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Corresponding author: Leandro J.C.L. Moraes ( leandro.jclm@gmail.com ) Academic editor: Anthony Herrel
© 2017 Leandro J.C.L. Moraes, Alexandre P. de Almeida, Rafael de Fraga, Rommel R. Zamora, Renata M. Pirani, Ariane A.A. Silva, Vinícius T. de Carvalho, Marcelo Gordo, Fernanda P. Werneck.
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.
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Moraes LJCL, Almeida AP, Fraga R, Rojas RR, Pirani RM, Silva AAA, de Carvalho VT, Gordo M, Werneck FP (2017) Integrative overview of the herpetofauna from Serra da Mocidade, a granitic mountain range in Northern Brazil . ZooKeys 715: 103-159. https://doi.org/10.3897/zookeys.715.20288
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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.
Amazonia, bioacoustics, biogeography, lowland forest, morphology, mountain, mtDNA, Pantepui, phylogenetic relationships
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 (INPA, 2016), highly isolated from other mountains and with difficult access. Here we present and discuss the diversity of amphibians and reptiles of the area and their biotic affinities, using an integrative approach combining morphological, bioacoustical and molecular analyses to identify specimens. We found remarkable records, and make observations concerning species taxonomy, ecology and distribution patterns in the Guiana Shield highlands region.
The Guiana Shield highlands region is located in northern South America, within the limits of Venezuela, Guyana, Suriname, and Brazil (Fig.
This study was conducted at Serra da Mocidade (Figs
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 (INPA-H) and of Genetics Resources (INPA-HT) of the Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Amazonas, Brazil, respectively.
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: (AS) Active survey; (PT) Pitfall traps; (TN) Trammel nets; (HM) Hook with meat bait; (GT) Glue traps; (SG) Shotgun; (OE) Occasional encounters. Morphological measurements: (SVL) Snout-vent length; (CL) Caudal length; (CAL) Carapace length; (CW) Carapace width. Geographical distribution: (WD) Widely distributed in Amazonia; (WA) Western Amazonia; (EA) Eastern Amazonia; (AN) Andes; (GS) Guiana Shield; (GH) Guiana Shield highlands; (PE) Potentially endemic to the Serra da Mocidade region; (PR) Punctual restricted localities; (TZ) Transition zones between Amazonia and other biomes. Altitudinal range: (L) Lowland (below 500 m asl); (U) Upland (above 500 m asl).
Taxon | Altitude (m asl) | Sampling method | Morphological measurements (mm) | Geographic distribution | Altitudinal range | |||
---|---|---|---|---|---|---|---|---|
600 | 960 | 1,060 | 1,365 | |||||
Amphibia | 89 | 28 | 101 | 14 | ||||
Gymnophiona | 3 | |||||||
Rhinatrematidae | 1 | |||||||
Epicrionops sp. | 1 | OE | SVL 83.5 | PE § | U| | |||
Siphonopidae | 2 | |||||||
Brasilotyphlus sp. | 2 | OE | PE §,| | U| | ||||
Anura | 91 | 28 | 98 | 14 | ||||
Allophrynidae | 1 | |||||||
Allophryne ruthveni Gaige, 1926 | 1 | AS | SVL 28.1 | WD † | L‡‡‡ | |||
Aromobatidae | 25 | 4 | 23 | 8 | ||||
Anomaloglossus apiau Fouquet, Souza, Nunes, Kok, Curcio, Carvalho, Grant & Rodrigues, 2015 | 25 | 4 | 23 | 8 | AS, OE | SVL 15–23 | GH †,¶ | U§,¶ |
Bufonidae | 3 | 3 | ||||||
Rhaebo guttatus (Schneider, 1799) | 3 | 3 | AS | SVL 147–167 | WD † | L, U‡‡‡ | ||
Rhinella marina (Linnaeus, 1758) | 5 | SVL 21–44 | WD † | L‡‡‡ | ||||
Rhinella martyi Fouquet, Gaucher, Blanc & Vélez-Rodriguez, 2007 | 1 | 13 | 1 | AS, PT, OE | SVL 50–70 | GS †,# | L, U# | |
Craugastoridae | 10 | 8 | 11 | 2 | ||||
Pristimantis aff. vilarsi | 10 | 8 | 11 | 2 | AS | SVL 17–56.9 | GH †,§ | L, U‡‡‡ |
Centrolenidae | 5 | 4 | 8 | |||||
Hyalinobatrachium aff. taylori | 4 | 2 | 1 | AS | SVL 18–21 | PE †,§ | U‡‡‡ | |
Vitreorana ritae (Lutz, 1952) | 1 | 2 | 7 | AS | SVL 17–22 | GS, PR† | L, U‡‡‡ | |
Hemiphractidae | 2 | |||||||
Stefania sp. | 2 | AS, OE | SVL 52, 54 | PE †,§ | U† | |||
Hylidae | 11 | 10 | 40 | 3 | ||||
Boana boans (Linnaeus, 1758) | 8 | 2 | 9 | AS, OE | SVL 82–111 | WD † | L, U‡‡‡ | |
Boana multifasciata (Günther, 1859) | 1 | 2 | AS | SVL 55–72 | EA, TZ† | L, U‡‡‡ | ||
Boana xerophylla (Duméril & Bibron, 1841) | 1 | AS | SVL 57 | GS † | L, U‡‡‡ | |||
Dendropsophus minutus (Peters, 1872) | 3 | 14 | AS | SVL 20.5–27 | WD † | L, U‡‡‡ | ||
Dendropsophus parviceps (Boulenger, 1882) | 1 | 5 | AS | SVL 20–27 | WD † | L, U‡‡‡ | ||
Osteocephalus taurinus Steindachner, 1862 | 2 | 4 | 9 | 3 | AS | SVL 64.5–90 | WD, TZ† | L, U‡‡‡ |
Leptodactylidae | 19 | |||||||
Adenomera andreae (Müller, 1923) | 1 | AS | SVL 24 | WD †,†† | L‡‡‡ | |||
Leptodactylus guianensis Heyer & de Sá, 2011 | 2 | AS | SVL 103.7 | GS †,†† | L††,‡‡‡ | |||
Leptodactylus mystaceus (Spix, 1824) | 6 | AS, OE | SVL 50–59 | WD †,†† | L††,‡‡‡ | |||
Leptodactylus petersii (Steindachner, 1864) | 1 | AS | SVL 32.5 | WD †,†† | L††,‡‡‡ | |||
Physalaemus ephippifer (Steindachner, 1864) | 7 | AS, PT | SVL 20–28 | GS †,†† | L††,‡‡‡ | |||
Ranidae | 11 | |||||||
Lithobates palmipes (Spix, 1824) | 11 | AS | SVL 72–96 | WD † | L‡‡‡ | |||
Reptilia | 58 | 2 | 13 | |||||
Squamata | 43 | 2 | 13 | |||||
‘Sauria’ | 34 | 1 | 5 | |||||
Gymnophthalmidae | 3 | |||||||
Cercosaura ocellata Wagler, 1830 | 1 | PT | SVL 56.5 | EA ‡,†††† | L‡‡ | |||
Tretioscincus oriximinensis Ávila-Pires, 1995 | 2 | AS, GT | SVL 53, 55 | GS, PR‡,‡‡, †††† | L, U‡‡ | |||
Dactyloidae | 12 | 2 | ||||||
Anolis punctatus Daudin, 1802 | 1 | AS | SVL 83 | WD ‡,§§ | L, U‡‡ | |||
Anolis fuscoauratus d’Orbigny, 1837 | 11 | 1 | AS | SVL 40–49 | WD ‡,§§ | L, U‡‡ | ||
Anolis planiceps Troschel, 1848 | 1 | AS | SVL 40 | GS ‡,§§ | L, U‡‡ | |||
Phyllodactylidae | 4 | |||||||
Thecadactylus rapicauda (Houttuyn, 1782) | 4 | AS, GT, OE | SVL 92–115 | WD ‡,|| | L‡‡ | |||
Sphaerodactylidae | 5 | |||||||
Pseudogonatodes guianensis Parker, 1935 | 5 | AS, GT | SVL 15–17 | WD ‡,|| | L‡‡ | |||
Polychrotidae | 1 | |||||||
Polychrus marmoratus (Linnaeus, 1758) | 1 | SG | SVL 133 | WD ‡,§§ | L‡‡ | |||
Tropiduridae | 2 | 1 | 3 | |||||
Plica plica (Linnaeus, 1758) | 2 | 1 | 3 | AS, PT, SG, OE | SVL 52–141 | WD ‡,§§ | L, U‡‡ | |
Teiidae | 3 | |||||||
Ameiva ameiva ameiva (Linnaeus, 1758) | 3 | SG | SVL 52–85 | WD ‡,‡‡ | L‡‡ | |||
Scincidae | 4 | |||||||
Mabuya nigropunctata (Spix, 1825) | 4 | PT, SG | SVL 72–105 | WD ‡,‡‡ | L‡‡ | |||
Serpentes | 9 | 1 | 8 | |||||
Colubridae | 2 | 2 | ||||||
Atractus riveroi Roze, 1961 | 3 | PT | SVL 229–290, CL 29.1–54.5 | GH ‡,¶¶ | U¶¶ | |||
Chironius fuscus (Linnaeus, 1758) | 6 | 4 | AS | SVL 565, 603, CL 320, 357 | WD ‡,## | L, U§§§ | ||
Chironius septentrionalis Dixon, Wiest & Cei, 1993 | 1 | AS | SVL 1,480, CL 350 | GH ‡,## | L, U‡‡‡,§§§ | |||
Drymobius rhombifer (Günther, 1860) | 1 | AS | SVL 365, CL 131 | WD ‡,## | L, U‡‡‡ | |||
Dipsas catesbyi (Sentzen, 1796) | 1 | OE | SVL 229, CL 89 | WD ‡,††† | L, U‡‡‡ | |||
Dipsas indica indica Laurenti, 1768 | 1 | AS | SVL 520, CL 209 | WD ‡,## | L, U‡ | |||
Dipsas pavonina Schlegel, 1837 | 1 | OE | SVL 275, CL 95 | EA, AN‡,††† | L, U‡‡‡ | |||
Imantodes cenchoa (Linnaeus, 1758) | 1 | AS | SVL 713, CL 315 | WD ‡,## | L‡ | |||
Xenodon rabdocephalus rabdocephalus (Wied, 1824) | 1 | AS | SVL 440, CL 399 | WD ‡,## | L## | |||
Elapidae | 1 | |||||||
Micrurus remotus Roze, 1987 | 1 | OE | SVL 42.7, CL 7 | WA ‡,## | L, U## | |||
Viperidae | 2 | 1 | 2 | |||||
Bothrops atrox (Linnaeus, 1758) | 1 | 1 | AS, PT | SVL 93.5, 952, CL 17.5, 170 | WD ‡,## | L, U## | ||
Bothrops bilineatus bilineatus (Wied, 1821) | 1 | 1 | AS | SVL 450, 626, CL 80, 104 | WD ‡,## | L, U## | ||
Lachesis muta muta (Linnaeus, 1766) | 1 | AS | SVL 1,575, CL 175 | WD ‡,## | L||| | |||
Testudines | 13 | |||||||
Chelidae | 11 | |||||||
Mesoclemmys gibba (Schweigger, 1812) | 10 | TN, HM | CAL 109–189, CW 84–138 | WD ‡,¶¶¶ | L¶¶¶ | |||
Platemys platycephala melanonota Ernst, 1984 | 1 | OE | - | WD ‡,¶¶¶ | L¶¶¶ | |||
Testudinidae | 2 | |||||||
Chelonoidis denticulatus (Linnaeus, 1766) | 2 | OE | - | WD ‡,¶¶¶ | L¶¶¶ | |||
Crocodylia | 2 | |||||||
Alligatoridae | 2 | |||||||
Paleosuchus trigonatus (Schneider, 1801) | 2 | AS | SVL 160, 675 | WD ‡,### | L, U### |
Amphibian diversity. Examples of amphibians recorded in the Serra da Mocidade mountain range. a Anomaloglossus apiau, male b Anomaloglossus apiau, female c Rhaebo guttatus d Rhinella martyi eHyalinobatrachium aff. taylorif Vitreorana ritae g Dendropsophus minutus h Dendropsophus parviceps i Boana boans j Boana xerophylla. Photographs by Haroldo Palo Jr. (c–j).
Amphibian diversity. Examples of amphibians recorded in the Serra da Mocidade mountain range. a Boana multifasciata b Osteocephalus taurinus c Stefania sp. d Leptodactylus guianensis e Leptodactylus mystaceus f Physalaemus ephippifer gPristimantis aff. vilarsih Epicrionops sp. Photographs by Haroldo Palo Jr. (a, b, d–g), and Marcos Amend (h).
Lizard diversity. Examples of lizards recorded in the Serra da Mocidade mountain range. a Anolis fuscoauratus b Anolis planiceps c Cercosaura ocellata d Tretioscincus oriximinensis e Polychrus marmoratus f Thecadactylus rapicauda g Mabuya nigropunctata h Plica plica. Photographs by Haroldo Palo Jr. (a–c, e–h) and Marcos Amend (d).
Snake diversity. Examples of snakes recorded in the Serra da Mocidade mountain range. a Chironius septentrionalis b Chironius fuscus c Drymobius rhombifer d Atractus riveroi, morph 1 e Atractus riveroi, morph 2 f Dipsas indica indica g Dipsas pavonina h Imantodes cenchoa. Photographs by Haroldo Palo Jr. (a, b, f–h) and Marcos Amend (d, e).
Snake, chelonian and crocodilian diversity. Examples of snakes, chelonians and the crocodilian recorded in the Serra da Mocidade mountain range. a Xenodon rabdocephalus rabdocephalus b Micrurus remotus c Bothrops atrox d Bothrops bilineatus bilineatus e Lachesis muta muta f Mesoclemmys gibba g Platemys platycephala melanonota h Paleosuchus trigonatus. Photographs by Haroldo Palo Jr. (a, c, e–h).
Habitat diversity. Examples of habitats sampled in the Serra da Mocidade mountain range. a Submontane rainforest at 600 m asl b Pacú River, main water body near camp #1 c Montane rainforest at 1,060 m asl d, e Rocky streams at 1,060 m asl f Montane rainforest at 1,365 m asl. Photographs by Ramiro Melinski (a–c, e–f).
Variation in species richness and composition. a, b Extrapolated rarefaction curves showing variation in species richness related to sampling effort at our total sampling a and at distinct altitudinal levels b of the Serra da Mocidade mountain range. Observed data are in full lines and extrapolated in dashed lines c Non-metric multidimensional scaling (NMDS) ordination for amphibian and reptile assemblages from mountain ranges of Guiana Shield highlands and nearby lowland habitats, showing the mixed influence in the Serra da Mocidade composition. Mountain ranges: (MO) Mocidade; (AP) Apiaú; (Du) Duida; (Ma) Marahuaka; (AT) Auyantepui; (Ch) Chimantá; (Gq) Guaiquinima; (NE) Neblina; (TA) Tamacuari; (YU) Yutajé-Corocoro; (RO) Roraima; (SA) Sarisariñama; (NL) Nassau Lely. Lowland habitats: (F1, O1) ESEC Maracá; (F2, O2) PARNA Viruá; (F3, O3) Roraima Lowlands; (F4, O4) Samã and Miang rivers region; (F5, O5) Parque Nacional Canaima; (F6, O6) Parque Nacional da Serra da Mocidade and Estação Ecológica Niquiá; (F7) Kurupukari. References are detailed in the text.
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 Leptodactylus Fitzinger, 1826 only recorded at 600 m asl or the snakes Micrurus remotus Roze, 1987 and Chironius septentrionalis Dixon, Wiest & Cei, 1993 only recorded at 1,060 m asl (Fig.
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 Dendropsophus minutus (Peters, 1872), Rhinella martyi Fouquet, Gaucher, Blanc & Vélez-Rodriguez, 2007, Boana boans (Linnaeus, 1758) and Anomaloglossus apiau Fouquet, Souza, Nunes, Kok, Curcio, Carvalho, Grant & Rodrigues, 2015. We obtained DNA sequences from 74 specimens of taxonomically confusing taxa (10 species) to conduct our phylogenetic analyses. These analyses revealed that some species initially thought by us to be new taxa represent taxa already described, for instance A. apiau, R. martyi, Dendropsophus parviceps (Boulenger, 1882), Vitreorana ritae (Lutz, 1952) and Tretioscincus oriximinensis Ávila-Pires, 1995. Additionally, molecular data indicated the existence of some new candidate species (
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 |
---|---|---|---|
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 |
Lowland habitats | |||
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 Stefania sp., Epicrionops sp., Brasilotyphlus sp. and Hyalinobatrachium aff. taylori (Table
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.
Epicrionops sp. – The genus Epicrionops Boulenger, 1883 is distributed in mountainous habitats of the Andes (seven species) and the Guiana Shield highlands [Epicrionops niger (Dunn, 1942)] (
Phylogenetic relationships of caecilians. Maximum likelihood phylogenetic tree of caecilians families Siphonopidae and Rhinatrematidae, based on a 468bp fragment of the 16S mtDNA. Only bootstrap values >80% are shown (5,000 replicates). The GenBank accession numbers appear after the names of downloaded sequences, and specimens from the Serra da Mocidade are highlighted.
Brasilotyphlus sp. – The genera Microcaecilia Taylor, 1968 and Brasilotyphlus Taylor, 1968 (possibly synonymous by lack of diagnosability–see
Anomaloglossus apiau – The high endemism levels of the small cryptically coloured terrestrial frogs of the genus Anomaloglossus recorded from Guiana Shield highlands mountains (
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) |
---|---|---|---|---|---|---|---|
Anomaloglossus apiau | 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) |
Anomaloglossus apiau | 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) |
Dendropsophus minutus | Serra da Mocidade, RR, Brazil | Single note | 0.09 (0.04–0.18) | 13 (11.2–17.4) | - | - | 3.72 (2.1–4.5) |
Dendropsophus minutus | Different localities‡ | Single note | 0.11 (0.03–0.2) | 14.7 (11.1–18.3) | - | - | 3.75 (2.2–5.3) |
Boana boans | 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) |
Boana boans | Different localities| | Long train | 0.42 (0.18–1.19) | 2.05 (0.57–4.7) | - | - | 0.648 (0.2–1.1) |
Rhinella martyi | Serra da Mocidade, RR, Brazil | Series of pulses | 0.302 (±0.026) | 0.61 (±0.18) | 0.015 (±0.004) | - | 1.237 (±0.03) |
Rhinella martyi | Guiana Shield lowlands§ | Series of pulses | 0.295 (±0.013) | - | 0.009 (±0.001) | - | 1.169 (±0.04) |
The population of Serra da Mocidade had adult males with 15–20 mm SVL, and females slightly larger than originally described for A. apiau (19–23 mm SVL) (see
Phylogenetic relationships of Anomaloglossus. Maximum likelihood phylogenetic tree of Anomaloglossus species, based on a 361bp fragment of the 16S mtDNA. Only bootstrap values >80% are shown (5,000 replicates). The GenBank accession numbers appear after the names of downloaded sequences, and specimens from the Serra da Mocidade are highlighted.
This record of A. apiau from the Serra da Mocidade (first outside the type locality) is remarkable, since the species was not recorded from the mountain range of the Serra da Maroquinha, located at less than 5 km southeast from the Serra do Apiaú. New studies on the cryptic diversity, evolution and biogeography of the genus Anomaloglossus (such as
Rhinella martyi – Rhinella martyi has a confusing taxonomic history, as do many of the small-medium terrestrial forest bufonids in the Rhinella margaritifera group (
Individuals of R. martyi were found on leaf-litter inside primary forests, and calling males on the banks of streams, mostly at 1,060 m asl (Fig.
Pristimantis aff. vilarsi – Pristimantis is one of the most speciose genus of vertebrates (
Hyalinobatrachium aff. taylori – The species of Hyalinobatrachium from Serra da Mocidade (Fig.
Phylogenetic relationships of Hyalinobatrachium. Maximum likelihood phylogenetic tree of Hyalinobatrachium species from Guiana Shield, based on a 465bp fragment of the 16S mtDNA. Only bootstrap values >80% are shown (5,000 replicates). The GenBank accession numbers appear after the names of downloaded sequences, and specimens from the Serra da Mocidade are highlighted.
The diversity of Hyalinobatrachium in the Guiana Shield highlands region appears underestimated, since some lineages were recently described as new species after an integrative revision (
Vitreorana ritae – The small glassfrog Vitreorana ritae is apparently widely distributed in the Guiana Shield (
Phylogenetic relationships of Vitreorana. Maximum likelihood phylogenetic tree of Vitreorana species, based on a 496bp fragment of the 16S mtDNA. Only bootstrap values >80% are shown (5,000 replicates). The GenBank accession numbers appear after the names of downloaded sequences, and specimens from the Serra da Mocidade are highlighted.
Stefania sp. – The marsupial frog genus Stefania have an evolutionary history intrinsically linked to the evolution of the Guiana Shield highlands landscape, as the genus has a geographical range restricted to this region and high endemism levels in distinct mountain ranges (
Phylogenetic relationships of Stefania. Maximum likelihood phylogenetic tree of Stefania species, based in a 536bp fragment of the 16S mtDNA. Only bootstrap values >80% are shown (5,000 replicates). The GenBank accession numbers appear after the names of downloaded sequences, species numbers of undescribed taxa follow
Dendropsophus minutus – The species complex of small arboreal Dendropsophus minutus hylids is widely distributed in South America east of Andes, occupying a broad altitudinal range (
Dendropsophus parviceps – Recent molecular studies on the evolution of the genus Dendropsophus found a polyphyletic Dendropsophus parviceps species group sensu
Phylogenetic relationships of Dendropsophus. Maximum likelihood phylogenetic tree of some species from Dendropsophus parviceps clade, based on a 350bp fragment of the 16S mtDNA. Only bootstrap values >80% are shown (5,000 replicates). The GenBank accession numbers appear after the names of downloaded sequences, and specimens from the Serra da Mocidade are highlighted.
Phylogenetic relationships of Tretioscincus. Maximum likelihood phylogenetic tree of Tretioscincus species and populations, based on a 427bp fragment of the 16S mtDNA. Only bootstrap values >80% are shown (5,000 replicates). The GenBank accession numbers appear after the names of downloaded sequences, and specimens from the Serra da Mocidade are highlighted.
Boana boans, B. multifasciata, B. xerophylla and Osteocephalus taurinus – These medium to large sized arboreal hylids have wide geographical ranges in Amazonia: B. boans (Fig.
Adenomera andreae and Leptodactylus petersii – These species are both terrestrial frogs, typical of Amazonian lowlands (
Lithobates palmipes – This large ranid inhabit forest habitats near to slow-flowing water bodies (lakes, ponds and rivers), is widely distributed in Amazonia, Atlantic Forest and transitional habitats and may represent a species complex. The presence of several gaps in the known species distribution hampers a precise geographical determination (
Pseudogonatodes guianensis – Pseudogonatodes guianensis is a small leaf-litter lizard widely distributed within Amazonian lowlands (
Plica plica – This widely distributed arboreal lizard (
Mabuya nigropunctata – Specimens of Mabuya from Serra da Mocidade (Fig.
Intraspecific analyses of molecular variation indicated a strong genetic structure and multiple lineages within this widely distributed Amazonian taxon (
Tretioscincus oriximinensis – The small cryptic specimens of Tretioscincus from Serra da Mocidade (Fig.
There is a subtle morphological divergence between T. oriximinensis populations from northern (including Serra da Mocidade) and eastern Amazonia (
Atractus riveroi – This groundsnake typical from Guiana Shield highlands was previously known by only two specimens (
Chironius fuscus and C. septentrionalis – Two species of diurnal Chironius snakes were recorded at Serra da Mocidade: one is a typical lowland species widely distributed in Amazonia and other ecosystems in South America (Chironius fuscus – Fig.
Drymobius rhombifer – Despite being widely distributed in Amazonia (
Micrurus remotus – The holotype of this small monadal coral snake is from the Guiana Shield highlands region [Cerro de la Neblina (
Platemys platycephala melanonota – Platemys platycephala (Schneider, 1792) is a solitary and nocturnal chelid, which inhabits shallow temporary pools within Amazonian lowland rainforests (
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 (A. apiau, R. martyi, and T. oriximinensis, with genetic distances less than 2%), discovered putative divergent lineages of known species (H. aff. taylori, P. aff. vilarsi, V. ritae, and D. parviceps, with genetic distances between 3–6%), as well as candidate new species (Stefania sp., Epicrionops sp. and Brasilotyphlus sp., with genetic distances between 10–17%). The taxonomic status of the putative new species detected in this study needs to be confirmed using a broader and more detailed analyses of data sources, which may increase the known species diversity at Serra da Mocidade.
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., D. minutus, D. parviceps, B. xerophylla, A. punctatus, B. b. bilineatus). The Serra da Mocidade mountain range has a complex hydrologic mosaic, with streams that vary in their basin origins and amounts of dissolved sediments (
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 (INPA), Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), Comando Militar da Amazônia (CMA), and Grifa Filmes. We are grateful to R. Ferreira for assistance and sharing of data regarding the conservation unit, T. Laranjeiras, H. Palo Jr., M. Amend and R. Melinski for contribution with landscape and specimen photographs, members of Thematic Laboratory of Molecular Biology (INPA) for help during sequencing process and A. Fouquet, P. Passos, P. Nunes, T. Mott, R. MacCulloch and O. Entiauspe for help in species identification. Adrian Barnett helped with the English. Specimens were collected under the permission issued by ICMBio (processes 52206-1 and 44832-1). RF, LJCLM and APA thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do Amazonas (FAPEAM) for scholarship. FPW thanks financial support from CNPq (475559/2013-4), FAPEAM (062.00665/2015), Partnerships for Enhanced Engagement in Research from the U.S. National Academy of Sciences and U.S. Agency of International Development (PEER NAS/USAID PGA-2000005316), and L’Oréal-Unesco For Women in Science Program.
Specimens examined
Data type: (measurement/occurence/multimedia/etc.)