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Corresponding author: Carlos Eduardo Costa-Campos ( eduardocampos@unifap.br ) Academic editor: Angelica Crottini
© 2018 Yuri Breno Silva e Silva, Carlos Eduardo Costa-Campos.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Silva e Silva YB, Costa-Campos CE (2018) Anuran species composition of Cancão Municipal Natural Park, Municipality of Serra do Navio, Amapá state, Brazil. ZooKeys 762: 131-148. https://doi.org/10.3897/zookeys.762.22634
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In this study, the first survey of anuran species in the Cancão Municipal Natural Park is presented, a protected area of approximately 370 hectares of Amazonian forest located in the northwest center region of the state of Amapá, Brazil. The work was performed during the dry and rainy season, through active visual and auditory survey, totaling 216 man hours of sampling effort. Forty-nine species of anuran amphibians were recorded in the Cancão Municipal Natural Park, including three new records: Hyalinobatrachium iaspidiense, Pristimantis cf. ockendeni, and Scinax garbei. Three species, Hyalinobatrachium iaspidiense, Ameerega pulchripecta, and Anomaloglossus baeobatrachus, are listed as Data Deficient and one is listed as Vulnerable (Atelopus hoogmoedi) according red lists of IUCN. The rarefaction curve cumulative species did not reach an asymptote, indicating that site has potential for species that have not yet been recorded. Nine species were represented by only one individual and were considered rare in the studied environments, eight species were defined as common, and the 32 remaining species were classified as having intermediary abundance. Our data indicated that Cancão Municipal Natural Park contains a considerable portion of the anurans species richness of Amapá state, turn the area into a place of great importance for the conservation of the anurans of the Eastern Amazon.
Amazonia, conservation, eastern Amazon, species list
Most of the currently documented amphibian species in Brazil have been discovered during the last forty years (
This amphibian species richness can be considered underestimated in number and complexity when considering enormous areas of Brazil which have yet to be inventoried, and there are many localities were surveys have been insufficient (
Due to difficult to access, many Amazonian areas are still poorly known regarding their amphibian fauna and with insufficient sampling (
In the Amazonian biome, studies on anurans are concentrated in states of Amazonas, Pará, Rondônia and Acre, other localities in the Brazilian Amazon lack inventories (
Study area. Fieldwork was conducted at the Cancão Municipal Natural Park (Figure
Sampling. Animals were registered during diurnal and nocturnal active visual search and auditory census in different microhabitats used by frogs (
The specimens were collected under permit SISBIO number 32651-1 issued by the Brazilian Ministry of Environment (MMA-ICMBio). Voucher adults collected were deposited at the Coleção Herpetológica da Universidade Federal do Amapá (UNIFAP) and Coleção Herpetológica do Museu Paraense Emílio Goeldi “Osvaldo Rodrigues da Cunha” (MPEG). The conservation status quoted follows
Data analysis. To analyze the anurans species richness, rarefaction curves of species were constructed based on the number of individuals and number of samples (
The dominances were represented by Whittaker Diagram, obtained by ranking species, starting with the most abundant, along the x-axis and the logarithm abundances on the y-axis. Rare species were those represented by a single individual (singletons). The other species were classified as having intermediate abundance. The pattern of the species abundance distribution was fitted to the geometric, logarithmic, log-normal, and broken-stick models. Model fit was assessed by the chi square adherence test (
The Spearman correlation coefficient analysis was performed to compare climatic conditions (available from the NHMET database) during the sampling period with abundance. To check the influence of environmental data on amphibian abundance, multiple regression analyses were conducted, including data on rainfall, temperature, and humidity as independent variables. The normality of the data was tested with the KOLMOGOROV-SMIRNOV analysis (
Forty-nine anuran species have been recorded in the Cancão Municipal Natural Park (Table
Species recorded in the Cancão Municipal Natural Park, municipality of Serra do Navio, Amapá state: 1 Allophryne ruthveni 2 Allobates femoralis 3 Anomaloglossus baeobatrachus 4 Atelopus hoogmoedi 5 Rhaebo guttatus 6 Rhinella margaritifera complex 7 R. marina 8 R. martyi 9 Hyalinobatrachium iaspidiense 10 Pristimantis chiastonotus 11 P. marmoratus 12P. cf. ockendeni13 P. zeuctotylus 14 P. zimmermanae 15 Ameerega pulchripecta 16 Dendrobates tinctorius 17 Adelophryne gutturosa 18 Boana boans 19 B. calcarata 20 B. cinerascens 21 B. dentei 22 B. fasciata 23 B. geographica 24 B. multifasciata.
Continued. 25 Dendropsophus counani 26 D. leucophyllatus 27Dendropsophus cf. microcephalus28 D. minutus 29 Osteocephalus oophagus 30 O. taurinus 31 Scinax boesemani 32 S. garbei 33 S. nebulosus 34 S. ruber 35 Adenomera andreae 36 A. hylaedactyla 37 Leptodactylus knudseni 38 L. lineatus 39 L. longirostris 40 L. mystaceus 41 L. pentadactylus 42 L. petersii 43 L. rhodomystax 44 L. stenodema 45 Phyllomedusa bicolor 46 P. vaillantii 47 Pithecopus hypochondrialis, and 48 Pipa pipa.
List of amphibian species recorded at Cancão Municipal Natural Park, municipality of Serra do Navio, Amapá State. Sampled areas: Terra firme trail at Cancão forest (TC), Amapari trail (TA), treefall gap at stream Cancão (TS), and treefall gap at Cancão forest (TF). Red List species included in some category of
Family/Species | Sampled areas | IUCN | |||
---|---|---|---|---|---|
TC | TA | TS | TF | ||
Allophrynidae | |||||
Allophryne ruthveni Gaige, 1926 | X | LC | |||
Aromobatidae (Allobatinae) | |||||
Allobates femoralis (Boulenger, 1884) | X | X | LC | ||
Aromobatidae (Aromobatinae) | |||||
Anomaloglossus baeobatrachus (Boistel & de Massari, 1999) | X | DD | |||
Bufonidae | |||||
Atelopus hoogmoedi Lescure, 1974 | X | VU | |||
Rhaebo guttatus (Schneider, 1799) | X | X | LC | ||
Rhinella margaritifera complex of species | X | X | X | X | LC |
Rhinella marina (Linnaeus, 1758) | X | X | X | X | LC |
Rhinella martyi Fouquet, Gaucher, Blanc & Vélez-Rodriguez, 2007 | X | LC | |||
Centrolenidae (Hyalinobatrachinae) | |||||
Hyalinobatrachium iaspidiense (Ayarzaqüena, 1992) * | X | DD | |||
Craugastoridae (Ceuthomantinae) | |||||
Pristimantis chiastonotus (Lynch & Hoogmoed, 1977) | X | X | X | LC | |
Pristimantis marmoratus (Boulenger, 1900) | X | LC | |||
Pristimantis cf. ockendeni (Boulenger, 1912) * | X | X | X | LC | |
Pristimantis zeuctotylus (Lynch & Hoogmoed, 1977) | X | LC | |||
Pristimantis zimmermanae (Heyer & Hardy, 1991) | X | LC | |||
Dendrobatidae (Colostethinae) | |||||
Ameerega pulchripecta (Silverstone, 1976) ** | X | X | DD | ||
Dendrobatidae (Dendrobatinae) | |||||
Dendrobates tinctorius (Cuvier, 1797) | X | LC | |||
Eleutherodactylidae | |||||
Adelophryne gutturosa Hoogmoed & Lescure, 1984 | X | LC | |||
Hylidae | |||||
Boana boans (Linnaeus, 1758) | X | X | X | X | LC |
Boana calcarata (Troschel in Schomburgk 1848) | X | LC | |||
Boana cinerascens (Spix, 1824) | X | X | X | LC | |
Boana dentei (Bokermann, 1967) ** | X | LC | |||
Boana fasciata (Günther, 1859 “1858”) | X | X | LC | ||
Boana geographica (Spix, 1824) | X | LC | |||
Boana multifasciata (Günther, 1859 “1858”) | X | X | X | LC | |
Dendropsophus counani Fouquet, Souza, Nunes, Kok, Curcio, de Carvalho, Grant & Rodrigues, 2015 | X | X | – | ||
Dendropsophus leucophyllatus (Beireis, 1783) | X | LC | |||
Dendropsophus cf. microcephalus (Cope, 1886) | X | LC | |||
Dendropsophus minutus (Peters, 1872) | X | LC | |||
Osteocephalus oophagus Jungfer & Schiesari, 1995 | X | LC | |||
Osteocephalus taurinus Steindachner, 1862 | X | X | LC | ||
Scinax boesemani (Goin, 1966) | X | X | LC | ||
Scinax garbei (Miranda-Ribeiro, 1926) * | X | LC | |||
Scinax nebulosus (Spix, 1824) | X | X | LC | ||
Scinax ruber (Laurenti, 1768) | X | X | X | X | LC |
Trachycephalus resinifictrix (Goeldi, 1907) | X | X | LC | ||
Leptodactylidae (Leptodactylinae) | |||||
Adenomera andreae (Müller, 1923) | X | X | X | X | LC |
Adenomera hylaedactyla (Cope, 1868) | X | X | X | X | LC |
Leptodactylus knudseni Heyer, 1972 | X | LC | |||
Leptodactylus lineatus (Schneider, 1799) | X | LC | |||
Leptodactylus longirostris Boulenger, 1882 | X | X | X | LC | |
Leptodactylus mystaceus (Spix, 1824) | X | X | X | X | LC |
Leptodactylus pentadactylus (Laurenti, 1768) | X | LC | |||
Leptodactylus petersii (Steindachner, 1864) | X | LC | |||
Leptodactylus rhodomystax Boulenger, 1884 “1883” | X | LC | |||
Leptodactylus stenodema Jiménez de la Espada, 1875 | X | LC | |||
Phyllomedusidae | |||||
Phyllomedusa bicolor (Boddaert, 1772) | X | LC | |||
Phyllomedusa vaillantii Boulenger, 1882 | X | X | LC | ||
Pithecopus hypochondrialis (Daudin, 1800) | X | X | X | LC | |
Pipidae | |||||
Pipa pipa (Linnaeus, 1758) | X | LC |
Three new records of anurans are presented for the Cancão Municipal Natural Park, namely Hyalinobatrachium iaspidiense (Centrolenidae), Pristimantis cf. ockendeni (Craugastoridae), and Scinax garbei (Hylidae). None of the frog species recorded at the Cancão Municipal Natural Park is classified as threatened in the red lists of
Hyalinobatrachium iaspidiense is known from Brazil, Ecuador, French Guiana, Guyana, Peru, Suriname, Venezuela, and is expected to occur in the Amazonian areas between the Ecuadorian and Peruvian localities and the Guiana region (
Pristimantis cf. ockendeni is distributed throughout the Amazonian basin of Peru, Ecuador, southern Colombia, and Brazil in the states of Acre and Amazonas (
Scinax garbei is known from Ecuador, adjacent Peru, Bolivia, Colombia, and Venezuela (
The frog species richness estimated for the area by Bootstrap and Jack-knife was 54 and 63 species, respectively, and the rarefaction curve cumulative species did not reach an asymptote. We believe that site has potential for species that have not yet been recorded (Figure
Spearman correlations obtained with the studied period were not significant for rainfall data (R = 0.564, P = 0.056), temperature (R = 0.467, P = 0.167) and relative humidity (R = 0.267, P = 0.877). According to multiple regressions, amphibian abundance does not seem to be related to any of the abiotic factors considered (F3, 8 = 1.240; P = 0.179; r = 0.563 for the entire analysis; F3, 8 = 3.422; P = 0.091 for rainfall; F3, 8 = 1.097; P = 0.320 for temperature; and F3, 8 = 0.720; P = 0.579 for relative humidity (Figure
Correlation of recorded anuran abundance and abiotic factors in Cancão Municipal Natural Park, municipality of Serra do Navio Amapá state, from January through December 2013. A Anuran abundance (black bars) and rainfall (grey squares and line) B anuran abundance (black bars) and temperature (grey squares and line) C anuran abundance (black bars) and relative humidity (grey squares and line).
Nine species (Allophryne ruthveni, Rhinella martyi, Pristimantis zimmermanae, Boana calcarata, B. dentei, Osteocephalus oophagus, Scinax garbei, Leptodactylus lineatus and Pipa pipa) were represented by only one individual and were considered rare in the studied environments. Applying the number of singletons to the other end of the abundance distribution, eight species were defined as common, including P. chiastonotus (157 individuals), B. multifasciata (123 individuals), R. margaritifera complex (123 individuals), and B. boans (105 individuals). The 32 remaining species were classified as having intermediary abundance (Figure
The dendrogram obtained from cluster analysis evidences three major groups: (A) sites located in the treefall gaps, (B) sites in the Terra firme forest, and (C) sites belonging to the Amapari River with temporary ponds. The group (A) is characterized by the higher Boana multifasciata, B. cinerascens and Pithecopus hypochondrialis, species occurring in open areas. For the group (B), the most frequent species were Rhinella margaritifera complex species and Pristimantis chiastonotus. The last group, (C), is characterized by the high frequency of occurrence of Allobates femoralis and Adenomera andreae. The coefficient of cophenetic correlation for the cluster analysis was 0.997 (Figure
Dendrogram for cluster analysis (UPGMA) using the Jaccard’s Similarity Index between the anurans of the Cancão Municipal Natural Park. Cophenetic correlation coefficient = 0.997. Sampled areas: Group A Treefall gap at stream Cancão (TS) and Treefall gap at Cancão forest (TF); Group B Terra firme trail at Cancão forest (TC); Group C Amapari trail (TA).
Our data indicate that Cancão Municipal Natural Park contains a considerable portion of the anurans species richness of Amapá state. The anuran fauna corresponded to 65.7 % of the recorded species for the Tumucumaque Mountains National Park (
The results obtained from the rarefaction curve and the Jack-knife1 and Bootstrap estimators suggest that the species composition is still underestimated, and more long-term studies may reveal the presence of additional species in the area. Future studies should be complemented with combined and/or different approaches in fieldwork, such as the use of pitfall traps for leaf-litter species, increased visual search times (
The finding of a large number of species of the families Hylidae and Leptodactylidae was similar to the results of other studies and follows the pattern found in neotropical environments (
The record of Atelopus hoogmoedi and Ameerega pulchripecta in the area studied is relatively important. Atelopus hoogmoedi is a terrestrial and diurnal species, and is most commonly found at small streams in primary forest (
The cluster analysis of the anuran assemblages generated three groups. The group A and B showed a more differentiated assemblage. Group C are located on the right bank of the Amapari River, and presented high values of abundance and richness. The results can be attributed to the similar characteristics between the sites. The main hypotheses proposed to explain barrier formation separating populations and causing the differentiation of species in Amazonia during the course of geological history are based on different factors (
The results of the present study thus provide new data on geographic distribution of species showed three new records of the Brazilian Amazonian and important insights into the diversity of amphibians in the northern Brazil. The high amphibian richness recorded in this study for the eastern Amazon, combined with the presence of populations of Data Deficient or Vulnerable species, contributes to the knowledge on species, reinforcing the importance of the Cancão Municipal Natural Park for the conservation of anurans species.
We thank Jiří Moravec and the anonymous reviewers for their constructive comments, which helped us to improve the manuscript. We are also grateful to Albertina Lima, Antoine Fouquet, Marinus Hoogmoed, Tiago de Carvalho and Ulisses Caramaschi for collaborating in the identification of some species. We thank all those who helped on the fieldwork Bruna Lobo, Daniel Valentim, Hélio Pamphylio, Lígia Carvalho, Mayara Melo and Raimundo Baía. We thank Universidade Federal do Amapá (UNIFAP) and Christopher Jaster (PARNA Montanhas do Tumucumaque) for logistical support during the fieldwork and Instituto Chico Mendes de Conservação da Biodiversidade – ICMBio for collecting permit (# 32651-1).