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Corresponding author: Arielson S. Protázio ( neu_ptz@hotmail.com ) Academic editor: Uri García-Vázquez
© 2021 Arielson S. Protázio, Airan S. Protázio, Larissa S. Silva, Lennise C. Conceição, Hugo S. N. Braga, Uilton G. Santos, André C. Ribeiro, Amanda C. Almeida, Vívian Gama, Marcos V. S. A. Vieira, Tiago A. F. Silva.
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:
Protázio AS, Protázio AS, Silva LS, Conceição LC, Braga HSN, Santos UG, Ribeiro AC, Almeida AC, Gama V, Vieira MVSA, Silva TAF (2021) Amphibians and reptiles of the Atlantic Forest in Recôncavo Baiano, east Brazil: Cruz das Almas municipality. ZooKeys 1060: 125-153. https://doi.org/10.3897/zookeys.1060.62982
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A list of amphibian and reptile species that occur in open and forested areas of the Atlantic Forest in the municipality of Cruz das Almas, in the Recôncavo Baiano, eastern Brazil is presented. Field sampling occurred between January 2015 to March 2019, totalling 117 samples distributed in three areas: Parque Florestal Mata de Cazuzinha, Mata da Cascalheira, and Riacho do Machado. A total of 1,848 individuals of 69 species (31 anurans, 14 lizards, 19 snakes, two amphisbaenians, and three testudines) was recorded. Additionally, one individual of Ophiodes striatus was found in Mata da Cascalheira after the end of sampling, totalling 15 lizard species and 70 herpetofaunal species. The prevalence of open-area species and the presence of Phyllopezus lutzae, Diploglossus lessonae, and Dryadosaura nordestina in interior forest patches are discussed. Additionally, a new record of the invasive terrapin Trachemys dorbigni in the State of Bahia is reported.
Amphisbaena, anuran, diversity, lizards, species richness, snakes, testudines
The Atlantic Forest is a biome that occupies the entire east of South America and of Brazil and is considered one of the most diverse in species richness and levels of endemism (
Despite its high richness, Brazil is also a country with high levels of threat to biodiversity. According to the Brazil Red Book of Threatened Species of Fauna (
The State of Bahia is a state with great richness of herpetofauna species (
The Recôncavo Baiano is a region located in the eastern portion of the State of Bahia, corresponding to the portion of land that lies around Todos os Santos Bay (
Although a large part of the Recôncavo Baiano is located in the Atlantic Forest, studies characterising the herpetofauna of this region have been conducted almost exclusively in Serra da Jibóia and Serra do Timbó, which represent a set of mountains (elevational range 660–900 m above sea level, respectively) disjoined in the eastern portion of Serra do Espinhaço, in transition with the Caatinga (
This panorama reinforces the appeal for increased studies in forested and open areas of eastern Bahia to improve the characterisation of the richness and species composition of the herpetofauna of this portion of the Atlantic Forest. This information is essential to identify and monitor population fluctuations, enabling an accurate diagnosis of the ecosystem’s integrity and allowing access to the mechanisms that are involved in generating the region’s fauna diversity. In this study, we present a list of amphibian and reptile species that occur in open and forested areas of the municipality of Cruz das Almas, as part of a long-term project that seeks to characterise the herpetofauna of all the municipalities that are part of the Recôncavo Baiano, to minimise differences in the sample efforts along the different regions of the Atlantic Forest and to fill the information gaps regarding the state fauna.
The study was conducted in Cruz das Almas municipality, Bahia State, in northeast Brazil (12°40'25"S, 39°06'05"W) (Figure
Field activities were concentrated in three areas of the municipality that presented good conservation status and potential for finding herpetofauna specimens (Figure
Habitats sampled during the field works A view of Mata de Cazuzinha showing tall trees and shrubs B inside the Mata de Cazuzinha C temporary pond in Mata da Cascalheira D lagoon in Mata da Cascalheira E temporary pond in the Riacho do Machado F pitfall trap in the interior of the forest at Riacho do Machado.
(i) Parque Florestal Mata de Cazuzinha (12°39'58"S, 39°06'25"W; elevation 235 m): This is a forest fragment of ca. 20 ha, inserted in an urban matrix. It is considered an area of secondary vegetation, but presents a homogeneous and dense aspect, with predominance of arboreal vegetation of medium and large size. There is no evidence of permanent waterbodies inside the Cazuzinha forest, yet it has a forest structure that enables moisture concentration. Because it is located in an urban environment, the Cazuzinha forest suffers great anthropic pressure associated with hunting, wood removal and waste deposit. The area is intensely frequented by the local population for leisure activities.
(ii) Riacho do Machado (12°40'35.89"S, 39°25'59"W; elevation 226 m): The largest forest patch fragment in Cruz das Almas municipality. It is located between the experimental area of the Empresa Brasileira de Pesquisas Agropecuárias (Brazilian Agricultural Research Corporation) and the campus of the Federal University of Recôncavo da Bahia. This area is inserted in a hillside region and has medium-sized trees. It has a central lake ca. 5 m deep and a stream that names the patch. The homogeneous aspect of the vegetation indicates that the area has not been much accessed for wood removal, probably due to the difficulty of access. Nevertheless, during this study, some actions of burning, cutting and timber extraction were witnessed. Inside the forest, there are regions of “swamps”, which are propitious environments for the reproduction of anurans, as well as regions with rocky outcrops.
(iii) Mata da Cascalheira (12°39'29"S, 39°04'48"W; elevation 212 m): Cascalheira forest patch is an area of secondary forest, with predominance of shrubby vegetation and grasses. The forest patch is inserted in a region of hillsides and has a lagoon in the central region, which is ca. 4 m deep and contains large amounts of cattail and macrophytes. Mata da Cascalheira is inserted in the campus of the Federal University of Recôncavo da Bahia, which is a benchmark in agricultural studies. Thus, much of the patch has already been used as pastureland or arable land, with the formation of small puddles during rain events. In addition, it is possible to find some houses near the forest patch, where the residents engage in subsistence farming activity. Some areas of the Mata da Cascalheira were used for the extraction of land and stones for construction.
We conducted the field activities from January 2015 to Mach 2019, through non-standard day and night collections in the three different areas, totalling 117 samples. All daytime collections started at 8 am and ended at 5 pm, while night-time collections started at 6 pm and ended at midnight. The collections were performed by at least three and at most eight researchers. To collect the specimens, we used the techniques of visual encountering through random search inside and around the patches, aided by shot guns, and the places investigated were holes, burrows, tree trunks, fallen trunks, the interior of bromeliads, rocks, and all microhabitats conducive to the encounter of individuals in shelter or in activity (Figure
All animals collected were euthanised via intraperitoneal injection of 2% lidocaine, fixed in 10% formaldehyde, preserved in 70% alcohol, and deposited in the Herpetological Collection of the Universidade Federal do Recôncavo da Bahia (Sisbio Permit 46558-1 and 46558-2; CEUA-UFRB Permit 23007.007559/2016-71). The animals collected had a small fragment of the liver extracted to create a genetic database of the herpetofauna of the Recôncavo Baiano region, providing support for future studies.
To evaluate the quality of our sampling effort, we used the data of species richness and abundance of individuals to produce rarefaction curves (1,000 randomisations), using the ESTIMATES 9.1.0 program (
Finally, we compared the similarity of the species composition of the amphibian and reptiles of Cruz das Almas with the species composition of other assemblages of the Brazilian Atlantic Forest. We performed an analysis considering only anurans, lizards, and snakes. Data on the composition of anurans from other assemblages were obtained from 32 studies, while data on the composition of lizards and snakes were obtained from 21 studies. For this, we subdivided the Atlantic Forest into four biogeographic sub-regions, based on
We recorded a total of 1,848 individuals, distributed in 69 species of amphibians and reptiles (31 anurans, 14 lizards, 19 snakes, two amphisbaenians, and three testudines). Additionally, in December 2020, after the end sampling, we found an individual of Ophiodes striatus in Mata da Cascalheira, adding a lizard species to the list, totalling 15 lizard species and 70 herpetofauna species. The anurans identified belong to the families Bufonidae (3 spp.), Craugastoridae (1 sp.), Hylidae (13 spp.), Leptodactylidae (11 spp.), Microhylidae (1 sp.) and Phyllomedusidae (2 spp.) (Table
Check list of amphibians identified at Cruz das Almas municipality, Bahia State.
Taxon | Species | Abundance |
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Anura | ||
Bufonidae | Rhinella crucifer (Wied-Neuwied, 1821) | 2 |
Rhinella granulosa (Spix, 1824) | 24 | |
Rhinella jimi (Stevaux, 2002) | 54 | |
Craugastoridae | Pristimantis paulodutrai (Bokermann, 1975) | 118 |
Hylidae | Boana albomarginata (Spix, 1824) | 107 |
Boana crepitans (Wied-Neuwied, 1824) | 29 | |
Boana faber (Wied-Neuwied, 1821) | 5 | |
Dendropsophus elegans (Wied-Neuwied, 1824) | 229 | |
Dendropsophus branneri (Cochran, 1948) | 84 | |
Dendropsophus minutus (Peters, 1872) | 7 | |
Dendropsophus novaisi (Bokermann, 1968) | 11 | |
Dendropsophus oliveirai (Bokermann, 1963) | 63 | |
Scinax auratus (Wied-Neuwied, 1821) | 46 | |
Scinax eurydice (Bokermann, 1968) | 23 | |
Scinax pachycrus (Miranda-Ribeiro, 1937) | 3 | |
Scinax x-signatus (Spix, 1824) | 60 | |
Trachycephalus atlas Bokermann, 1966 | 2 | |
Leptodactylidae | Leptodactylus fuscus (Schneider, 1799) | 38 |
Leptodactylus macrosternum Miranda-Ribeiro, 1926 | 100 | |
Leptodactylus mystaceus (Spix, 1824) | 16 | |
Leptodactylus natalensis Lutz, 1930 | 24 | |
Leptodactylus vastus Lutz, 1930 | 24 | |
Leptodactylus troglodytes Lutz, 1926 | 54 | |
Physalaemus albifrons (Spix, 1824) | 1 | |
Physalaemus cuvieri Fitzinger, 1826 | 106 | |
Physalaemus kroyeri (Reinhardt & Lütken, 1862) | 95 | |
Pseudopaludicola cf. mystacalis (Cope, 1887) | 1 | |
Pseudopaludicola florencei Andrade, Haga, Lyra, Leite, Kwet, Haddad, Toledo & Giaretta, 2018 | 16 | |
Microhylidae | Dermatonotus muelleri (Boettger, 1885) | 10 |
Phyllomedusidae | Phyllomedusa bahiana Lutz, 1925 | 13 |
Pithecopus nordestinus (Caramaschi, 2006) | 30 |
Check list of reptiles identified at Cruz das Almas municipality, Bahia State.
Taxon | Species | Abundance |
---|---|---|
Squamata | ||
Amphisbaenidae | Amphisbaena alba Linnaeus, 1758 | 14 |
Amphisbaena vermicularis Wagler, 1824 | 5 | |
Lizards | ||
Dactyloidae | Norops fuscoauratus (D’Orbigny, 1837) | 9 |
Diploglossidae | Diploglossus lessonae Peracca, 1890 | 2 |
Ophiodes striatus (Spix, 1824) | 1 | |
Gekkonidae | Hemidactylus mabouia (Moreau de Jonnès, 1818) | 144 |
Phyllopezus lutzae (Loveridge, 1941) | 11 | |
Phyllopezus pollicaris (Spix, 1825) | 50 | |
Gymnophthalmidae | Dryadosaura nordestina Rodrigues, Freire, Pellegrino & Sites, 2005 | 1 |
Iguanidae | Iguana iguana (Linnaeus, 1758) | 1 |
Mabuyidae | Brasiliscincus heathi (Schmidt & Inger, 1951) | 5 |
Psychosaura macrorhyncha (Hoge, 1946) | 2 | |
Polychrotidae | Polychrus acutirostris Spix, 1825 | 3 |
Sphaerodactylidae | Coleodactylus meridionalis (Boulenger, 1888) | 19 |
Teiidae | Ameiva ameiva (Linnaeus, 1758 | 35 |
Salvator merianae Duméril & Bibron, 1839 | 4 | |
Tropiduridae | Tropidurus hispidus (Spix, 1825) | 72 |
Snakes | ||
Boidae | Boa constrictor Linnaeus, 1758 | 4 |
Epicrates assisi Machado, 1945 | 5 | |
Colubridae | Chironius carinatus (Linnaeus, 1758) | 1 |
Erythrolamprus miliaris (Linnaeus, 1758) | 1 | |
Erythrolamprus reginae (Linnaeus, 1758) | 3 | |
Leptodeira annulata (Linnaeus, 1758) | 1 | |
Tantilla melanocephala (Linnaeus, 1758) | 2 | |
Dipsadidae | Dipsas neuwiedi (Ihering, 1911) | 3 |
Helicops leopardinus (Schlegel, 1837) | 1 | |
Pseudoboa nigra (Duméril, Bibron & Duméril, 1854) | 5 | |
Oxyrhopus petolarius (Linnaeus, 1758) | 1 | |
Oxyrhopus trigeminus Duméril, Bibron & Duméril, 1854 | 6 | |
Philodryas olfersii (Lichtenstein, 1823) | 7 | |
Philodryas patagoniensis (Girard, 1858) | 1 | |
Thamnodynastes pallidus (Linnaeus, 1758) | 3 | |
Xenodon merremii (Wagler, 1824) | 3 | |
Elapidae | Micrurus ibiboboca (Merrem, 1820) | 17 |
Typhlopidae | Amerotyphlops brongersmianus (Vanzolini, 1976) | 3 |
Viperidae | Bothrops leucurus Wagler, 1824 | 6 |
Testudines | ||
Chelidae | Phrynops geoffroanus (Schweigger, 1812) | 1 |
Emydidae | Trachemys dorbigni (Duméril & Bibron, 1835) | 1 |
Testudinidae | Chelonoidis carbonarius (Spix, 1824) | 1 |
Anuran species identified at Cruz das Almas municipality, Bahia State A Rhinella crucifer B Rhinella granulosa C Rhinella jimi D Pristimantis paulodutrai E Boana albomarginata F Boana crepitans G Boana faber H Dendropsophus branneri I Dendropsophus elegans J Dendropsophus minutus K Dendropsophus novaisi L Dendropsophus oliveirai M Scinax auratus N Scinax eurydice OScinax pachycrus.
Anuran species identified at Cruz das Almas municipality, Bahia State A Scinax x-signatus B Trachycephalus atlas C Phyllomedusa bahiana D Pithecopus nordestinus E Leptodactylus macrosternum F Leptodactylus fuscus G Leptodactylus mystaceus H Leptodactylus natalensis I Leptodactylus troglodytes J Leptodactylus vastus K Physalaemus albifrons L Physalaemus cuvieri M Physalaemus kroyeri N Pseudopaludicola florencei O Dermatonotus muelleri.
Reptile species identified at Cruz das Almas municipality, Bahia State A Norops fuscoauratus B Diploglossus lessonae C Hemidactylus mabouia D Phyllopezus lutzae E Phyllopezus pollicaris F Dryadosaura nordestina G Iguana iguana H Brasiliscincus heathi I Psychosaura macrorhyncha J Polychrus acutirostris K Coleodactylus meridionalis L Ameiva ameiva M Tropidurus hispidus N Amphisbaena alba O Amphisbaena vermicularis.
Reptile species identified at Cruz das Almas municipality, Bahia State A Boa constrictor B Epicrates assisi C Chironius carinatus D Erytrolamprus miliaris E Erytrolamprus reginae (juvenile) F Leptodeira annulata G Tantilla melanocephala H Dipsas neuwiedi I Pseudoboa nigra (juvenile) J Pseudoboa nigra (adult) K Oxyrhopus petolarius L Oxyrhopus trigeminus M Philodryas olfersii N Philodryas patagoniensis O Thamnodynastes pallidus.
The rarefaction curve approached the asymptote only for amphibians, demonstrating that the sample effort managed to obtain a satisfactory representation of species (Figure
Mean and standard deviation of the species richness estimated with different estimators in Cruz das Almas municipality. Herpetofauna represent the combination of amphibians, lizards, snakes, amphisbaenians, and testudines.
Amphibians | Lizards | Snakes | Herpetofauna | |
Observed richness | 31 | 15 | 19 | 70 |
Bootstrap | 32 ± 0 | 16 ± 0 | 22 ± 0 | 77 ± 0 |
Chao 2 | 31 ± 0.62 | 16 ± 1.79 | 26 ± 8.06 | 81 ± 8.05 |
Jackknife 1 | 33 ± 1.39 | 18 ± 1.68 | 25 ± 2.32 | 84 ± 3.58 |
Jackknife 2 | 31 ± 0 | 19 ± 0 | 30 ± 0 | 91 ± 0 |
Singletons | 2 | 3 | 6 | 14 |
The cluster analysis revealed that the assemblages of anurans, lizards, and snakes from Cruz das Almas formed close groups with those assemblages from northeast Brazil, specifically from north and south of the São Francisco River. This result indicates that there is a faunal similarity between assemblages inserted in the Central Corridor of the Atlantic Forest and the Pernambuco Endemism Centre (Figures
The anuran species richness identified in Cruz das Almas corresponds to 5% of the anuran richness currently known for the Atlantic Forest (
According to
None of the anuran species found in our study revealed an unusual or unexpected record for the region, having been previously reported for the State of Bahia and the Atlantic Forest (
The Cruz das Almas assemblage presented a low number of typical species from forested areas and prevalence of typical species from open land. This result explains the greater similarity of the Cruz das Almas assemblage with other assemblage from open land and Atlantic Forest-Caatinga ecotones observed in our cluster analysis. Anthropic actions may have shaped the current pattern of the Cruz das Almas assemblage, leading to the reduction of species more specialised to forest habitats. This scenario reveals the need for greater efforts to preserve the remaining forest fragments in the region. Nevertheless, Pristimantis paulodutrai was the dominant species in the interior of forest fragments in Mata de Cazuzinha, often found vocalising perched on herbaceous vegetation. Besides P. paulodutrai, only Rhinella jimi, Leptodactylus troglodytes, Physalaemus cuvieri, and Physalaemus kroyeri were also identified in the Mata de Cazuzinha, but only on the edge, where they used waterbodies formed after the rains. We believe that P. paulodutrai’s dominance of the urban forest fragment is due to the absence of waterbodies inside the fragment, which may have limited the permanence of other species.
The reptile species richness of the Cruz das Almas assemblage corresponds to 12.5% of the known reptile richness for the Atlantic Forest (
For the lizards, our results revealed the presence of species previously recorded for Bahia State and the Atlantic Forest (
Analysis of the species composition revealed two endemic species of the Atlantic Forest (Phyllopezus lutzae and Dryadosaura nordestina), which corresponds to 14.9% of the lizard fauna recorded in the study (
The lizard Diploglossus lessonae can be found in areas of Atlantic Forest and Caatinga in northeast Brazil (
For snakes, none of the species found in our study represents a new finding, as they are species that were previously registered in the State of Bahia and for the Atlantic Forest (
We believe that the difference in snake species richness between the assemblages of the Bahia State may be more associated with the sample design involved in the data collection than necessarily with a biological effect arising from the locality and study area.
Although we found a species richness similar to that presented by
Finally, in this study, we report a new record of the water tiger Trachemys dorbigni for the Bahia State. The species is distributed throughout southern South America, in the countries of Argentina, Uruguay and Brazil, especially in the States of Rio Grande do Sul and Santa Catarina (
The two amphisbaenian species identified in our study are common and frequently recorded in the Atlantic Forest inventories from the Brazilian northeast (
We thank Joanna K. G. Oliveira, Diego S. Macedo, Ubiraci R. Carmo Júnior, and Lucas S. Nascimento for their valuable contributions in field work. We thank the ICMbio for collection license. We thank Daniel O. Mesquita and an anonymous reviewer for comments and suggestions that improved this article.