Checklist of the Amphibians of the Sipaliwini Area, Suriname

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Herpetology Notes, volume 8: 63-68 (2015) (published online on 10 March 2015)

Checklist of the Amphibians of the Sipaliwini area, Suriname

Antoine Fouquet1,*, Jean-Pierre Vacher2, Vanessa Kadosoe3, Rawien Jairam3 and Paul Ouboter3

The Guiana Shield comprises highlands on the western visited this area in 1968 (Hoogmoed, 1969) and part (Pantepui), and low hilly landscape mostly covered provided a list of the species of the savanna (Hoogmoed, by evergreen rainforest on the eastern part (Hammond, 2013). Ten km north of the community lays a Mountain 2005). The eastern part is bounded by the Atlantic range (Apalagadi or Apararake) where a new species of Ocean to the north and the east, by the Amazon River Anomaloglossus has been found in 1989 and described to the south and can be somewhat arbitrarily separated in 2012 as A. leopardus (Ouboter and Jairam, 2012), but by the Rio Negro and the Rio Essequibo to the west. on the basis of only three preserved specimens. Ouboter The amphibian communities found in that bioregion and Jairam (2012) also provide records of amphibians have strong affinities with the rest of the adjacent in this area based on their field notes and specimens in part of Amazonia, but also contain a high proportion the collections of the National Zoological Collection of endemic species (Duellman, 1999). Recent studies of Suriname (NZCS) and the Leiden Natural History suggest that the degree of endemism of the eastern Museum. A third source of comparative information Guiana Shield may be much higher than currently from this area is the herpetological survey undertaken accepted (Fouquet et al., 2007, 2012a). Strong genetic during a “rapid biodiversity assessment” in the nearby structure on mtDNA within many species have also Kwamalatsamutu area (Ouboter et al., 2011). been recovered throughout the eastern Guiana Shield In order to improve datasets on amphibian suggesting past changes in habitat at a much finer scale communities of this remote area and more generally on than previously assumed (Fouquet et al., 2012a,b). the biodiversity of the Guiana Shield, we undertook a These progresses in our understanding of the spatio- field inventory in the Sipaliwini area. We herein provide temporal structure of the biodiversity of that region are a list of the amphibian species encountered and compare however still hampered by the lack of material collected it to previously published records. in remote localities. This is particularly the case for the Two sites within the Sipaliwini Nature Reserve central part of the Guiana Shield, to which accessibility (Suriname) were investigated; (1) the forest of Apalagadi is very limited. A prominent example is an area located Mountain, (2.17816 N; 56.08521 W) located 10 km in southern Suriname at the border with Brazil and north of (2) the savanna and the lowland forest/savannas known as Sipaliwini savanna. The ‘true’ great Sipaliwini surrounding the Sipaliwini community (2.02682 N; savanna lies a few km to the east of a Trio settlement that 56.12564 W)(Figure 1). Two people searched the first can be reached by plane (Figure 1). M.S. Hoogmoed 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, 1 CNRS Guyane USR3456, Immeuble Le Relais, 2 Avenue flooded areas). Calling males were recorded and both Gustave Charlery, 97300, Cayenne, French Guiana. sexes were collected when possible. Specimens were 2 Laboratoire Évolution et Diversité Biologique, UMR 5174 photographed alive, euthanized using Xylocaine 2%, CNRS/UPS/ENFA, Université Paul Sabatier, 118 route de labeled, and then fixed using formalin after tissue was Narbonne, 31062 Toulouse Cedex 9, France 3 National Zoological Collection Suriname (NZCS), Anton de sampled and stored in 95% ethanol. Kom University of Suriname, Paramaribo, Suriname We detected 76 species of amphibians (71 collected) * Corresponding author e-mail:[email protected] including one Gymnophiona. Only four hylid species 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 now contains 84 species of amphibians. This represents collected because calling perches were too high up in one of the highest species richness records reported for the trees (Table 1). Sixteen species were found in the a single area within the Guiana Shield. It is particularly open savanna, of which 12 were exclusively found there. remarkable given the comparatively short survey Forty-eight species were found in the surrounding forest time and limited survey methods (exclusively active among which 23 were only found there. Forty species searches). The high number of species can only partly were found in Apalagadi, of which 15 were exclusively be explained through heterogeneity of the landscape as found there. The vast majority of species recorded the majority of species (63) were detected in a single were hylids (30 species) followed by leptodactylids (15 habitat type, namely forest. Another likely explanation species). Dendrobatids and centrolenids also showed a may be the fact that this area is at the crossover between high richness with nine and seven species, respectively. assemblages comprised of species originating from Twenty-three species have not been recorded during different parts of the Guiana Shield. previous inventories in that region. However, the Some of the new occurrence records are particularly presence of Dendropsophus gaucheri and Scinax sp. noteworthy. Hypsiboas punctatus is for example a 1 were already mentioned in Fouquet et al. (2011) and species associated with open habitat and thought Fouquet (2008), based on material collected by Brice to be restricted to the coastal area of the Guiana P. Noonan in 2003. Only eight species recorded by Shield and the swamps of the Amazon River. The previous visitors were not found, notably Leptodactylus presence of this species as well as other open habitat macrosternum (Hoogmoed, 2013) which is noteworthy dwellers, such as Dendropsophus gaucheri, Scinax because this species is associated to savanna. When nebulosus, S. x-signatus, Scinax fuscomarginatus considering all records, the total species list for the area (Figure 2), Adenomera hylaedactyla, Leptodactylus 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 (Avila-Pires et al., 2010). Therefore, this new record is Pseudopaludicola sp. (Figure 2) in the central part of the not surprising. The second is an undescribed species of shield strongly support past connections between open Allobates documented so far only from the southern half habitats that are currently completely isolated (Fouquet of French Guiana (pers. obs.). Consequently, this new et al., 2011, 2012a). record extends its range about 300 km westward. The occurrence of Hyalinobatrachium kawense We finally highlight the discovery of Chiasmocleis (Figure 2) may seem surprising given that it was only haddadi (Figure 2), a small microhylid recently known to occur in the vicinity of Cayenne in French described from Kotika in French Guiana (Peloso et al., Guiana (Castroviejo-Fisher et al., 2011). However, 2013) and also documented in Southern French Guiana this is probably only the consequence of the lack of and Amapà. This new record extends its range more data available on Centrolenidae. We also recorded than 300 km westward. Cochranella geijskesi, H. mondolfii, H. iaspidiense, H. This survey certainly allowed improving our cappellei, H. taylori, and Vitreorana oyampiensis and understanding of the distribution of the amphibians of this is to be linked with the recent progresses in our the region but also pointed out the efforts that remain understanding of the distributional boundaries and calls to be undertaken in order to unravel the structure of the of centrolenid frogs (Castroviejo-Fisher et al., 2011). biodiversity in the eastern Guiana Shield. Other interesting discoveries were Allobates sumtuosus (Figure 2) and Allobates sp. gr. trinileatus. The first is Acknowledgements. We thank the Nature conservation division known from Trombetas and from Manaus to Central of Suriname and Anton de Kom University of Suriname and P.J.R. Guyana (Simoes et al., 2013) and in northern Parà Kok for providing a pre-review on this manuscript. This work has 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.

SIPA SIPA HOOGMOED RAP OUBOTER & SPECIES APALAGADI SAVANNA FOREST 2013 KWAMALA JAIRAM 2012

Gymnophiona Caecilidae Microcaecilia taylori X X X Anura Allophrynidae Allophryne ruthveni X X X Bufonidae Amazophrynella cf. manaos X X Rhaebo guttatus X X X X Rhinella lescurei1 X X Rhinella marina X X X X X X Rhinella martyi X X X X Centrolenidae Cochranella geijskesi* X X Hyalinobatrachium cappellei X Hyalinobatrachium iaspidiense X X Hyalinobatrachium kawense X Hyalinobatrachium mondolfii X Hyalinobatrachium taylori X X X Vitreorana oyampiensis X Ceratophryidae Ceratophrys cornuta X X Craugastoridae Pristimantis chiastonotus X X X X Pristimantis inguinalis X Pristimantis sp. gr. unistrigatus X X Pristimantis zeuctotylus X X X X Dendrobatidae Allobates femoralis X X X X Allobates cf. granti X X X Allobates sp. gr. trinileatus X X Allobates sumtuosus X Ameerega hahneli X X X X Ameerega trivittata X X ͳ X X Anomaloglossus leopardus X X Anomaloglossus stepheni X X X X Dendrobates tinctorius X X X Hylidae Dendropsophus brevifrons X X Dendropsophus cf. minusculus X X X Dendropsophus gaucheri X X Dendropsophus leucophyllatus X X Dendropsophus marmoratus* X Dendropsophus minutus X X Hypsiboas boans X X X X X Hypsiboas calcaratus X X Hypsiboas cinerascens X X Hypsiboas fasciatus X X Hypsiboas geographicus X X X X Hypsiboas multifasciatus X X Hypsiboas ornatissimus X X Hypsiboas punctatus X Osteocephalus cabrerai1 X Osteocephalus helenae1 X Osteocephalus leprieurii1 X Osteocephalus oophagus X X Osteocephalus taurinus X X Phyllomedusa bicolor* X X Phyllomedusa hypochondrialis X X X X Phyllomedusa tomopterna X Phyllomedusa vaillantii X Scinax boesemani X X X Scinax fuscomarginatus X X X Scinax nebulosus X X X

ʹ Allobates sumtuosus X Ameerega hahneli X X X X Ameerega trivittata X X X X Anomaloglossus leopardus X X Anomaloglossus stepheni X X X X Dendrobates tinctorius X X X Hylidae Dendropsophus brevifrons X X Dendropsophus cf. minusculus X X X Dendropsophus gaucheri X X Dendropsophus leucophyllatus X X Dendropsophus marmoratus* X Checklist of the Amphibians of the Sipaliwini area, Suriname Dendropsophus minutus X X 67 Hypsiboas boans X X X X X FigureHypsiboas 2. Continued. calcaratus X X Hypsiboas cinerascens X X Hypsiboas fasciatus SIPA SIPAX HOOGMOED RAP X OUBOTER & SPECIES APALAGADI Hypsiboas geographicus SAVANNA FOREST X 2013 X KWAMALAX JAIRAMX 2012 GymnophionaHypsiboas multifasciatus X X CaecilidaeHypsiboas ornatissimus X X MicrocaeciliaHypsiboas punctatus taylori X X X X 1 AnuraOsteocephalus cabrerai X 1 AllophrynidaeOsteocephalus helenae X 1 AllophryneOsteocephalus ruthveni leprieurii X X X BufonidaeOsteocephalus oophagus X X AmazophrynellaOsteocephalus taurinuscf. manaos X X X RhaeboPhyllomedusa guttatus bicolor* X X X X RhinellaPhyllomedusa lescurei hypochondrialis1 X X X X RhinellaPhyllomedusa marina tomopterna X X X X X X RhinellaPhyllomedusa martyi vaillantii X X X X CentrolenidaeScinax boesemani X X X CochranellaScinax fuscomarginatus geijskesi* X X X X X HyalinobatrachiumScinax nebulosus cappellei X X X X HyalinobatrachiumScinax proboscideus iaspidiense2 X X X HyalinobatrachiumScinax ruber kawense X X X HyalinobatrachiumScinax sp. 1 mondolfii X X ʹ HyalinobatrachiumScinax sp. 2 taylori X X X VitreoranaScinax sp. 3 oyampiensis X X CeratophryidaeScinax x-signatus X X CeratophrysTrachycephalus cornuta hadroceps* X X CraugastoridaeTrachycephalus resinifictrix* X X PristimantisLeptodactylidae chiastonotus X X X X PristimantisAdenomera andreae inguinalis X X X PristimantisAdenomera heyerisp. gr. unistrigatus X X X PristimantisAdenomera hylaedactyla zeuctotylus X X X X X DendrobatidaeLeptodactylus guianensis X X X X X AllobatesLeptodactylus femoralis knudseni X X X X AllobatesLeptodactyluscf. granti longirostris X X X X AllobatesLeptodactylussp. gr macrosternum. trinileatus 1 X X X X Leptodactylus myersi1 X Leptodactylus mystaceus X X X X Leptodactylus pentadactylus X ͳ X X Leptodactylus rhodomystax X X X Leptodactylus sp. 1 gr. podicipinus X X X Leptodactylus sp. 2 gr. podicipinus X X Leptodactylus stenodema X Lithodytes lineatus X X Physalaemus ephippifer X X X X Pseudopaludicola sp. X X Microhylidae Chiasmocleis haddadi X Chiasmocleis shudikarensis X X Hamptophryne boliviana X X X Otophryne pyburni X Pipidae Pipa aspera1 X

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Accepted by Raffael Ernst