Corresponding author: Leandro J.C.L. Moraes (
Academic editor: A. Herrel
The Brazilian mountain ranges from the Guiana Shield highlands are largely unexplored, with an understudied herpetofauna. Here the amphibian and reptile species diversity of the remote Serra da Mocidade mountain range, located in extreme northern Brazil, is reported upon, and biogeographical affinities and taxonomic highlights are discussed. A 22-days expedition to this mountain range was undertaken during which specimens were sampled at four distinct altitudinal levels (600, 960, 1,060 and 1,365 m above sea level) using six complementary methods. Specimens were identified through an integrated approach that considered morphological, bioacoustical, and molecular analyses. Fifty-one species (23 amphibians and 28 reptiles) were found, a comparable richness to other mountain ranges in the region. The recorded assemblage showed a mixed compositional influence from assemblages typical of other mountain ranges and lowland forest habitats in the region. Most of the taxa occupying the Serra da Mocidade mountain range are typical of the Guiana Shield or widely distributed in the Amazon. Extensions of known distribution ranges and candidate undescribed taxa are also recorded. This is the first herpetofaunal expedition that accessed the higher altitudinal levels of this mountain range, contributing to the basic knowledge of these groups in remote areas.
Moraes LJCL, Almeida
Scientific interest in mountain ranges arises primarily because they are characterized by a geographical isolation associated with differential availability of topographical, climatic, and edaphic conditions along the altitudinal gradients (
Initial discoveries concerning the amphibian and reptile diversity from Guiana Shield highlands were reported by localized expeditions at the transition between the nineteenth and twentieth centuries (
More recently, studies have shown that diversification and evolutionary patterns of distinct species were associated with the landscape history of the region (
Furthermore, most specimens currently collected during biological inventories are identified using morphological characteristics. However, given the pervasive occurrence of cryptic diversity (
Recently, a multidisciplinary initiative conducted an expedition (“Biodiversity of the Serra da Mocidade”) to inventory the biological diversity of distinct taxonomic groups in the poorly known region of the Serra da Mocidade, a remote granitic mountain range located in northern Brazil (
The Guiana Shield highlands region is located in northern South America, within the limits of Venezuela, Guyana, Suriname, and Brazil (Fig.
Study area. Location of
This study was conducted at Serra da Mocidade (Figs
Serra da Mocidade. Panoramic views of the Serra da Mocidade mountain range (
The lowland regional climate has low annual temperature variation, ranging from 24° C to 27° C (average 26° C), a rainy season from April to September and a dry season from October to March (
Logistic support from the Brazilian Army allowed aerial access at altitudes only accessible by helicopters, and the installation of two base camps from which it was possible to reach different altitudinal levels (Fig.
Surveys were conducted in two teams, each with three trained herpetologists, one from each base camp (first team at base camp #1 for 15 to 23 January 2016, and second team at base camp #2 for 25 January to 06 February 2016), totaling 22 days of field work and 66 man-days of sampling effort. To maximize characterization of the regional herpetofaunal diversity we used six complementary survey methods to detect individuals: (1) active surveys (
Specimens were killed with an injection of Thiopental® or Lidocaine, fixed with 10% formalin, and preserved in 70% ethanol. We removed muscle or liver tissue from specimens before the fixation process and stored it in absolute ethanol. Voucher specimens and tissue samples were deposited in the Collections of Amphibians and Reptiles (
Taxonomic identifications were performed using morphological, bioacoustical, and molecular analyses, following the taxonomic arrangements of
The specimens’ morphologies were analysed according to original descriptions, taxonomic and phylogenetic revisions, dichotomous keys, field guides and results from similar expeditions from Guiana Shield highlands (
The calls from some amphibian species were recorded in uncompressed wav format, with a Zoom H1 Handy Recorder (Zoom Corporations, Tokyo, Japan) equipped with an internal microphone, distant about 1–2 m to the emitter. The calls were digitised and analysed using Raven Pro. 1.5 (Cornell Laboratory of Ornithology) at a sampling frequency of 44 KHz and 16-bit resolution. Call structures were visually analysed in the spectrograms, and we measured the following quantitative parameters, considered in amphibian taxonomy (
When specimens were part of groups already considered as a complex of multiple species or when we considered the possibility of an undescribed taxon, we explored their taxonomic status using DNA sequences of mitochondrial gene 16S, a standard marker for amphibians and reptiles (
DNA sequences obtained were compared with those available for closely related taxa in GenBank (
In order to investigate the relationship between the recorded diversity and sampling effort, as well as to identify differences in species richness between altitudinal levels, we performed extrapolated rarefaction curves (
To identify biogeographical patterns and evaluate the contribution of adjacent regions to the composition of the local herpetofauna at Serra da Mocidade, we classified species according to their known geographical distribution, delimiting boundaries of biogeographic regions based on the main geological compartments for Northern South America (
To verify the contribution of altitudinal generalists and specialists to the species composition of the Serra da Mocidade herpetofauna, we also classified species according to their known altitudinal range as reported in the literature, as lowland (occuring mainly below 500 m asl) and upland (occuring mainly above 500 m asl) species (
A total of 305 specimens (232 amphibians, 58 squamates, 13 chelonians, and two crocodilians) was recorded, belonging to 51 species (23 amphibians, 24 squamates, three chelonians, and one crocodilian) from 25 families (Table
Recorded species. List of amphibians and reptiles recorded at the Serra da Mocidade mountain range, with respective sample sizes at each distinct altitudinal level (m above sea level), sampling methods, morphological data, and species’ geographical and altitudinal distributions. Sampling methods: (
Taxon | Altitude (m asl) | Sampling method | Morphological measurements (mm) | Geographic distribution | Altitudinal range | |||
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600 | 960 | 1,060 | 1,365 | |||||
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Amphibian diversity. Examples of amphibians recorded in the Serra da Mocidade mountain range.
Amphibian diversity. Examples of amphibians recorded in the Serra da Mocidade mountain range.
Lizard diversity. Examples of lizards recorded in the Serra da Mocidade mountain range.
Snake diversity. Examples of snakes recorded in the Serra da Mocidade mountain range.
Snake, chelonian and crocodilian diversity. Examples of snakes, chelonians and the crocodilian recorded in the Serra da Mocidade mountain range.
Habitat diversity. Examples of habitats sampled in the Serra da Mocidade mountain range.
Variation in species richness and composition.
The number of specimens recorded during sampling was similar in both camps (149 at base camp #1 vs. 158 at base camp #2), with some species exclusively recorded at distinct altitudinal levels, as with frogs of the genus
Altitudinal species variation. Altitudinal variation in species composition and relative abundance (width of the black bars) of amphibians and reptiles from our sampling at the Serra da Mocidade mountain range. Note that some species were exclusively recorded in a given altitudinal level while other are altitudinal generalists.
Advertisement calls were obtained for a few anuran species, and they were useful to assign or confirm species identification, such as
The species richness of Serra da Mocidade is comparable to that recorded for other mountain ranges in the Guiana Shield highlands region, which harbour a low number of species compared to Guiana Shield lowland forest habitats (Table
Species richness. Herpetofaunal richness variation at some mountain ranges in the Guiana Shield highlands (including data for all altitudinal levels) and at lowland habitats in the region (compiled results of inventories). Data are presented as raw species number/percentage of total herpetofauna and references are detailed in the text.
Mountain range | Amphibians | Reptiles | Total |
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Mocidade | 23/0.45 | 28/0.55 | 51 |
Apiaú | 23/0.48 | 25/0.52 | 48 |
Duida | 10/0.38 | 16/0.62 | 26 |
Marahuaka | 14/0.74 | 5/0.26 | 19 |
Auyantepui | 14/0.35 | 26/0.65 | 40 |
Chimantá | 8/0.42 | 11/0.58 | 19 |
Guaiquinima | 11/0.33 | 22/0.67 | 33 |
Neblina | 51/0.45 | 62/0.55 | 113 |
Los Testigos | 4/0.67 | 2/0.33 | 6 |
Lema | 31/0.53 | 28/0.47 | 59 |
Guanay | 4/0.57 | 3/0.43 | 7 |
Yaví | 3/0.50 | 3/0.50 | 6 |
Tamacuari | 7/0.64 | 4/0.36 | 11 |
Yutajé-Corocoro | 6/0.60 | 4/0.40 | 10 |
Roraima | 15/0.65 | 8/0.35 | 23 |
Sarisariñama | 16/0.44 | 20/0.56 | 36 |
Nassau, Lely | 32/0.59 | 22/0.41 | 54 |
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Forests | 72/0.42 | 100/0.58 | 172 |
Open habitats | 40/0.54 | 33/0.46 | 73 |
This same mixed influence is corroborated regarding biogeographical regions, as the composition of the amphibian assemblage was most strongly influenced by widely distributed Amazonian forest lineages (47%), but also included species restricted to, or typical for, the Guiana Shield (22%), Guiana Shield highlands (8%) and Eastern Amazonia (4%). The reptile assemblage composition showed a similar pattern, with most species widely distributed in Amazonia (75%) and smaller proportions of exclusive lineages from the Guiana Shield (7%), Guiana Shield highlands (7%), Eastern Amazonia (7%) and Western Amazonia (3.5%). Some of the taxa we collected are potentially endemic to the Serra da Mocidade mountain range, such as
Most of the amphibian species we recorded on Serra da Mocidade occur across wide altitudinal ranges along their geographical distribution (43%). Several species are typical from the Amazonian lowlands (35%), and some are typical of the uplands (22%). The reptilian assemblage showed a similar altitudinal pattern: most of the Serra da Mocidade species are generalists in terms of altitudinal range (53.5%) or lowland forms (43%), and few are typical of the uplands (3.5%). When we analysed the distinct assemblages recorded at 600 m asl and above 900 m asl, we found different distribution patterns at a finer scale: at 600 m asl, assemblages were mainly composed of lowland species (47% of amphibians and 52% of reptiles) and altitudinal generalists (42% of amphibians and 48% of reptiles). Above 900 m asl, no elements from lowland forests were recorded for either taxonomic group and assemblages were composed of upland species (33% of amphibians and 11% of reptiles) and altitudinal generalists (67% of amphibians and 89% of reptiles) (Fig.
Accounts of the remarkable species are provided below, with comments on ecology, taxonomy, morphology, evolutionary distinctiveness, and biogeography.
Phylogenetic relationships of caecilians. Maximum likelihood phylogenetic tree of caecilians families
Quantitative bioacoustical results. Summary of bioacoustical analyses of advertisement calls of some species recorded from the Serra da Mocidade mountain range, with literature data for comparison. Data are presented as mean, with associated amplitude (–) or standard deviation (±).
Species | Locality (References) | Call structure | Call duration (s) | Inter-call interval (s) | Pulse duration (s) | Pulse rate (pulses/s) | Dominant frequency (kHz) |
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Serra da Mocidade, RR, Brazil | Long trill | 19.07 (±4.89) | 15.76 (±4.12) | 0.039 (±0.002) | 8.4 (±0.67) | 4.109 (±0.148) |
|
Serra do Apiaú, RR, Brazil† | Long trill | 19.56 (±11.05) | 11.17 (±7.24) | 0.033 (±0.005) | 11.27 (±0.55) | 4.334 (±0.129) |
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Serra da Mocidade, RR, Brazil | Single note | 0.09 (0.04–0.18) | 13 (11.2–17.4) | - | - | 3.72 (2.1–4.5) |
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Different localities‡ | Single note | 0.11 (0.03–0.2) | 14.7 (11.1–18.3) | - | - | 3.75 (2.2–5.3) |
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Serra da Mocidade, RR, Brazil | Long train | 0.34 (0.18–0.51) | 1.51 (1.27–2.10) | - | - | 1.036 (0.9–1.1) |
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Different localities| | Long train | 0.42 (0.18–1.19) | 2.05 (0.57–4.7) | - | - | 0.648 (0.2–1.1) |
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Serra da Mocidade, RR, Brazil | Series of pulses | 0.302 (±0.026) | 0.61 (±0.18) | 0.015 (±0.004) | - | 1.237 (±0.03) |
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Guiana Shield lowlands§ | Series of pulses | 0.295 (±0.013) | - | 0.009 (±0.001) | - | 1.169 (±0.04) |
† Fouquet et al. 2015, ‡
The population of Serra da Mocidade had adult males with 15–20 mm
Bioacoustical data. Oscillograms (upper graphs) and sonograms (lower graphs) of advertisement calls of species recorded in the Serra da Mocidade mountain range.
Phylogenetic relationships of
This record of
Individuals of
Phylogenetic relationships of
The diversity of
Phylogenetic relationships of
Phylogenetic relationships of
Phylogenetic relationships of
Phylogenetic relationships of
Intraspecific analyses of molecular variation indicated a strong genetic structure and multiple lineages within this widely distributed Amazonian taxon (
There is a subtle morphological divergence between
Several remarkable herpetofaunal records were found during the first large biological expedition conducted at the Serra da Mocidade mountain range. Based on our results, it is evident that the herpetofauna inhabitant of this mountain range has a greater biotic affinity with lowlands from the Amazon region, but some elements typical of the uplands from Guiana Shield highlands region occurs above 900 m asl.
However, the local species diversity is certainly underestimated in our results, especially at higher altitudinal zones, as this mountain range has an extensive unexplored area of upland forests, which may harbour populations of undescribed amphibians and reptiles typical of the Guiana Shield highlands region. Additionally, the sampling period covered the dry season in the region. This, linked to the fact that the strong El Niño event of 2015-2016 produced higher temperatures throughout the year (
Integrative approaches are increasingly being used in biological inventories (e.g.,
With the molecular approach, based on reciprocal monophyly, high nodal support and genetic distances of mtDNA, we detected additional samples and extended the distribution of known lineages (
Several attempts have been made to define biogeographical sub-regions within Guiana Shield highlands, mainly based on assemblage similarities among isolated mountain ranges (e.g.,
Some species that are often altitudinal-generalists were only found on the Serra da Mocidade at altitudes higher than 900 m (e.g.,
The results from this short-term multidisciplinary expedition (see other scientific results in
The Expedition “Biodiversity of the Serra da Mocidade” was the result of a collaboration between the Instituto Nacional de Pesquisas da Amazônia (
Specimens examined
(measurement/occurence/multimedia/etc.)