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Home , Alopoglossus, Alopoglossus angulatus, Anilius, Anomalepididae, Arthrosaura, Arthrosaura kockii

Herpetology Notes, volume 14: 539-550 (2021) (published online on 18 March 2021)

Checklist of the from the Cancão Municipal Natural Park, state of Amapá, eastern Amazon,

Carlos Eduardo Costa-Campos1,*, Patrick Ribeiro Sanches1, Fillipe Pedroso-Santos1, Vinicius A. M. B. de Figueiredo1, Rodrigo Tavares-Pinheiro1, and Wirley Almeida-Santos2

Abstract. The distribution of the in the eastern Amazon region is still poorly known. Here we give a list of reptile species from the Cancão Municipal Natural Park, municipality of Serra do Navio, state of Amapá, Brazil. We recorded through active search a total of 57 species, including two , one crocodilian, 30 , and 24 . Two species, Mesoclemmys gibba () and Pseudoboa coronata (), were new records for the state of Amapá. The number of species in forested and open area environments accounted for 62.5% and 37.5 % of total species sampled, respectively. Of the 57 recorded species, 42 were assigned as Least Concern according to the Red List of Threatened Species from the International Union for Conservation of Nature, and 15 have not been evaluated so far. Our findings complement the available information about the distribution and richness of species that compose the herpetofauna of Amazonia.

Keywords. Herpetofauna, Amazon biome, Filling gaps, Inventories.

Introduction conservation importance (Drummond et al., 2008; Hilário et al., 2017). Herpetofauna is particularly diverse in Brazilian In the state of Amapá, herpetological inventories are Amazon, with more than 375 species of reptiles (Ávila- concentrated on anurans (Queiroz et al., 2011; Pereira- Pires and Prudente, 2019). However, this number is Júnior et al., 2013; Araújo and Costa-Campos, 2014; likely underestimated due to the vast Amazonian extent Campos et al., 2015; Benício and Lima, 2017; Lima (6 million km2) and many areas that remain remote or et al., 2017; Silva-e-Silva and Costa-Campos, 2018; difficult to access and are still poorly known in terms of Costa-Campos and Freire, 2019). Due to the lack of their herpetofauna (Azevedo-Ramos and Galatti, 2002; information about inventories on reptiles in the region, Ávila-Pires et al., 2007; Ávila-Pires et al., 2010). we present here the reptile species list based on novel Despite the growing number of studies addressing the data through field expeditions to the Cancão Municipal geographic distribution and richness of the Amazonian Natural Park, municipality of Serra do Navio, in state herpetofauna (e.g., Ávila-Pires et al., 2018; Fonseca of Amapá, Brazil. Additionally, we briefly address the et al., 2019; Debien et al., 2019; Freitas et al., 2020; species conservation status based on the IUCN (2020) Frazão et al., 2020), the diversity of these taxa in the and new distribution records of some species. state of Amapá is still poorly known. The state of Amapá has about 72 % of its territory covered by Materials and Methods protected areas (Dias et al., 2016). The majority of the state is within a continuum of 12 conservations units Study area. The Cancão Municipal Natural Park and five indigenous lands, representing an area of great (CMNP), a National Park category (SNUC, 2000) created by municipality of Serra do Navio, comprises 370 ha of Amazonian in the northwest centre portion of the state of Amapá, Brazil (Figure 1). The climate of the region is classified as Equatorial (Am of 1 Laboratório de Herpetologia, Departamento de Ciências Biológicas e da Saúde, Universidade Federal do Amapá, Köpper-Geiger classification), with average temperature Macapá, Amapá 68903-419, Brazil. of 27.6 ºC and rainfall annual of 2,850 mm (Alvares et 2 Secretaria Municipal de Turismo, Prefeitura Municipal de al., 2013). Serra do Navio, Serra do Navio, Amapá 68948-000, Brazil. Data sampling. Surveys of lizards and snakes were * Corresponding author. E-mail: [email protected] undertaken from March 2018 to December 2018. We © 2021 by Notes. Open Access by CC BY-NC-ND 4.0. established two sampling transects of 5 km each in 540 Carlos Eduardo Costa-Campos et al.

Figure 1. Map of the Cancão Municipal Natural Park, in the municipality of Serra do Navio, state of Amapá, Brazil.

the study area: (1) Terra Firme trail at Cancão forest Mesoclemmys gibba (Schweigger, 1812), Paleosuchus (0.90275°N, 52.00497°W) and (2) River Amapari trail trigonatus (Schneider, 1801), Corallus caninus (0.9008°N, 52.0134°W). Three sampling events were (Linnaeus, 1758), nebulatus (Linnaeus, 1758), conducted by three people in each of the two sites. Each variegate (Duméril, Bibron & Duméril, 1854), sampling event consisted of two periods of three hours Philodryas olfersii (Lichtenstein, 1823), and Bothrops between 0900h-1200h (day) and 1800h-2100h (night), bilineatus bilineatus (Wied, 1821) were observed and through visual surveys (Corn and Bury, 1990; Franco et photographed (but not collected). Specimens of the first al., 2002). Therefore, the sampling effort employed in three species were not collected because we did not each site totalled 54 person-hours (3 people × 6 hours have a collecting permit when they were recorded, while × 3 sampling events). Pitfall traps with drift fences and specimens of the other species escaped during sampling. incidental encounters were not used in the sampling. Voucher specimens (ICMBio/SISBIO #48102-2) Data Analysis. We performed three accumulation were deposited in the Herpetological Collection of curves for (1) lizards, (2) snakes, and (3) all reptile Laboratório de Herpetologia from Universidade Federal species (turtles, crocodilian, lizards, and snakes) in do Amapá (Appendix I). The species conservation a combined analysis using the sample-based method status was based on the IUCN (2020). The taxonomic (Gotelli and Colwell, 2001) through 1000 randomisations nomenclature applied herein follows Costa and Bérnils of an abundance matrix where each column represents (2018). a species and each row represents a sample. We used species richness estimator Jacknife1 to determine the Results expected richness of (1) lizards, (2) snakes, and (3) reptiles combined. This analysis was performed using We recorded a total of 57 reptile species in the study EstimateS v.9.1.0 (Colwell, 2013). Species richness area, including two turtles, one crocodilian, 30 lizards, was calculated using the Menhinick’s index using PAST and 24 snakes (Table 1, Figures 2–5). The number of software (Hammer et al., 2001). species recorded in forest only (considering water Voucher specimens. Specimens were anesthetised environments in primary and secondary ), in with 5 % lidocaine, fixed with 10 % formalin, and open area only, and in both (forest and open area preserved in 70 % ethanol (Heyer et al., 1994). Sampled environments), accounted for 63.2, 21.1, and 15.7 % of individual of Chelonoidis carbonarius (Spix, 1824), total species sampled, respectively. Of the 57 recorded Checklist of the reptiles from the Cancão Municipal Natural Park, Brazil 541

Table 1. recorded at Cancão Municipal Natural Park, municipality of Serra do Navio, state of Amapá, Brazil. Sampled areas: Terra Firme trail at Cancão forest (TC); River Amapari trail (TA). Habitats: Open area (OA); Forest (F); IUCN Red List Criteria: LC – Least Concern; NE - not evaluated. *First record for the state of Amapá. Table 1.

Taxon Sampled areas Habitats IUCN TC TA OA F TESTUDINES Testudinidae Chelonoidis carbonarius (Spix, 1824) X X X NE Mesoclemmys gibba (Schweigger, 1812)* X X NE CROCODYLIA Paleosuchus trigonatus (Schneider, 1801) X X LC (Lizards) Hemidactylus mabouia (Moreau de Jonnès, 1818) X X X NE Thecadactylus rapicauda (Houttuyn, 1782) X X LC Chatogekko amazonicus (Andersson, 1918) X X X LC Gonatodes humeralis (Guichenot, 1855) X X X LC Lepidoblepharis heyerorum Vanzolini, 1978 X X X LC Mabuyidae Copeoglossum nigropunctatum (Spix, 1825) X X X X LC Dactyloa punctata (Daudin, 1802) X X X NE Norops auratus (Daudin, 1802) X X X NE Norops chrysolepis (Duméril and Bibron, 1837) X X NE Norops fuscoauratus (D’Orbigny, 1837 in Duméril and X X NE Bibron, 1837) Norops ortonii (Cope, 1868) X X NE iguana iguana (Linnaeus, 1758) X X X X LC marmoratus (Linnaeus, 1758) X X LC plica (Linnaeus, 1758) X X X NE Plica umbra umbra (Linnaeus, 1758) X X X LC azureum azureum (Linnaeus, 1758) X X X LC superciliosus (Linnaeus, 1758) X X LC Alopoglossidae angulatus (Linnaeus, 1758) X X LC Iphisa elegans elegans Gray, 1851 X X LC aff. argulus Peters, 1863 X X LC ocellata Wagler, 1830 X X LC bicarinatus (Linnaeus, 1758) X X LC

542 Carlos Eduardo Costa-Campos et al.

Table 1. Continued.

Taxon Sampled areas Habitat IUCN TC TA OA F Boulenger 1900 X X LC kockii (Lidth de Jeude, 1904) X X LC Loxopholis guianense (Ruibal, 1952) X X X LC Ameiva ameiva ameiva (Linnaeus, 1758) X X X LC cryptus Cole and Dessauer, 1993 X X X NE calcarata Spix, 1825 X X X LC Kentropyx striata (Daudin, 1802) X X X LC Tupinambis teguixin (Linnaeus, 1758) X X X NE SQUAMATA (Snakes) squamosus (Schlegel, 1839) X X LC Aniliidae scytale (Linnaeus, 1758) X X LC Boa constrictor constrictor Linnaeus, 1758 X X NE Corallus caninus (Linnaeus, 1758) X X X LC Corallus hortulanus (Linnaeus, 1758) X X X LC exoletus (Linnaeus, 1758) X X LC Chironius scurrulus (Wagler in Spix, 1824) X X LC Dendrophidion dendrophis (Schlegel, 1837) X X LC Leptophis ahaetulla (Linnaeus, 1758) X X LC fulgidus (Daudin, 1803) X X X LC Dipsadidae Dipsas catesbyi (Sentzen, 1796) X X X LC Dipsas variegata (Duméril, Bibron & Duméril, 1854) X X X LC Sibon nebulatus (Linnaeus, 1758) X X X LC Apostolepis quinquelineata Boulenger, 1896 X X NE Helicops angulatus (Linnaeus, 1758) X X X X LC Philodryas argentea (Daudin, 1803) X X LC Philodryas olfersii (Lichtenstein, 1823) X X LC melanogenys melanogenys (Tschudi, 1845) X X LC Pseudoboa coronata Schneider, 1801* X X LC compressus (Daudin, 1803) X X X LC Erythrolamprus miliaris miliaris (Linnaeus, 1758) X X LC Micrurus lemniscatus lemniscatus (Linnaeus, 1758) X X LC Bothrops bilineatus bilineatus (Wied, 1821) X X NE Bothrops atrox (Linnaeus, 1758) X X X X NE

Checklist of the reptiles from the Cancão Municipal Natural Park, Brazil 543

Figure 2. Reptiles recorded in Cancão Municipal Natural Park, municipality of Serra do Navio, state of Amapá, Brazil. A) Chelonoidis carbonarius; B) Mesoclemmys gibba; C) Paleosuchus trigonatus; D) Hemidactylus mabouia; E) Thecadactylus rapicauda; F) Chatogekko amazonicus; G) Gonatodes humeralis; H) Lepidoblepharis heyerorum; I) Copeoglossum nigropunctatum; J) Dactyloa punctata; K) Norops auratus; L) Norops chrysolepis; M) Norops fuscoauratus; N) Norops ortonii; O) Iguana iguana iguana. 544 Carlos Eduardo Costa-Campos et al.

Figure 3. Reptiles recorded in Cancão Municipal Natural Park, municipality of Serra do Navio, state of Amapá, Brazil. A) Polychrus marmoratus; B) ; C) Plica umbra umbra; D) azureum; E) Uranoscodon superciliosus; F) ; G) Iphisa elegans elegans; H) Cercosaura aff. argulus; I) Cercosaura ocellata ocellata; J) ; K) Neusticurus rudis; L) ; M) Loxopholis guianense; N) Ameiva ameiva ameiva; O) Cnemidophorus cryptus. Checklist of the reptiles from the Cancão Municipal Natural Park, Brazil 545

Figure 4. Reptiles recorded in Cancão Municipal Natural Park, municipality of Serra do Navio, state of Amapá, Brazil. A) Kentropyx calcarata; B) Kentropyx striata; C) Tupinanbis teguixin (Photo by Girlan Dias); D) Typhlophis squamosus; E) Anilius scytale; F) Boa constrictor constrictor; G) Corallus caninus; H) Corallus hortulanus; I) Chironius exoletus; J) Chironius scurrulus; K) Dendrophidion dendrophis; L) Leptophis ahaetulla ahaetulla; M) Oxybelis fulgidus; N) Dipsas catesbyi; O) Dipsas variegata. 546 Carlos Eduardo Costa-Campos et al.

Figure 5. Reptiles recorded in Cancão Municipal Natural Park, municipality of Serra do Navio, state of Amapá, Brazil. A) Sibon nebulatus; B) Apostolepis quinquelineata; C) Helicops angulatus; D) Philodryas argentea; E) Philodryas olfersii (Photo by Kurazo Okada); F) Oxyrhopus melanogenys melanogenys; G) Pseudoboa coronata; H) Siphlophis compressus; I) Erythrolamprus miliaris miliaris; J) Micrurus lemniscatus lemniscatus; K) Bothrops atrox. species, 42 were assigned as least concern (LC) by IUCN (Sanches et al., 2020; Tavares-Pinheiro et al., 2021). Red List criteria, and 15 have not been evaluated (NE) Based on the Jackknife1 estimator, the rarefaction (IUCN, 2020). Mesoclemmys gibba (Schweigger, 1812) curve implies on a species richness of 36.3 species, and Pseudoboa coronata Schneider, 1801 represents 35.7 snake species, and 76.8 reptile fauna combined. As the first record of these species for the state of Amapá none of the curves reached asymptote, we believe that Checklist of the reptiles from the Cancão Municipal Natural Park, Brazil 547 the area should harbour more reptile species than we rarefaction curve for snake species was still rising. We recorded here (Figure 6). did not collect at least six snake species which are widely Menhinick’s Index revealed that Terra Firme trail at distributed in the Amazonia domain and commonly Cancão forest (6.56) had higher richness compared to known in Amapá: Epicrates cenchria (Linnaeus, 1758), the River Amapari trail (6.00). In addition, forest habitats Eunectes deschauenseei Dunn & Conant, 1936, Lachesis (6.71) had higher species richness value compared to muta (Linnaeus, 1766), Micrurus surinamensis (Cuvier, open areas (4.58). 1817), Chironius fuscus (Linnaeus, 1758), and Dipsas indica Laurenti, 1768. All these species are presumed to Discussion occur in the studied area (Campos et al., 2015; Nogueira et al., 2019; Prudente et al., 2020). The local richness of lizards we found for the study area As observed in other studies encompassing the (30 species) is consistent with other studies performed in Amazonia domain, we found a higher species richness the Brazilian Amazonia, which has recorded a minimum in forested habitats (Ávila-Pires et al., 2009; Ávila- local richness of 22 lizard species and a maximum of Pires et al., 2010; Nogueira et al., 2019), although some 44 species per inventory area (Ávila-Pires et al., 2009; species were also associated, exclusively or not, with Ávila-Pires et al., 2010; Prudente et al., 2013). Here, open areas, such as Copeoglossum nigropunctatum, the Gymnophthalmidae had the highest species richness (seven species, 23.3 % of the total), followed by Teiidae (five, 16.7 %) and Tropiduridae (four, 13.3 %). The pattern of higher numbers of lizard species recorded for Gymnophthalmidae and Teiidae is common in the (Prudente et al., 2013; Ribeiro-Júnior and Amaral, 2017; Peixoto et al., 2019). Among snakes, Dipsadidae was the most diverse, with 11 species (45.8 % of the total number), followed by Colubridae (five species, 20.8 %) and Boidae (three species, 12.5 %). A large number of dipsadid snakes have also been reported in several studies in the Amazon domain (Santos-Costa et al., 2015; Nogueira et al., 2019). The Cancão Municipal Natural Park (CMNP) reptile assemblage is composed of a mix of forest and open area species and represents 34.8 % of the reptile species found in the state of Amapá (Costa and Bérnils, 2018). In our list, one taxon (i.e., Cercosaura aff. argulus) has uncertainty in terms of its identification, due to some taxonomic issues, which may indicate a need for further taxonomic revisions. The richness of reptiles at the CMNP is high when compared to other inventories in state of Amapá: Fazendinha Environmental Protection Area (23 lizard species; Campos et al., 2015), and in areas of dense and open forest in the Tumucumaque Mountains National Park (34 species; Lima, 2008). In the CMNP, most reptile species (36 species, 63.2 %) were found only in forested environments, whereas eight species (14 %) are widely distributed in both environments (open area and forest). Regarding the geographic distribution of the species sampled, most of Figure 6. Sample-based rarefaction curves estimated for them (68.4 %) are widely distributed in Amazonia or reptile species with the Jackknife1 estimator for Cancão can exceed the range out of Amazonia to other biomes. Municipal Natural Park, municipality of Serra do Navio, state None of the three rarefaction curves reached the of Amapá, Brazil. A) Lizards, B) snakes, and C) all reptiles asymptote. Despite the large number of species, the combined (turtles, crocodilian, lizards, and snakes). 548 Carlos Eduardo Costa-Campos et al.

Helicops angulatus, and Bothrops atrox. Many reptile in Parque Estadual do Utinga, a protected area surrounded by species found in our study are frequently associated urbanization. Herpetology Notes 11: 499–512. with anthropogenic habitats, such as the exotic gekkonid Ávila-Pires, T.C.S., Prudente, A.L.C. (2019): The census: reptiles. Available at: http://www.museu-goeldi.br/ Hemidactylus mabouia and the native lizards Iguana censo/. Accessed on 23 August 2019. iguana iguana, Ameiva ameiva ameiva, Cercosaura Azevedo-Ramos, C., Galatti, U. (2002): Patterns of ocellata ocellata, Cnemidophorus cryptus, as well as diversity in brazilian Amazonia: conservation implications. the snakes Typhlophis squamosus, and Boa constrictor Biological Conservation 103: 103–111. constrictor. Benício, R.A., Lima, J.D. (2017): Anurans of Amapá National Our results suggest that CMNP has a relatively high Forest, Eastern Amazonia, Brazil. Herpetology Notes 10: 627– 633. local species richness, which is representative of the Campos, C.E.C., Lima, J.D., Lima, J.R.F. (2015): Riqueza e reptile diversity in the Brazilian Amazon. This paper composição de répteis Squamata (lagartos e anfisbenas) da Área provides the first official list of reptiles for Cancão de Proteção Ambiental da Fazendinha, Amapá, Brasil. Biota Municipal Natural Park. Our findings complement the Amazônia 5: 84–90. available information about the distribution and richness Colwell, R.K. 2013. EstimateS: Statistical Estimation of Species of species that compose the herpetofauna of Amazonia. Richness and Shared Species from Samples. Version 9. Department of Ecology & Evolutionary Biology, University of Connecticut, Storrs, Connecticut, USA. Available at: http://purl. Acknowledgments. We are grateful to Ronildo Benício who oclc.org/estimates. Accessed 29 April 2020. provided useful suggestions on an earlier version of this Corn, P.S., Bury, R.B. (1990): Sampling methods for terrestrial manuscript and pre-peer-review; colleagues of “Laboratório and reptiles. General Technical Report. Portland, de Herpetologia” for support during our field work; Instituto OR, US Department of Agriculture, Forest Service, Pacific Chico Mendes de Conservação da Biodiversidade (ICMBio) for Northwest Research Station. providing collection permits (SISBIO #48102-2) and Prefeitura Costa, H.C., Bérnils, R.S. (2018): Répteis do Brasil e suas unidades Municipal de Serra do Navio for authorising us to conduct the federativas: lista de espécies. Herpetologia Brasileira 7: 11–57. research in the Cancão Municipal Natural Park. We thank Pró- Costa-Campos, C.E., Freire, E.M.X. (2019): Richness and Reitoria de Ensino de Graduação, Universidade Federal do composition of anuran assemblages from an Amazonian Amapá (UNIFAP) and Christopher Jaster (PARNA Montanhas savanna. ZooKeys 843: 149–169. do Tumucumaque) for logistical support during the fieldwork. 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Appendix. Voucher specimens collected at the Cancão Municipal Natural Park, municipality of Serra do Navio, Amapá state, Brazil and deposited at the Herpetological Collection of Laboratório de Herpetologia from Universidade Federal do Amapá.

Squamata (Lizards) - Hemidactylus mabouia CECC 2448; Thecadactylus rapicauda CECC 3221; Chatogekko amazonicus CECC 3253; Gonatodes humeralis CECC 2449; Lepidoblepharis heyerorum CECC 2940; Copeoglossum nigropunctatum CECC 2967; Dactyloa punctata CECC 2450; Norops auratus CECC 3222; Norops chrysolepis CECC 2952; Norops fuscoauratus CECC 3446; Norops ortonii CECC 2451; Iguana iguana iguana CECC 2452; Polychrus marmoratus CECC 2453; Plica plica CECC 3220; Plica umbra umbra CECC 3511; Uracentron azureum azureum CECC 2454; Uranoscodon superciliosus CECC 3490; Alopoglossus angulatus CECC 2455; Iphisa elegans elegans CECC 2456; Cercosaura aff. argulus CECC 3480; Cercosaura ocellata ocellata CECC 2457; Neusticurus bicarinatus CECC 3321; Neusticurus rudis CECC 2472; Arthrosaura kockii CECC 2458; Loxopholis guianense CECC 3314; Ameiva ameiva ameiva CECC 2459; Cnemidophorus cryptus CECC 2473; Kentropyx calcarata CECC 2474; Kentropyx striata CECC 2475; Tupinanbis teguixin CECC 3444. Squamata (Snakes) - Typhlophis squamosus CECC 2476; Anilius scytale CECC; Boa constrictor constrictor CECC 2477; Corallus hortulanus CECC 3295; Chironius exoletus CECC 2478; Chironius scurrulus CECC 2479; Dendrophidion dendrophis CECC 2480; Leptophis ahaetulla ahaetulla CECC 3297; Oxybelis fulgidus CECC 2481; Dipsas catesbyi CECC 2482; Apostolepis quinquelineata CECC 2483; Helicops angulatus CECC 1881; Philodryas argentea CECC 2484; Oxyrhopus melanogenys melanogenys CECC 2485; Pseudoboa coronata CECC; Siphlophis compressus CECC 2486; Erythrolamprus miliaris miliaris CECC 2487; Micrurus lemniscatus lemniscatus CECC 2488 Bothrops atrox CECC 3299.

Accepted by Fábio Hepp