A comprehensive survey of amphibians and reptiles in the extreme north of Madagascar

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1 Herpetology Notes, volume 2: (2009) (published online on 07 April 2009) A comprehensive survey of amphibians and reptiles in the extreme north of Madagascar Steven Megson 1, Polly Mitchell 1, Jörn Köhler 2, Charles Marsh 3, Michael Franzen 4, Frank Glaw 4, Neil D Cruze* 5 Abstract. We surveyed the western dry forest and coastal forest of the Ampombofofo area in the extreme north of Madagascar for its herpetofauna. We recorded a total of nine amphibian and 46 reptile species via opportunistic searching and pitfall trapping. This is the first such survey and consequently providing new records for the area for all of the species found. For those species endemic to Madagascar, these records also represent the northernmost limit of their known range. We also surveyed the coastal forest of Orangea and recorded a total of three amphibian and 22 reptile species. Furthermore, we provide new additions to the species list for Montagne des Français. We discovered several species in this massif during our relatively short surveys that were not previously known from this site: Reptiles include Gehyra mutilata, Leioheterodon modestus, and Paracontias hildebrandti. Amphibians include an unidentified speces of Cophylinae and two additional species of Stumpffia. The results of this and other surveys in surrounding areas have now demonstrated that many of the species previously considered to be endemic to Montagne des Français are in fact regionally endemic to the north of Madagascar. However, the forested areas located in the extreme north are subject to numerous human induced environmental problems resulting in habitat destruction and remain a high conservation management priority. Therefore we strongly recommend that Montagne des Français should be granted full-protected status so that it is able to function as a biological refuge. Herein, we provide additional conservation and development recommendations for the other terrestrial ecosystems surveyed. Keywords. Amphibia, Antsiranana region, Ampombofofo, conservation, Orangea, Madagascar, Montagne des Français, Reptilia. Introduction The amphibians and reptiles of Madagascar are extremely diverse and display a high level of endemism (Glaw and Vences, 2007). Although the amount of information regarding Malagasy herpetofauna has increased dramatically over the past decade further detailed surveys focused on Malagasy amphibians and reptiles are still required (D Cruze et al., in press). The majority of herpetological survey work in Madagascar has focused on long established protected areas (D Cruze et al., in press). Current information regarding non-protected areas and secondary habitats is extremely 1 Frontier, The Society for Environmental Exploration, Rivington Street, London, EC2A3QP, UK; stevie_meg@hotmail.com 2 Hessisches Landesmuseum Darmstadt, Department of Natural History Zoology, Friedensplatz 1, Darmstadt, Germany; joern.koehler@hlmd.de 3 Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire, SL5 7PY, United Kingdom; charles.marsh07@imperial.ac.uk 4 Zoologische Staatssammlung München, Münchhausenstr. 21, München, Germany; MF: Michael.Franzen@zsm.mwn.de; FG: Frank.Glaw@zsm.mwn.de 5 The World Society for the Protection of Animals, 89 Albert Embankment, London, WE1 7TP, United Kingdom; cruzecontrol@gmail.com * corresponding author Figure 1. Map of study area in northern Madagascar.

2 32 Steven Megson et al. Table 1. Conservation status and distribution of the amphibian and reptile species found during surveys of Ampombofofo in northern Madagascar Species Amphibia Ranidae sensu lato Relative abundance Ecological distribution Altitude (m a.s.l.) Habitat type Hoplobatrachus tigerinus C S F/A x x x x II Ptychadena mascareniensis A T/S F/A x x x x Mantellidae Dry 1 Dry 2 Wet 1 Wet 2 CITES listing Regionally endemic Aglyptodactylus securifer* SC T F x x + Blommersia cf. wittei* R S F x Boophis tephraeomystax C AB/T/S F/A x x x x Laliostoma labrosum SC T/S F x x Mantella viridis*** C T/S F x x x x II + Microhylidae Stumpffia sp. 1 I T/S F x x + Stumpffia sp. 2 R T/S F x + Reptilia Chamaeleonidae Brookesia stumpffi SA AB/T F x x x II Furcifer oustaleti A AB/T F/A x x x x II Furcifer pardalis A AB/T F/A x x x x II Furcifer petteri SA AB/T F/A x x x II Gekkonidae Blaesodactylus boivini A AB F/A x x x x + Ebenavia inunguis I AB/T A x x Geckolepis cf. maculata A AB F/A x x x x Geckolepis sp. I AB F x x x x + Hemidactylus frenatus I AB A x x x Hemidactylus mercatorius R AB A x x Lygodactylus heterurus trilineigularis R AB/T F/A x + Paroedura cf. karstophila R T F x x + Paroedura stumpffi C AB/T F/A x x x x + Phelsuma abbotti A AB F/A x x x x II Phelsuma grandis A AB F/A x x x x II + Uroplatus ebenaui I AB F x x x x II Uroplatus sp. nov. aff. henkeli C AB F x x x x II + Gerrhosauridae Zonosaurus boettgeri I AB/T F x x + Scincidae Amphiglossus ardouini R T F x + Cryptoblepharus boutonii cognatus C T 0-10 x x x x Cryptoscincus minimus R T F/A x x Madascincus cf. intermedius 1 A T F/A x x x x Madascincus cf. intermedius 2 A T F/A x x x x + Trachylepis elegans A T F/A x x x x Trachylepis tavaratra C T F/A x x x + scarce (Andreone et al., 2003; Kremen et al., 2008; D Cruze et al., in press) and must be targeted in order to ensure that informative conservation decisions are made. This paper is part of a series of research articles (D Cruze and Sabel, 2005; D Cruze et al., 2006; D Cruze et al., 2007, 2008) that contributes to the existing knowledge by highlighting the findings of an extensive biodiversity survey conducted in the north of Madagascar. This and other fieldwork conducted in recent years has revealed the extraordinary importance of the extreme north as a biological center of herpetological diversity and endemism, which has included the discovery of a multitude of undescribed herpetological taxa (e.g. Pintak and Böhme, 1988; Raselimanana et al., 2000; Glaw et al., 2001; 2005; 2006a, b, Raxworthy and Nussbaum 2006; Köhler et al., 2008) and resulted in significant geographic range extensions (e.g. Raxworthy and Nussbaum, 1994; Rakotondravony, 2006; D Cruze et al., 2006, 2007). The herpetofauna in the extreme north of Madagascar is currently conserved by a network of protected areas consisting of Montagne D Ambre National Park, Forêt d Ambre Special Reserve, Analamera Special Reserve, Ankarana Special Reserve and Montagne des Français (recently awarded temporary protected status). Of these five biological refuges, three have been recently subjected to intensive survey work (Raxworthy and

3 Amphibians and reptiles of northern Madagascar 33 Table 1. continued Species Boidae Relative abundance Ecological distribution Altitude (m a.s.l.) Habitat type Dry 1 Dry 2 Wet 1 Wet 2 CITES listing Regionally endemic Acrantophis madagascariensis** I T F/A x x x x I Sanzinia madagascariensis volontany** I AB/T F/A x x x x I Colubridae sensu lato Dromicodryas quadrilineatus C T F/A x x x Heteroliodon fohy I T F x x x + Ithycyphus miniatus C AB/T F/A x x x x Langaha madagascariensis I AB/T F x x Leioheterodon madagascariensis A T F/A x x x x Leioheterodon modestus C T F/A x x x x Liophidium therezieni I T F x x x x + Liophidium torquatum C T F/A x x x x Madagascarophis colubrinus C AB/T F/A x x x Mimophis mahfalensis A AB/T F/A x x x x Pseudoxyrhopus quinquelineatus I T F x x x Stenophis granuliceps C AB/T F/A x x x + Stenophis inopinae I AB/T F x x x + Stenophis variabilis R AB/T F x Typhlopidae Ramphotyphlops braminus I T F x Typhlops cf. microcephalus I T F x x x x Typhlops sp 2 R T F x + Xenotyphlops grandidieri R T F x + Pelomedusidae Pelusios castanoides R S F x Relative Abundance: A = abundant, C = common, I = infrequent, R = rare. SA = seasonally abundant, SC = seasonally common. Ecological Distribution: AB = arboreal, T = terrestrial, S = semiaquatic. Habitat: F =, A = anthropogenically disturbed. Seasonal Data: Wet = Wet season, Dry = Dry season, x = present. *Listed as Least Concern in the 2008 IUCN Red List of Threatened Species **Listed as vulnerable. ***Listed as Endangered. + = Regionally endemic Figure 2. Photographic documentation of some of the habitat types surveyed during this study. A= Ampombofofo; B= Orangea; C= Montagne des Français; and D= Pitfall trap in Orangea.

4 34 Steven Megson et al. Table 2. Location and description of pitfall lines used to capture amphibians and reptiles at Ampombofofo (capture rate % is number of amphibians and reptiles caught per trap day). Season Line Habitat Microhabitat Latitude (S) Longitude (W) Altitude (m) Start date Finish date Days Trap days Capture rate % Dry 1 1 Primary /10/ /10/ Dry 1 2 Primary /10/ /10/ Dry 1 3 Primary /10/ /10/ Dry 1 4 Steep hillside /11/ /11/ Dry 1 5 Steep hillside /11/ /11/ Dry 1 6 Steep hillside /11/ /11/ Dry 1 7 Disturbed Open scrub /11/ /11/ Dry 1 8 Disturbed Open scrub /11/ /11/ Dry 1 9 Secondary /11/ /11/ Dry 1 10 Secondary /11/ /11/ Dry 1 11 Secondary /11/ /11/ Wet 1 12 Primary /01/ /02/ Wet 1 13 Primary /01/ /02/ Wet 1 14 Primary /01/ /02/ Wet 1 15 Secondary /02/ /02/ Wet 1 16 Secondary /02/ /02/ Wet 1 17 Secondary /02/ /02/ Wet 1 18 Disturbed Acacia ridge /02/ /02/ Wet 1 19 Disturbed Acacia ridge /02/ /02/ Wet 1 20 Disturbed Acacia ridge /02/ /02/ Wet 1 21 Disturbed Acacia ridge /04/ /04/ Wet 1 22 Disturbed Acacia ridge /04/ /04/ Wet 1 23 Disturbed Acacia ridge /04/ /04/ Wet 2 24 Secondary /05/ /05/ Wet 2 25 Secondary /05/ /05/ Wet 2 26 Secondary /05/ /05/ Wet 2 27 Secondary /04/ /05/ Wet 2 28 Secondary /04/ /05/ Wet 2 29 Secondary /04/ /05/ Wet 2 30 Primary /05/ /05/ Wet 2 31 Primary /05/ /05/ Wet 2 32 Primary /05/ /05/ Wet 2 33 Secondary /05/ /05/ Wet 2 34 Disturbed Open scrub /05/ /05/ Wet 2 35 Disturbed Open scrub /05/ /05/ Dry 2 36 Secondary /08/ /08/ Dry 2 37 Secondary /08/ /08/ Dry 2 38 Secondary /08/ /08/ Dry 2 39 Disturbed Acacia ridge /08/ /08/ Dry 2 40 Disturbed Acacia ridge /08/ /08/ Dry 2 41 Disturbed Acacia ridge /08/ /08/ Dry 2 42 Disturbed Acacia ridge /10/ /10/ Dry 2 43 Disturbed Acacia ridge /10/ /10/ Dry 2 44 Disturbed Acacia ridge /10/ /10/ Dry 2 45 Secondary /11/ /12/ Nussbaum, 1994; D Cruze et al., 2007, 2008). Only the forest found within the Analamera Special Reserve and Ankarana Special Reserve have not been subject to indepth biodiversity surveys that have resulted in detailed published species lists (but see Hawkins et. al., 1990). The intention of this study was to survey a previously undocumented area of low altitude with large patches of relatively undisturbed western dry forest located outside of the protected areas in the extreme north of Madagascar. Firstly, this survey would serve to identify any species that do not currently receive protection within these biological refuges and provide researchers with the opportunity to assess the current conservation threats that they might face. Secondly, it was hoped that the information gathered would contribute to the existing literature regarding Malagasy patterns of biodiversity by documenting the composition, geographical and ecological distribution of any species encountered. Crucially this information can then be used in the assessment of future conservation priorities. Study Sites The majority of our study was conducted by a team of researchers and volunteers in Ampombofofo in the Bobaomby region (Fig. 1), approximately 20 km north of the town of Antsiranana (Diego Suarez), the administrative capital of the Antsiranana province. The

5 Amphibians and reptiles of Northern Madagascar 35 Table 3. Amphibians and reptiles caught in the pitfall traps at Ampombofofo Pifall line number Aglyptodactylus securifer Laliostoma labrosum Stumpffia sp. 1 Mantella viridis Total Amphibia Amphiglossus ardouini Madascincus cf. intermedius1/2* Brookesia stumpffi Furcifer petteri Blaesodactylus boivini Geckolepis cf. maculata Lygodactylus heterurus Paroedura stumpffi Trachylepis elegans Trachylepis tavaratra Typhlops microcephalus Typhlops sp. 2 Ramphotyphlops braminus Liophidium torquatum Liophidium therezieni Mimophis mahfalensis Pseudoxyrhopus quinquelineatus Total Reptilia Total specimens Total

6 36 Table 4. Amphibian and reptile species found during surveys of Orangea in northern Madagascar 2007/2008 and their threat and conservation status. Species IUCN Status CITES listing Regio Amphibia Ranidae sensu lato Hoplobatrachus tigerinus LC II Ptychadena mascareniensis Hyperoliidae Heterixalus andrakata Reptilia Chamaeleonidae Furcifer oustaleti Furcifer pardalis Furcifer petteri Gekkonidae Geckolepis sp. Hemidactylus mercatorius Paroedura stumpffi Phelsuma abbotti Uroplatus sp. nov. aff. henkeli Scincidae Cryptoblepharus boutonii cognatus Cryptoscincus minimus Madascincus cf. intermedius 1 Madascincus cf. intermedius 2 Paracontias rothschildi Paracontias sp. nov. Trachylepis elegans Colubridae sensu lato Dromicodryas quadrilineatus Leioheterodon madagascariensis Leioheterodon modestus Liophidium therezieni Liophidium torquatum Mimophis mahfalensis Typhlopidae Xenotyphlops grandidieri close proximity to the coast and the sandstone geology has created a unique habitat matrix of large patches of primary western dry forest fringed by primary coastal forest. In addition, anthropogenically disturbed areas of habitat are also present throughout this region (Fig. 2 provides photographic documentation of the main habitat types surveyed during this study). Our study mainly concentrated on an area of forest surrounding the village of Ampombofofo with researchers operating from a base camp situated at S, E. Fieldwork in this region consisted of five survey periods, LC LC II II II II II Steven Megson et al. which were conducted during both wet and dry seasons over a period of approximately 15 months. Each survey period lasted approximately 9 weeks in length and can be summarised as follows: Survey 1: 9 October to 14 December 2006; Survey 2: 4 January to 8 March 2007; Survey 3: 3 April to 13 June 2007; Survey 4: 4 July to 15 September 2007; and Survey 5: 8 October to 13 December Fieldwork was conducted throughout the full altitudinal range (0-100 m a.s.l.) within all habitat types. A second team conducted fieldwork in the Andavakoera region of Montagne des Français (Fig. 1) ( S, E, 140 m a.s.l.), in January and February 2006 and again between 16 to 25 February The area has already been subject to a detailed survey effort (D Cruze et al., 2007). The vegetation within the calcareous massif of Montagne des Français has been described as transitional midaltitude rainforest and dry deciduous western forest (Ramanamanjato et al., 1999) (Fig. 2). A third team conducted fieldwork in an area of coastal scrub forest located within the area known as Orangea (Figures 1 and 2) ( S, E, ca. 25 m a.s.l.), in 22 February to 5 March 2007 and 19 to 28 February All of the study sites are part of the Western Ecoregion defined by Cornet (1974), and the N Bemarivo centre of endemism identified by Wilmé et al. (2006). The region is characterized by a reliable wet season that runs from November to March during which the majority of rainfall occurs. This period is followed by a pronounced dry season that can last up to seven months during which rainfall is highly infrequent. However the mean annual precipitation of Montagne des Français is believed to be slightly higher than the 980 mm received by Antsiranana (Nicoll and Langrand, 1989). Materials and Methods Due to the lack of field information regarding the herpetofauna of this location we used a wide range of sampling methods in order to collect data for as many species as possible. We also made a concerted effort to identify anthropogenic activities that represent threats to the conservation of this area. We used three 100 m pitfall trap-lines with drift fences as described in Raxworthy and Nussbaum (1994), which were left in place for a total of seven - 11 days. We conducted opportunistic searches (D Cruze et al., 2007) across the full range of altitudes and habitats night and day searching in order to reveal the presence of species not captured by the other methods. We also made direct counts along line transects to identify species and assess their distribution and abundance. We specifically targeted calling anurans after rainfall. A total of 45 trap lines were constructed at Ampombofofo during the survey period, the details of which are shown in table 2. A total of four trap lines were constructed in Orangea and six

7 Amphibians and reptiles of Northern Madagascar 37 in Montagne des Français (Tab. 5). We classified the species encountered during this survey using a system similar to that used by D Cruze and Sabel (2005) that can be summarised as follows; Abundant (species encountered in large numbers regularly all year round), common (encountered on a regular basis all year round), infrequent (unpredictable and few individuals encountered), rare (rarely encountered), seasonally abundant (encountered in large numbers on a regular basis during a certain time of year but otherwise infrequent or rarely seen), or seasonally common (encountered on a regular basis during certain times of year but otherwise infrequent). These classifications are based on data collected using all survey techniques and refer to the total number of individuals encountered for each species. Finally, we also estimated the altitudinal range for all of the species currently recorded from the survey sites. We used the minimum and maximum elevations [combined data of our surveys and that of Raxworthy and Nussbaum (1994)] to calculate the elevational range of each species. This method makes the assumption that each species is distributed continuously through the minimum and maximum elevation recorded. The following information was recorded for each collected specimen: date, latitude, longitude, habitat, microhabitat and altitude. We also made colour notes and took photographs. We took voucher specimens (preserved in 70% ethanol) and tissue samples for all voucher specimens. Reptile and amphibian specimens were deposited at the Université d Antananarivo, Département de Biologie Animale (UADBA) and Zoologische Staatssammlung München (ZSM). A list of specimens can be found in Appendix I. Results Ampombofofo A complete species list is given in table 1 along with the current CITES listing (CITES Species Database, Geneva, Switzerland) and IUCN status (IUCN Red List of Threatened Species 2008, Species Survival Commission, Gland, Switzerland) for each of the relevant species. Table 1 also includes ecological data for each species including habitat type (classified as either forest or anthropogenically disturbed habitat), ecological distribution and relative abundance. During this survey, we recorded a total of nine amphibian and 46 reptile species in Ampombofofo region, giving a total herpetofaunal diversity of 55 species. It can now be assumed that the herpetofauna of the Ampombofofo region consists of at least one chelonian, 25 lizards, 20 snakes and nine species of anurans. We classify a total of 12 species (22%) as abundant, 13 species (24%) as common, 15 species (27%) as infrequent, 11 species (20%) as rare, two species (4%) as seasonably abundant and two species (4%) as seasonally common. Of the 55 species encountered we found 26 (47%) to be present during wet and dry season sample periods, two species (4%) only in the dry season and eight species (15%) only during the wet season. A total of 242 amphibians and reptiles were caught in pitfall traps, the details of which can be seen in table 3. These individuals were captured over 5349 trap days, giving an overall capture rate of 4.5% per trap day. The pitfall traps caught four amphibian, 11 lizard and seven snake species. Two fossorial species (Typhlops cf. microcephalus and Typhlops sp. 1) were only caught using pitfall traps. At least one amphibian and one reptile species represent what appear to be undescribed species: Stumpffia sp. 1, and Typhlops sp. 1. Of the 55 species encountered during this survey, one species, Cryptoblepharus boutonii cognatus, was not found throughout the entire altitudinal range of the Ampombofofo region. With regards to primary habitat in the Ampombofofo region three species (6%) were found only in anthropogenically disturbed non-forest habitat, 24 species (44%) were found solely within relatively undisturbed forest habitat. 27 (49%) occurred in both undisturbed and disturbed habitat. One species (2%), Cryptoblepharus boutonii cognatus, was only observed on rocks along the coast. 21 (38%) species were found solely in terrestrial situations, nine (16%) only in arboreal situations and 16 (29%) in both. Five species (9%) were found to be occurring in both terrestrial and semi aquatic habitat, three (6%) species solely in semi aquatic environment and one species (2%) occurred in all three habitats, terrestrial, semi aquatic and arboreal situations. The majority of the species found in the Ampombofofo region are endemic to Madagascar (89%). Ptychadena mascareniensis and Leioheterodon madagascariensis are found on other Indian Ocean Islands. Pelusios castanoides occurs on the African mainland, Hoplobatrachus tigerinus is native to India, Cryptoblepharus boutonii occurs on many Indian Ocean Islands, the Australian region and African mainland, Hemidactylus frenatus has a wide global distribution and Hemidactylus mercatorius occurs on the African mainland and other Indian Ocean islands. We recorded 21 species (38%) that are regional endemics restricted to only a few places in north Madagascar (Table 1). One species is listed as endangered, two species are listed as vulnerable but need updating and seven species are listed as least concern on the 2007 IUCN Red List of Threatened Species. A total of 12 species (22%) are listed on the CITES appendices.

8 38 Steven Megson et al. Table 5. Location and description of pitfall lines used to capture amphibians and reptiles at Orangea (O1-O4) and Montagne des Français (MDF1- MDF6) (capture rate % is number of amphibians and reptiles caught per trap day). Site, Season Habitat Microhabitat Latitude Longitude Altitude Start Finish Days Trap Capture Line (m a.s.l.) date date days rate % O1 Wet 1 Coastal scrub 12 14' ' /02/ /03/ forest O2 Wet 3 Coastal scrub /02/ /02/ forest O3 Wet 3 Coastal scrub /02/ /02/ forest O4 Wet 3 Coastal scrub forest /02/ /02/ MDF1 Wet 3 Valley /02/ /02/ MDF2 Wet 3 Slight hillside /02/ /02/ MDF3 Wet 3 Slight hillside /02/ /02/ MDF4 Wet 3 Disturbed Canyon ' ' /02/ /02/ MDF5 Wet 3 Disturbed Canyon ' ' /02/ /02/ MDF6 Wet 3 Disturbed Canyon ' ' /02/ /02/ Orangea A total of 34 reptile specimens were captured in the pitfall traps over a total of 381 trap days, giving an overall capture rate of 8.9%. The pitfalls captured five lizard and two snake species. During the survey a total of three amphibian and 22 reptile species were recorded in Orangea providing a total of 25 species. It can now be assumed that the herpetofauna of Orangea consists of at least three anurans, 15 lizards and seven snake species (Table 4). Twentytwo (88%) of the species encountered are endemic to Madagascar and six species (24%) are regionally endemic. Three species (12%) appear as Least Concern on the IUCN red list of endangered species and six (24%) appear in the CITES Appendices (Table 4). Montagne des Français A total of 23 amphibians and reptiles were captured in the pitfall traps. The 23 individuals were captured over 660 trap days resulting in a capture rate of 4%. The pitfalls set up in forest habitat yielded an average capture rate of 6%, where as the pitfalls placed in more anthropogenically disturbed areas only yielded an average capture rate of 1%. At Montagne des Français a total of eight amphibian and 29 reptile species were recorded during the survey period. The majority of species found (95%) are endemic to Madagascar, with Leioheterodon madagascariensis occurring on other Indian Ocean Islands and Gehyra mutilata occurring widely across Southeast Asia. Of the species recorded, 19 (51%) are regionally endemic. Six (16%) of the species recorded were previously unknown for the Massif: Cophylinae gen. sp., Gehyra mutilata, Leioheterodon modestus, Paracontias hildebrandti, Stumpffia sp. 3 and Stumpffia sp. 4. Three of which (8%) are locally endemic; Cophylinae gen. sp., Stumpffia sp. 3 and Stumpffia sp. 4. These new records bring the total number of herpetofaunal species in the area to 67. Two species (5%) appear as least concern on the IUCN red list of endangered species: Aglyptodactylus securifer, Mantidactylus bellyi and one species (3%) appears as Endangered: Mantella viridis. Seven species (19%) appear in the CITES appendices; Mantella viridis, Brookesia ebenaui, Brookesia sp. nov., Brookesia stumpffi, Furcifer oustaleti, Furcifer pardalis, Furcifer petteri and Uroplatus sp. nov. aff. henkeli. Discussion Pitfall Trapping The pitfall traps set up in forest habitat of Montagne des Français yielded a higher average capture rate then those deployed in the more anthropogenically disturbed areas. It is difficult to determine the specific causal factors responsible for this from the results of our particular study. However, it seems that our data supports the contention that anthropogenic habitat alteration (loss, degradation or fragmentation) can have a strong negative influence on tropical herpetofaunal communities (Vallan, 2003). We recommend that more research should be conducted out to investigate this further. Unfortunately we can not directly compare pitfall trapping between the various study sites because this survey method was not kept constant e.g. pitfall trapping differed greatly in terms of duration and seasonal implementation.

9 Amphibians and reptiles of Northern Madagascar 39 Range extensions: Ampombofofo All of the species discovered in this survey are new records for Ampombofofo. It is important to note that for all of these species this locality data represent the northernmost limit of their known range. Many species encountered during this study require special mention as their occurrence in Ampombofofo significantly contributes to the current information regarding their distribution in Madagascar. Until recently, Mantella viridis was considered as critically endangered (now changed to endangered by Andreone et al., 2008a) and was thought to be restricted to only a few localities in the extreme north of Madagascar (D Cruze et al., 2007; Glaw and Vences, 2007). However a recent study conducted by Mercurio and Andreone (2008) revealed the presence of this species in a total of 42 different localities. Our study revealed that M. viridis was locally abundant in the Ampombofofo region, which supports the suggestion that the status of this species needs to be re-evaluated (Mecurio and Andreone, 2008). The presence of Liophidium therezieni at this locality is noteworthy because (although its conservation status has yet to be assessed) prior to this survey this terrestrial snake was only known from two locations; Montagne des Français and Anatelo (Franzen et al., in press). Its presence in the Ampombofofo region and at Orangea represents only the third and fourth localities for this species. Our findings indicate that it is a relatively adaptable species that is not restricted to limestone habitat. The specimen ZSM 1612/2008 was found at 11:00 approximately cm under the ground when digging holes for the construction of basecamp. The individual was unearthed in an area of secondary western dry forest ( S, E). During the survey in Ampombofofo six other individuals were recorded. Individuals were encountered throughout a variety of different habitat types. L. therezieni was observed both on the steep slopes of the primary western dry forest at the Pteropus rufus roost and in the primary western dry forest surrounding Ampombofofo, and it was also recorded in riparian habitat. At night individuals were observed active amongst leaf litter in mango plantations edging the river. During the survey individuals were also recorded in more degraded habitat, as well as in the coastal scrub forest amongst thin leaf litter coverage on sandy soil, also in open scrubland that had once been rice padis or had been cleared for zebu grazing. Although additional specimens were not taken, morphological data for these snakes was recorded. This study also provides an important additional locality for Amphiglossus ardouini. The genus Amphiglossus has a wide distribution and inhabits most of Madagascar s environments. However, most species dwell in the leaf litter and are often very secretive (Glaw and Vences, 2007). As a result both the habits and distribution of A. ardouini are largely unknown. One specimen was discovered on 11 November 2006 in an area of secondary western dry forest ( S, E) as it was being consumed by a Dromicodryas quadrilineatus. Another individual was captured in a pitfall trap on 23 February The specimen was discovered early in the morning indicating nocturnal or crepuscular activity. The trap site was situated in an Acacia forest on sandy soil ( S, E). Prior to this survey this species was known from three localities only: Antsiranana, Ambilobe and Montagne des Français (Glaw and Vences, 2007). New records: Montagne des Français The herpetofauna of Montagne des Français [an area of herpetological importance that has been nominated as a Durban Vision Potential Site requiring some form of protection (Ministère de l Environment, des Eaux et Forets, 2005) and granted Temporary Protected Status] has been recently surveyed intensively by a team of researchers and volunteers (D Cruze et al., 2007). It is therefore remarkable that we discovered several species in this limestone massif during our relatively short surveys that were not previously known from this site: Reptiles include Gehyra mutilata, Leioheterodon modestus, and Paracontias hildebrandti. Amphibians include Cophylinae gen. sp., Stumpffia sp. 3 and Stumpffia sp. 4. These findings indicate that even intensive surveys, conducted by numerous researchers using different methods may often fail to obtain a complete herpetofaunal species inventory. To address this problem researchers have suggested: (1); the implementation of additional biodiversity and monitoring surveys; (2) increased collaboration with Malagasy researchers and self-funded volunteers; (3) application of molecular barcoding approaches to identify true species richness; and (4) the utilisation of approaches that speed up data availability via appropriate cyber infrastructure (D Cruze et al., in press; Vences et al., 2008). Relevance to patterns of biodiversity in northern Madagascar Natural biogeographical processes are believed to be largely responsible for the current distribution of

10 40 amphibians and reptiles in Madagascar (Wilmé et al., 2006). However the disruptive anthropogenic activity that followed human invasion approximately 2000 years ago is also believed to have played a pivotal role in shaping patterns of distribution (Vallan, 2003). For example it has been suggested that prior to human invasion continuous lowland corridors of dry or transitional forest linked the lower slopes of the five major massifs of Analamera, Ankarana, Daraina, Montagne D Ambre and Montagne des Français located in the north (Ramanamajato et al., 1999; D Cruze et al., 2006, in press). We suggest that prior to human invasion the forests of the Bobaomby region and Montagne des Français may have been linked via the Bobaomby spine region (the area around Windsor Castle) (Figure 1). It is also possible that this connected area of forest may have also stretched to include Orangea. These former corridors would help to explain how these species were able to cross the distance between these sites. It is clear that to better understand the biogeographical patterns of the herpetofauna in the north of Madagascar more data regarding their exact distribution and phylogenetic relationships must be gathered (Vences et al., 2004; Boumans et al., 2007). Following an extensive herpetological survey (D Cruze et al., 2007), Montagne des Français was until recently considered as an important biological center of herpetological endemism. At least eight species were considered to be locally endemic to this calcareous massif (D Cruze et al., 2007; Glaw and Vences, 2007). However, our results of surveys in surrounding areas have now demonstrated that many of these species are also present outside of this massif and are in fact regionally endemic to the north of Madagascar. Examples are Thamnosophis martae which has been recorded within the Forêt d Ambre Special Reserve (D Cruze et al., 2008) and Heteroliodon fohy and Liophidium therezieni that have been recorded from within the Ampombofofo Region (Megson et al., in press; Franzen et al., in press). This highlights both the importance and the necessity for increased herpetological survey effort in Madagascar as this type of baseline information is needed to facilitate informed decisions for existing conservation programs and guide the course of future management strategies (Andreone et al., 2008b; Kremen et al., 2008). Conservation Implications Socio-economic factors such as rapid population growth, poor education and other particular aspects of Malagasy culture are partly responsible for obliging local residents to employ harmful agricultural methods and other activities that lead to the exploitation of natural resources (Durbin et al., 2003) which can be a serious threat to amphibians and reptiles (Glaw and Vences, 2007). As a result of its close proximity to the administrative capital of the Antsiranana province (ca. 30 km) and neighbouring communes such as the villages of Ampombofofo and Ramena, the unique herpetofauna found in our study sites located in the extreme north Madagascar are vulnerable to these anthropogenic pressures. The major threats to the integrity of the herpetofauna of these areas are: (1) agricultural clearance for maize and rice cultivation; (2) charcoal production; (3) timber production; and (4) zebu grazing (during which sites are either selectively logged or cleared of all trees) (D Cruze et al., 2007). All of these threats have resulted in the degradation or clearance of large areas of forest in all three of our study sites. Continued forest clearance will lead to the eventual fragmentation of the remaining areas of forest (with serious consequences for the herpetofauna; e.g. Vallan, 2000; Vallan, 2003). This will be followed by local extirpation, and possibly extinctions, that will in turn place increased pressure on the existing system of protected areas in the north of Madagascar. Due to its remote location Ampombofofo remains far less affected by the rapid population growth compared to Montagne des Français or Orangea. The main pressure on the forest is anthropogenic but may be linked to climate change. After meetings with members of the local village it was explained that they had noticed a significant drop in rainfall and in the height of the river water within the last 15 years particularly. It is believed in the village that the reduction in rainfall is punishment from the Ancestors for the younger members of the village disobeying the local taboos (Fadis). It was explained that this lack of available water meant that once successful padi fields were simply too dry to yield an adequate crop. This lack of appropriate rice padis has forced the village to find alternate ways to generate income, e.g. charcoal production and the clearing of land to encourage breeding of Zebu, which are sold in Antsiranana to purchase rice. It was also explained that since charcoal production and the clearing of land for zebu grazing has become more frequent, soil is disappearing. Future action Steven Megson et al. The reptile and amphibian rich fauna found in the north of Madagascar is already recognized as a highly speciose region of the biodiversity hotspot that is Madagascar (D Cruze et al., 2008). To safeguard this diversity we

11 Amphibians and reptiles of Northern Madagascar 41 suggest that a detailed conservation management plan should be developed for the extreme north of Madagascar. As part of this plan we strongly recommend that Montagne des Français should be granted full-protected status so that it is able to function as a biological refuge for the threatened species that increasingly seem to be endemic to the extreme north of the island. In addition increased conservation management action is required to protect the biological diversity found within the existing protected areas found in the north of the country (D Cruze et al., 2008). Furthermore habitat restoration activity should be encouraged to improve connectivity with Orangea and the Bobaomby Region so as to address habitat fragmentation. In order to implement this in a sustainable and holistic manner we make the following additional conservation recommendations: Further assessment and monitoring of natural resource use activities. In particular, clearance of forest needs to be restricted and the remaining areas must be carefully monitored (e.g. by remote sensing using satellite data). \ Development and implementation of a largescale, regionally connected, more sustainable community-focused management system, which includes payments for ecosystem services, including biodiversity conservation and carbon sequestration. Development efforts, to promote sustainable agriculture practices and to improve human conditions. Village-based education programmes aimed at demonstrating alternative energy systems and crops, which are compatible with local traditions. Raising awareness about environmental problems. Village-based programmes targeting all socioeconomic groups. Acknowledgements. We would like to thank Sally Eaton, Amanda Martin, Edmond Randriamalala, Robert Devas, Adam Mushi, Stuart Brooker, The Village of Ampombofofo and all of the Frontier staff and volunteers in Furthermore, Parfait Bora, Hildegard Enting, Angelika Knoll, and Zoltan Nagy assisted during fieldwork in 2007 and The work was carried out in collaboration with the Département de Biologie Animale, Université d Antananarivo, and the Association Nationale pour la Gestion des Aires Protégées (ANGAP). We are grateful to the Malagasy authorities, in particular the Ministère de l Environnement et des Eaux et Forêts, for research and export permits. 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13 Amphibians and reptiles of Northern Madagascar 43 Appendix 1. Voucher specimens from Ampombofofo, Orangea and Montagne des Français. Ampombofofo Amphibia Mantellidae Aglyptodactylus securifer ZSM 1637/2008 ZSM 1636/2008, Blommersia cf. wittei UADBA 1937/2008, Boophis tephraeomystax ZSM 1645/2008, Laliostma labrosum UADBA 1955/2008, Mantella viridis FGZC Microhylidae Stumpffia sp.1 ZSM 1661/2008 ZSM 1663/2008, Stumpffia sp. 2 UADBA 1959 Reptilia Chamaeleonidae Brookesia stumpffi ZSM 1507/2008. Gekkonidae Blaesodactylus boivini ZSM 1519/2008, Ebenavia inunguis ZSM 1535/2008, Geckolepis cf. maculata ZSM 1521/2008, Hemidactylus frenatus UADBA 1929/2008, Lygodactylus heterurus ZSM 1543/2008 ZSM 1544/2008 ZSM 1545/2008, Paroedura cf. karstophila ZSM 1531/2008, Paroedura stumpffi UADBA 1936/2008, Uroplatus sp. nov. aff. henkeli ZSM 1924/2008. Scincidae Amphiglossus ardouini ZSM 1555/2008, Cryptoscincus minimus ZSM 1583/2008, Madascincus cf. intermedius 1 ZSM 1564/2008, Madascincus cf. intermedius 2 ZSM 1570/2008, Trachylepis cf. tavaratra ZSM 1552/2008 ZSM 1553/2008. Colubridae sensu lato Heteroliodon fohy ZSM 1624/2008, Langaha madagascariensis ZSM 1722/2008, Liophidium therezieni ZSM 1612/2008, Liophidium torquatum ZSM 1616/2008, Pseudoxyrhopus cf. quinquelineatus ZSM 1609/2008, Stenophis granuliceps ZSM 1604/2008, Stenophis inopinae UADBA 1720/2008, Stenophis variabilis ZSM 1606/2008 ZSM 1607/2008. Typhlopidae Typhlops microcephalus ZSM 1588/2008, Typhlops sp. 2 ZSM 1592/2008. Montagne des Français Amphibia Mantellidae Mantella viridis FGZC 1761 Microhylidae Stumpffia sp.2 ZSM 1671/2008, Stumpffia sp.3 ZSM 1672/2008, Stumpffia sp.4 ZSM 1667/2008, Cophylinae gen. sp. ZSM 1674/2008 Ranidae sensu lato Ptychadena mascareniensis ZSM 2066/2007 Reptilia Chamaeleonidae Brookesia ebenaui ZSM 2110/2007, Brookesia sp. nov. ZSM 1505/2008 ZSM 2146/2007 ZSM 2147/2007 ZSM 2148/2007 ZSM 2149/2007 Gekkonidae Geckolepis sp. ZSM 1523/2008 ZSM 2112/2007 Gehyra mutilata ZSM 1536/2008, Lygodactylus heterurus ZSM 1546/2008 Lygodactylus sp. ZSM 1547/2008, Paroedura cf. karstophila ZSM 2106/2007 ZSM 2107/2007, Paroedura stumpffi ZSM 1525/2008, Uroplatus sp. nov. aff. henkeli ZSM 2111/2007. Scincidae Amphiglossus ardouini ZSM 1554/2008, Amphiglossus sp. nov. 1 ZSM 1556/2008, Madascincus cf. intermedius 2 ZSM 1573/2008 ZSM 1574/2008, Madascincus cf. polleni ZSM 1559/2008 ZSM 1560/2008 ZSM 1561/2008, Paracontias hildebrandti ZSM 1578/2008, Colubridae sensu lato Alluaudina bellyi ZSM 1627/2008, Ithycyphus miniatus ZSM 1625/2008, Langaha madagascariensis ZSM 1621/2008 ZSM 2133/2007, Liophidium therezieni ZSM 2053/2007, Liophidium torquatum ZSM 1618/2008, Madagascarophis colubrinus ZSM 1620/2008, Madagascarophis sp. nov. ZSM 2130/2007, Mimophis mahfalensis ZSM 2101/2007, Pseudoxyrhopus cf. quinquelineatus ZSM 1610/2008, Thamnosophis martae ZSM 1595/2008 ZSM 1596/2008. Typhlopidae Typhlops microcephalus ZSM 1587/2008.