Checklist of the Amphibians of the Sipaliwini area, Suriname

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1 Herpetology Notes, volume 8: (2015) (published online on 10 March 2015) Checklist of the Amphibians of the Sipaliwini area, Suriname Antoine Fouquet 1, *, Jean-Pierre Vacher 2, Vanessa Kadosoe 3, Rawien Jairam 3 and Paul Ouboter 3 The Guiana Shield comprises highlands on the western part (Pantepui), and low hilly landscape mostly covered by evergreen rainforest on the eastern part (Hammond, 2005). The eastern part is bounded by the Atlantic Ocean to the north and the east, by the Amazon River to the south and can be somewhat arbitrarily separated by the Rio Negro and the Rio Essequibo to the west. The amphibian communities found in that bioregion have strong affinities with the rest of the adjacent part of Amazonia, but also contain a high proportion of endemic species (Duellman, 1999). Recent studies suggest that the degree of endemism of the eastern Guiana Shield may be much higher than currently accepted (Fouquet et al., 2007, 2012a). Strong genetic structure on mtdna within many species have also been recovered throughout the eastern Guiana Shield suggesting past changes in habitat at a much finer scale than previously assumed (Fouquet et al., 2012a,b). These progresses in our understanding of the spatiotemporal structure of the biodiversity of that region are however still hampered by the lack of material collected in remote localities. This is particularly the case for the central part of the Guiana Shield, to which accessibility is very limited. A prominent example is an area located in southern Suriname at the border with Brazil and known as Sipaliwini savanna. The true great Sipaliwini savanna lies a few km to the east of a Trio settlement that can be reached by plane (Figure 1). M.S. Hoogmoed 1 CNRS Guyane USR3456, Immeuble Le Relais, 2 Avenue Gustave Charlery, 97300, Cayenne, French Guiana. 2 Laboratoire Évolution et Diversité Biologique, UMR 5174 CNRS/UPS/ENFA, Université Paul Sabatier, 118 route de Narbonne, Toulouse Cedex 9, France 3 National Zoological Collection Suriname (NZCS), Anton de Kom University of Suriname, Paramaribo, Suriname * Corresponding author fouquet.antoine@gmail.com visited this area in 1968 (Hoogmoed, 1969) and provided a list of the species of the savanna (Hoogmoed, 2013). Ten km north of the community lays a Mountain range (Apalagadi or Apararake) where a new species of Anomaloglossus has been found in 1989 and described in 2012 as A. leopardus (Ouboter and Jairam, 2012), but on the basis of only three preserved specimens. Ouboter and Jairam (2012) also provide records of amphibians in this area based on their field notes and specimens in the collections of the National Zoological Collection of Suriname (NZCS) and the Leiden Natural History Museum. A third source of comparative information from this area is the herpetological survey undertaken during a rapid biodiversity assessment in the nearby Kwamalatsamutu area (Ouboter et al., 2011). In order to improve datasets on amphibian communities of this remote area and more generally on the biodiversity of the Guiana Shield, we undertook a field inventory in the Sipaliwini area. We herein provide a list of the amphibian species encountered and compare it to previously published records. Two sites within the Sipaliwini Nature Reserve (Suriname) were investigated; (1) the forest of Apalagadi Mountain, ( N; W) located 10 km north of (2) the savanna and the lowland forest/savannas surrounding the Sipaliwini community ( N; W)(Figure 1). Two people searched the first site during 4 days (8 people*day) and the second site was inventoried by 4 people during 4 days plus 2 people during 5 additional days (26 people*days ) during the rainy season (15-28/04/2014). We used visual and acoustic searches mainly during afternoons and nights in different habitats (river/stream banks, leaf litter, flooded areas). Calling males were recorded and both sexes were collected when possible. Specimens were photographed alive, euthanized using ylocaine 2%, labeled, and then fixed using formalin after tissue was sampled and stored in 95% ethanol. We detected 76 species of amphibians (71 collected) including one Gymnophiona. Only four hylid species

2 64 Antoine Fouquet et al. Figure 1. A, South America; B, northern South America indicating topography and the location of savannas (in white); C, the portion of the Sipaliwini savanna occurring in Suriname with the positions of the two main sampling location. and one centrolenid were exclusively heard but not collected because calling perches were too high up in the trees (Table 1). Sixteen species were found in the open savanna, of which 12 were exclusively found there. Forty-eight species were found in the surrounding forest among which 23 were only found there. Forty species were found in Apalagadi, of which 15 were exclusively found there. The vast majority of species recorded were hylids (30 species) followed by leptodactylids (15 species). Dendrobatids and centrolenids also showed a high richness with nine and seven species, respectively. Twenty-three species have not been recorded during previous inventories in that region. However, the presence of Dendropsophus gaucheri and Scinax sp. 1 were already mentioned in Fouquet et al. (2011) and Fouquet (2008), based on material collected by Brice P. Noonan in Only eight species recorded by previous visitors were not found, notably Leptodactylus macrosternum (Hoogmoed, 2013) which is noteworthy because this species is associated to savanna. When considering all records, the total species list for the area now contains 84 species of amphibians. This represents one of the highest species richness records reported for a single area within the Guiana Shield. It is particularly remarkable given the comparatively short survey time and limited survey methods (exclusively active searches). The high number of species can only partly be explained through heterogeneity of the landscape as the majority of species (63) were detected in a single habitat type, namely forest. Another likely explanation may be the fact that this area is at the crossover between assemblages comprised of species originating from different parts of the Guiana Shield. Some of the new occurrence records are particularly noteworthy. Hypsiboas punctatus is for example a species associated with open habitat and thought to be restricted to the coastal area of the Guiana Shield and the swamps of the Amazon River. The presence of this species as well as other open habitat dwellers, such as Dendropsophus gaucheri, Scinax nebulosus, S. x-signatus, Scinax fuscomarginatus (Figure 2), Adenomera hylaedactyla, Leptodactylus

3 Checklist of the Amphibians of the Sipaliwini area, Suriname 65 Figure 2. Some species of amphibians collected in the Sipaliwini area: A: Microcaecilia taylori; B: Hyalinobatrachium kawense; C: H. taylori; D: Allobates sumtuosus; E: Anomaloglossus leopardus; F: Scinax fuscomarginatus; G: Pseudopaludicola sp.; H: Lithodytes lineatus; I: Chiasmocleis haddadi. longirostris, L. macrosternum (Hoogmoed, 2013), and Pseudopaludicola sp. (Figure 2) in the central part of the shield strongly support past connections between open habitats that are currently completely isolated (Fouquet et al., 2011, 2012a). The occurrence of Hyalinobatrachium kawense (Figure 2) may seem surprising given that it was only known to occur in the vicinity of Cayenne in French Guiana (Castroviejo-Fisher et al., 2011). However, this is probably only the consequence of the lack of data available on Centrolenidae. We also recorded Cochranella geijskesi, H. mondolfii, H. iaspidiense, H. cappellei, H. taylori, and Vitreorana oyampiensis and this is to be linked with the recent progresses in our understanding of the distributional boundaries and calls of centrolenid frogs (Castroviejo-Fisher et al., 2011). Other interesting discoveries were Allobates sumtuosus (Figure 2) and Allobates sp. gr. trinileatus. The first is known from Trombetas and from Manaus to Central Guyana (Simoes et al., 2013) and in northern Parà (Avila-Pires et al., 2010). Therefore, this new record is not surprising. The second is an undescribed species of Allobates documented so far only from the southern half of French Guiana (pers. obs.). Consequently, this new record extends its range about 300 km westward. We finally highlight the discovery of Chiasmocleis haddadi (Figure 2), a small microhylid recently described from Kotika in French Guiana (Peloso et al., 2013) and also documented in Southern French Guiana and Amapà. This new record extends its range more than 300 km westward. This survey certainly allowed improving our understanding of the distribution of the amphibians of the region but also pointed out the efforts that remain to be undertaken in order to unravel the structure of the biodiversity in the eastern Guiana Shield. Acknowledgements. We thank the Nature conservation division of Suriname and Anton de Kom University of Suriname and P.J.R. Kok for providing a pre-review on this manuscript. This work has

4 66 Antoine Fouquet et al. Table 1. Species detected. Asterisks indicate species detected but not collected and 1 indicates species not detected but listed in previous surveys. SPECIES SAVANNA FOREST APALAGADI HOOGMOED 2013 RAP KWAMALA OUBOTER & JAIRAM 2012 Gymnophiona Caecilidae Microcaecilia taylori Anura Allophrynidae Allophryne ruthveni Bufonidae Amazophrynella cf. manaos Rhaebo guttatus Rhinella lescurei 1 Rhinella marina Rhinella martyi Centrolenidae Cochranella geijskesi* Hyalinobatrachium cappellei Hyalinobatrachium iaspidiense Hyalinobatrachium kawense Hyalinobatrachium mondolfii Hyalinobatrachium taylori Vitreorana oyampiensis Ceratophryidae Ceratophrys cornuta Craugastoridae Pristimantis chiastonotus Pristimantis inguinalis Pristimantis sp. gr. unistrigatus Pristimantis zeuctotylus Dendrobatidae Allobates femoralis Allobates cf. granti Allobates sp. gr. trinileatus Allobates sumtuosus Ameerega hahneli Ameerega trivittata Anomaloglossus leopardus Anomaloglossus stepheni Dendrobates tinctorius Hylidae Dendropsophus brevifrons Dendropsophus cf. minusculus Dendropsophus gaucheri Dendropsophus leucophyllatus Dendropsophus marmoratus* Dendropsophus minutus Hypsiboas boans Hypsiboas calcaratus Hypsiboas cinerascens Hypsiboas fasciatus Hypsiboas geographicus

5 Checklist of the Amphibians of the Sipaliwini area, Suriname 67 Figure 2. Continued. SPECIES SAVANNA FOREST APALAGADI HOOGMOED 2013 RAP KWAMALA OUBOTER & JAIRAM 2012 Hypsiboas multifasciatus Hypsiboas ornatissimus Hypsiboas punctatus Osteocephalus cabrerai 1 Osteocephalus helenae 1 Osteocephalus leprieurii 1 Osteocephalus oophagus Osteocephalus taurinus Phyllomedusa bicolor* Phyllomedusa hypochondrialis Phyllomedusa tomopterna Phyllomedusa vaillantii Scinax boesemani Scinax fuscomarginatus Scinax nebulosus Scinax proboscideus 2 Scinax ruber Scinax sp. 1 Scinax sp. 2 Scinax sp. 3 Scinax x-signatus Trachycephalus hadroceps* Trachycephalus resinifictrix* Leptodactylidae Adenomera andreae Adenomera heyeri Adenomera hylaedactyla Leptodactylus guianensis Leptodactylus knudseni Leptodactylus longirostris Leptodactylus macrosternum 1 Leptodactylus myersi 1 Leptodactylus mystaceus Leptodactylus pentadactylus Leptodactylus rhodomystax Leptodactylus sp. 1 gr. podicipinus Leptodactylus sp. 2 gr. podicipinus Leptodactylus stenodema Lithodytes lineatus Physalaemus ephippifer Pseudopaludicola sp. Microhylidae Chiasmocleis haddadi Chiasmocleis shudikarensis Hamptophryne boliviana Otophryne pyburni Pipidae Pipa aspera 1

6 68 benefited from an «Investissements d Avenir» grant managed by Agence Nationale de la Recherche (CEBA Center for the study of biodiversity in Amazonia, ref. ANR-10-LAB-25-01). We are also grateful to the Trio community in particular Nemo and Senio who accompanied us to Apalagadi. Our gratitude goes also towards Jérôme Murienne, Piero Delprete and Gunovaino Marjanom for their friendly company at the base camp and to Rawien Jairam for helping with permits and logistics. Nature conservation Division of Suriname authorized the research and Suriname Forest Service issued the export permit # Literature Cited Avila-Pires, T.C.S., Hoogmoed, M.S., Rocha, W.A. (2010): Notes on the vertebrates of northern Pará, Brazil: a forgotten part of the Guianan Region, I. Herpetofauna. Boletim domuseu Paraense Emílio Goeldi 5: Castroviejo-Fisher, S. Vila, C., Ayarzagüena, J., Blanc, M., Ernst, R. (2011): Species diversity of Hyalinobatrachium glassfrogs (Amphibia: Centrolenidae) from the Guiana Shield, with the description of two new species. Zootaxa 3132: Duellman, W.E. (1999): Patterns of distribution of Amphibians: a global perspective. Baltimore (MD), Johns Hopkins University Press. Fouquet, A., Gilles, A., Vences, M., Marty, C., Blanc, M., Gemmell N.J. (2007): Underestimation of species richness in Neotropical frogs revealed by mtdna analyses. PLoS ONE 2(10): e1109. doi: /journal.pone Fouquet, A., Ledoux, J-B., Scotti-Saintagne, C., Dubut, V., Noonan, B.P., Scotti I. (2012): The interplay of dispersal limitation, rivers and historical events shapes the genetic structure of an Amazonian frog. BJLS 106: Fouquet, A., Noonan, B. P., Blanc, M., Dill Orrico, V.G. (2011): Phylogenetic position of Dendropsophus gaucheri (Lescure and Marty 2000) highlights the need for an in-depth investigation of the phylogenetic relationships of Dendropsophus (Anura: Hylidae). Zootaxa 3035: Fouquet, A., Noonan, B.P., Rodrigues, M.T., Pech, N., Gilles, A., Gemmell N.J. (2012): Multiple quaternary refugia in the eastern Guiana Shield revealed by comparative phylogeography of 12 frog species. Systematic Biology 61: Antoine Fouquet et al. Hammond, D.S. (2005): Tropical forests of the Guiana Shield: ancient forests in a modern world. Cambridge (MA), CABI publishing. Hoogmoed, M.S. (1969): Notes on the herpetofauna of Surinam III. A new species of Dendrobates (Amphibia, Salientia, Dendrobatidae) from Surinam. Zool. Mededel 12: Hoogmoed, M.S. (2013): Status and Conservation of Amphibians in Suriname. In: Amphibian Biology, Volume 9 part 3, Status of Decline of Amphibians: Western Hemisphere: Venezuela, Guyana, Suriname, and French Guiana, p Heatwole, H., and Wilkinson, J.W., Eds. Baulkham Hills, NSW, Australia. Surrey Beatty & Sons. Ouboter, P.E., Jairam, R. (2012): Amphibians of Suriname. Brill. Ouboter,P.E., Jairam, R., Kasanpawiro, C. (2011): A rapid assessment of the amphibians and reptiles of the Kwamalasamutu region (Kutari/lower Sipaliwini Rivers), Suriname. In: A Rapid Biological Assessment of the Kwamalasamutu region, Southwestern Suriname, p O Shea, B.J., A nso, L.E., Larsen, T.H., Eds. RAP Bulletin of Biological Assessment 63. Conservation International, Arlington, VA. Peloso, P.L.V., Sturaro, M.J., Forlani, M.C.; Gaucher, P., Motta, A.P., Wheeler, W. (2014): Phylogeny, taxonomic revision, and character evolution of the genera Chiasmocleis and Syncope (Anura, Microhylidae) in Amazonia, with descriptions of three new species. Bulletin of the American Museum of Natural History 386: Simoes, P.I., Kaefer, I.L., Farias, I.P., Lima, A.P. (2013): An integrative appraisal of the diagnosis and distribution of Allobates sumtuosus (Morales, 2002)(Anura, Aromobatidae). Zootaxa 3746(3): Accepted by Raffael Ernst