena mascareniensis MRSN A2931 (S), A2795 (S), A2297 (A); MRSN-RJS (ADR); ZSM 719/2001 (IT) Mantellidae Boophis ankaratra MRSN A2274 (A); An3321 (ADK); ZSM 735/2001 (IT) Boophis elenae MRSN A2296* (F) Boophis goudoti MRSN A (S), A2865 (S), A2867 (S), A2249 (S), A2334 (F); A2451 (A); MZUT An (ADK); UADBA (S), (S); ZMA 19544* (S), MRSN-RJS 721 (ADR); ZSM 739/2001 (IT) Boophis marojezensis MRSN A2332, A2245* (F) Boophis microtympanum MRSN A (S), A (S), A (A), MZUT An65 (ADK) UADBA 21176, (S); ZMA 19555* (S); ZSM 722/2001 (IT) Boophis rhodoscelis MRSN A2319* (F), A2292* (F), A (A); MZUT An66 (ADK), An (ADK) Boophis sp. 1 (aff. ankaratra) (Duméril 1853) MRSN A2325*-2326* (F) Boophis sp. 2 (aff. boehmei) MRSN A2240* (A), MRSN-FAZC 11451* (F), 11453* (F) Boophis tephraeomystax MRSN A5009 (ADR) Blommersia kely MRSN A2926 (S), A2727 (S); ZMA 19551* (S) Gephyromantis sp. 1 (aff. blanci) MRSN A2256 (F) Gephyromantis sp. 2 (aff. plicifer) MRSN A2243*-2244* (F) Guibemantis liber MRSN A2285 (A); MZUT An (paralectotypes of Racophorus liber) (ADK) Mantella baroni MRSN A (F) Mantella betsileo MRSN-RJS (ADR) Mantella cowani MRSN A3204 (V), A (V), A3205 (F), A3203 (F); MRSN A3200 (A), MRSN A3202 (VT), MRSN A (A), A3201 (VT) Hybrids Mantella baroni Mantella cowani MRSN A (F); A3210 (F) Mantidactylus alutus MRSN A2932 (S), A2925 (S), A3023 (S), A2276 (A); MZUT An725 and (ADK) (lectotype and paralectotypes of Rana aluta); UADBA 21180, (S); ZMA (S); Mantidactylus brevipalmatus MRSN A2932 (S), A2951 (S), A2636 (S), A2239 (S), A2482 (A); UADBA 21181, 21183, (S); ZMA 19547*, 19549* (S), MRSN-RJS (ADR); ZSM 752/2001 (IT)
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