Research Article |
Corresponding author: Matheus de Oliveira Neves ( nevesmo@yahoo.com.br ) Academic editor: Andreas Maletzky
© 2019 Matheus de Oliveira Neves, André Yves, Elvis Almeida Pereira, Leandro Alves, Jacqueline Bonfim Vasques, Joaquim Fernandes Teixeira Coelho, Patricia 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:
Neves MO, Yves A, Pereira EA, Alves L, Vasques JB, Coelho JFT, Silva PS (2019) Herpetofauna in a highly endangered area: the Triângulo Mineiro region, in Minas Gerais State, Brazil. Herpetozoa 32: 113-123. https://doi.org/10.3897/herpetozoa.32.e35641
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The Brazilian Cerrado and Atlantic Forest shelter an especially rich herpetofauna and experience strong anthropogenic disturbances, which is also true for the western portion of Minas Gerais State. Herein, we present a list of the herpetofauna from the Triângulo Mineiro region in Minas Gerais State, southeastern Brazil. From 2012 to 2016, we sampled 28 localities along 23 municipalities in the region, using three sampling methods: active search, pitfall traps, and opportunistic records. We recorded 79 species, 44 amphibians and 35 reptiles. Three species (Bokermannohyla sazimai, Ololygon canastrensis, and Pithecopus azureus) are classified as “data deficient” (DD) according to the IUCN. One species (Proceratophrys moratoi) is classified as “critically endangered” (CR) according to the IUCN Red List, and “endangered” (EN) according to the national red list. However, we suggest listing P. moratoi in the “least concern” category. We also present the first record of Dendropsophus elianeae in Minas Gerais State, and distribution map of the species. Furthermore, we elucidate the composition of the herpetofauna in the Triângulo Mineiro region and contribute to future conservation plans for the region and the species.
amphibians, Atlantic Forest, Cerrado, checklist, new records, reptiles
Brazil harbors the most diverse herpetofauna in the world (
The transition zones between such domains lead to a wide overlap in geographic distribution of amphibians and reptiles, with phytophysiognomies ranging from savanna formations (e.g. Cerrado stricto sensu) to forest environments (e.g. gallery forest) (
This situation is the same in the Triângulo Mineiro region (TM hereafter) in western Minas Gerais State. The TM is characterized by the Atlantic Forest and Cerrado, which are the main physiognomies of the landscape. However, less than 25% of the TM remains undisturbed (
Some studies surveying the local herpetofauna in the TM region present amphibians (
The TM region is located in the western portion of Minas Gerais state, encompasses 66 municipalities, and covers nearly 90,000 km² (Fig.
Sampling areas distributed in the TM region, Minas Gerais State. Sampling points: (1) Rural Reserve, (2) Ferry of the Paranaíba River, (3) Meddle São Domingos River, (4) Santa Rita Farm, (5) Cisco Stream, (6) Low São Mateus Riverside, (7) High São Mateus Riverside, (8) Meddle Frutal Riverside, (9) Cocal Riverside, (10) Giral Powerplant Region, (11) Grande River Bank, (12) Mata Farm, (13) Delta Region, (14) Aroeiras Farm, (15) Grotão Farm, (16) Estreito Powerplant, (17) Low Piedade River, (18) High Barreirinho Stream, (19) Paranaíba’s Lake, (20) Garcias Region, (21) Cruz Riverside, (22) Samambaia Riverside, (23) Óleo Riverside, (24) Powerplant Region, (25) Paraíso Ranch, (26) Grupiara Dam, (27) Confins Region, and (28) D’Anta Stream. Dark gray: Atlantic Forest; Light gray: Cerrado.
Between 2012 and 2016, we sampled from 28 localities in 23 municipalities in the TM region (Fig.
Sampling areas distributed in the TM region, Minas Gerais State, Southeast Brazil with their respective municipalities, coordinates, and sampling efforts of active search (h) and pitfalls (days of sampling).
Locality | Municipality | Coordinates | Sampling efforts (h) | Pitfall (days of sampling) | |
---|---|---|---|---|---|
1 | Rural Reserve | Limeira do Oeste | 19°23'59.90"S, 50°46'1.17"W | 24 | – |
2 | Ferry of the Paranaíba River | Limeira do Oeste | 19°15'51.82"S, 50°46'54.93"W | 72 | – |
3 | Meddle São Domingos River | Santa Vitória | 19°11'55.72"S, 50°35'45.82"W | 24 | – |
4 | Santa Rita Farm | Carneirinho | 19°42'56.52"S, 50°35'38.91"W | 12 | – |
5 | Cisco Stream | Fronteira | 20°15'47.00"S, 49°13'45.00"W | 54 | 5 |
6 | Low São Mateus Riverside | Itapagipe | 19°55'49.73"S, 49°13'18.99"W | 54 | 5 |
7 | High São Mateus Riverside | Comendador Gomes | 19°43'29.00"S, 49°11'44.00"W | 54 | 5 |
8 | Meddle Frutal Riverside | Frutal | 19°57'43.73"S, 48°57'2.09"W | 54 | 5 |
9 | Cocal Riverside | Prata | 19°26'1.69"S, 48°52'46.69"W | 12 | – |
10 | Giral Powerplant Region | Conceição das Alagoas | 20°01'26"S, 48°13'24"W | 10 | – |
11 | Grande River Bank | Água Comprida | 19°58'52"S, 48°07'32"W | 36 | – |
12 | Mata Farm | Uberaba | 20°5'36.58"S, 47°53'50.39"W | 54 | 5 |
13 | Delta Region | Delta | 19°55'41.02"S, 47°45'1.09"W | 72 | 10 |
14 | Aroeiras Farm | Uberaba | 19°49'50.78"S, 47°42'37.75"W | 30 | 5 |
15 | Grotão Farm | Uberaba | 19°39'22.04"S, 47°43'1.28"W | 30 | – |
16 | Estreito Powerplant | Sacramento | 20°08'58"S, 47°16'37"W | 56 | – |
17 | Low Piedade River | Araporã | 18°31'46.58"S, 49°14'54.37"W | 36 | 5 |
18 | High Barreirinho Stream | Centralina | 18°38'53.60"S, 49°9'17.88"W | 36 | 5 |
19 | Paranaíba's Lake | Centralina | 18°29'39.13"S, 49°8'27.05"W | 36 | 5 |
20 | Garcias Region | Monte Alegre de Minas | 18°33'23.56"S, 48°59'47.57"W | 36 | 5 |
21 | Cruz Riverside | Tupaciguara | 18°39'44.50"S, 48°37'18.43"W | 36 | – |
22 | Samambaia Riverside | Tupaciguara | 18°46'26.00"S, 48°36'33.00"W | 12 | – |
23 | Óleo Riverside | Uberlândia | 18°56'10.75"S, 48°19'39.39"W | 24 | – |
24 | Powerplant Region | Araguari | 18°26'56"S, 47°59'21"W | 10 | – |
25 | Paraíso Ranch | Cascalho Rico | 18°33'39"S, 47°52'57"W | 12 | – |
26 | Grupiara Dam | Grupiara | 18°26'33"S, 47°47'20"W | 30 | – |
27 | Confins Region | Douradoquara | 18°23'03"S, 47°37'39"W | 20 | – |
28 | D'Anta Stream | Campos Altos | 19°40'6.72"S, 45°57'13.36"W | 40 | 5 |
Due to logistical issues, sampling efforts were not systematically undertaken. The herpetofauna was sampled using the following methods: i) active search (AS), ii) pitfall traps (PT), and iii) opportunistic records (OR). The AS method consisted of random search for specimens (from 16:00 to 22:00hs) in fallen trunks, rocky crevices, bromeliads, and marginal vegetation of water bodies (
We collected the individuals and killed them by immersion in water with benzocaine hydrochloride 250 mg/l or intraperitoneal injection of liquid lidocaine (
The conservation status of each taxon was verified using the list of endangered fauna species for Minas Gerais State (
We recorded a total of 79 species: 44 amphibians (Fig.
Anuran species recorded from sampling areas in the TM region of Minas Gerais State. Family Brachycephalidae: (a) Ischnocnema sp. (gr. guentheri); Family Bufonidae: (b) Rhinella mirandaribeiroi; Family Hylidae: (c) Boana lundii, (d) Dendropsophus elianeae, (e) Ololygon canastrensis, (f) Pseudis bolbodactyla, (g) Pseudis platensis, and (h) Scinax squalirostris; Family Leptodactylidae: (i) Physalaemus marmoratus, and (j) Pseudopaludicola falcipes; Family Microhylidae: (k) Chiasmocleis albopunctata; Family Odontophrynidae: (l) Proceratophrys moratoi.
List of anuran species recorded in the TM region, Minas Gerais State. Methods: (AS) Active Search, (OR) Opportunistic Records, and (PT) Pitfall Traps. Sampling points where specimens were found see Table
Order/Family/Species | Sampling | Sampling Points | Habitats (Microhabitats) |
---|---|---|---|
Anura | |||
Brachycephalidae | |||
Ischnocnema sp. (gr. guentheri) | AS | 28 | FF(ar) |
Bufonidae | |||
Rhinella schneideri (Werner, 1894) | AS, OR | 1–3, 5–7, 9–12, 16–21, 25, 27 | OF, RF, DA, PO, UR (ll, bs) |
Rhinella mirandaribeiroi (Gallardo, 1965) | AS | 7, 14, 21 | PO, SW (bs) |
Hylidae | |||
Boana albopunctata (Spix, 1824) | AS | 1–6, 8–15, 17–23, 25 | RF, DA, LK, PO, SW (sh, bs) |
Boana faber (Wied-Neuwied, 1821) | AS, OR | 13, 28 | FF, DA, LK (ar, ow) |
Boana lundii (Burmeister, 1856) | AS | 2, 3, 7–9, 12, 13, 15, 17, 18, 20–22, 28 | RF, FF, SW (ar) |
Boana raniceps Cope, 1862 | AS | 1–3, 5, 6, 10, 17–19, 25 | OF, LK, SW (sh) |
Bokermannohyla sazimai (Cardoso & Andrade, 1983) | AS | 15 | OF, ST (ar) |
Dendropsophus cruzi (Pombal & Bastos, 1998) | AS | 1–3, 7, 17–20, 22, 23 | OF, DA, LK, SW (sh) |
Dendropsophus elianeae (Napoli & Caramaschi, 2000) | AS | 1, 2, 13, 16, 18 | OF, DA, LK, SW (sh) |
Dendropsophus jimi (Napoli & Caramaschi, 1999) | AS | 11, 13–15, 19, 20, 23 | OF, DA, LK, SW (sh) |
Dendropsophus melanargyreus (Cope, 1887) | AS | 7, 19, 21 | OF, FF, PO (ar, sh) |
Dendropsophus minutus (Peters, 1872) | AS | 1, 3, 5, 7, 8, 10, 12- 23, 28 | OF, RF, FF, DA, LK, PO, SW (ar, sh) |
Dendropsophus nanus (Boulenger, 1889) | AS | 2, 5–7, 10, 12, 17, 1–21, 25 | OF, DA, LK, SW (sh) |
Ololygon canastrensis (Cardoso & Haddad, 1982) | AS | 28 | OF, DA (sh) |
Pseudis bolbodactyla Lutz, 1925 | AS | 1, 19 | LK (ow) |
Pseudis platensis (Linnaeus, 1758) | AS | 5 | LK (ow) |
Scinax constrictus Lima, Bastos & Giaretta, 2005 | AS | 2 | OF, DA (sh) |
Scinax fuscomarginatus (Lutz, 1925) | AS | 3, 5–7, 17–23 | OF, DA, LK (sh) |
Scinax fuscovarius (Lutz, 1925) | AS | 1, 2, 5–9, 14, 17–23, 28 | OF, RF, DA, PO, SW (sh, bs) |
Scinax squalirostris (A. Lutz, 1925) | AS | 15 | OF, SW (sh) |
Trachycephalus typhonius (Linnaeus, 1758) | AS | 1, 2, 6, 9, 10, 13 | OF, RF, DA, PO, ST (ar) |
Leptodactylidae | |||
Leptodactylus chaquensis (Cei, 1950) | AS | 1, 2, 6, 11–15, 25 | OF, DA, LK, ST, SW (sh) |
Leptodactylus fuscus (Schneider, 1799) | AS | 1–22, 25 | OF, FF, DA, LK, PO, SW (sh) |
Leptodactylus labyrinthicus (Spix, 1824) | AS | 1–3, 5–9, 11, 12, 14–21, 23, 25 | OF, DA, PO, ST, SW, UR (ll, bs) |
Leptodactylus latrans (Steffen, 1815) | AS | 6, 12, 19 | OF, DA, LK, PO, ST, SW (ll, bs) |
Leptodactylus mystaceus (Spix, 1824) | AS, PT | 6, 7, 12, 13, 17 | RF, FF (ll) |
Leptodactylus mystacinus (Burmeister, 1861) | AS, PT | 6, 12, 15, 18, 21, 25 | OF, RF, DA, SW (ll, bs) |
Leptodactylus podicipinus (Cope, 1862) | AS | 2, 5, 6, 8–10, 12–14, 16–22, 24 | OF, RF, DA, LK, PO, SW (ll, bs, ow) |
Leptodactylus syphax Bokermann, 1969 | AS | 7, 9 | OF (ll) |
Physalaemus centralis Bokermann, 1962 | AS, PT | 1, 5, 6, 8, 10, 13, 15, 17, 18, 20, 21 | OF, RF, DA, LK, PO, SW (ll, bs, ow) |
Physalaemus cuvieri Fitzinger, 1826 | AS, PT | 2, 3, 5–8, 10–15, 17–23, 25 | OF, RF, DA, LK, PO, SW (ll, bs, ow) |
Physalaemus marmoratus (Reinhardt & Lütken, 1862) | AS | 9, 20 | OF (bs) |
Physalaemus nattereri (Steindachner, 1863) | AS, PT, OR | 1, 2, 5–9, 11, 12, 15, 17–22 | OF, FF, DA, PO, SW (ll, bs, ow) |
Pseudopaludicola facureae Andrade & Carvalho, 2013 | AS | 1, 2–4, 18–22 | OF, DA, LK, SW (bs, ow) |
Pseudopaludicola falcipes (Hensel, 1867) | AS | 7, 9 | OF, DA, LK, ST, SW (bs, ow) |
Pseudopaludicola saltica (Cope, 1887) | AS | 8, 10, 11, 15, 19, 22 | OF, DA, LK, SW (bs, ow) |
Microhylidae | |||
Chiasmocleis albopunctata (Boettger, 1885) | AS, PT | 12–14, 17, 19 | OF, RF, PO (ll, ow) |
Dermatonotus muelleri (Boettger, 1885) | AS, PT | 12, 14, 15, 17–20 | OF, RF, FF, PO (ll, ow) |
Elachistocleis cesarii (Miranda-Ribeiro, 1920) | AS | 1, 2, 12, 14, 18–21 | OF, RF, DA, PO, ST, SW (bs) |
Odontophrynidae | |||
Proceratophrys moratoi (Jim & Caramaschi 1980) | AS | 5, 7, 14, 19, 21 | OF, FF, ST, SW (ll) |
Odontophrynus cultripes Reinhardt & Lutken, 1862 | AS, OR | 5, 23, 28 | OF, UR (ll) |
Phyllomedusidae | |||
Phitecopus azureus Cope, 1862 | AS | 7, 15, 18, 21, 23 | OF, RF, DA, ST, SW (ar, sh) |
Strabomantidae | |||
Barycholos ternetzi (Miranda-Ribeiro, 1937) | AS, PT | 5–9, 11–15, 17–21 | OF, RF, FF (ll) |
Reptile species recorded from sampling areas in the TM region of Minas Gerais State. Family Alligatoridae: (a) Paleosuchus palpebrosus; Family Boidae: (b) Eunectes murinus; Family Colubridae: (c) Chironius flavolineatus and (d) Tantilla melanocephala; Family Dipsadidae: (e) Helicops modestus, (f) Hydrodynastes gigas, (g) Oxyrhopus guibei, and (h) Oxyrhopus trigeminus; Family Dactyloidae: (i) Norops brasiliensis; Family Mabuyidae: (j) Copeoglossum nigropunctatum; Family Teiidae: (k) Cnemidophorus sp. (aff. ocellifer); Family Typhlopidae: (l) Typhlops brongersmianus.
List of reptile species recorded in the TM region, Minas Gerais State. Methods: (AS) Active Search, (OR) Opportunistic records, and (PT) Pitfall Traps; sampling sites where specimens were found are given in Table
Order/Family/Species | Sampling | Sampling Points | Habitats (Microhabitats) |
---|---|---|---|
Crocodylia | |||
Alligatoridae | |||
Paleosuchus palpebrosus (Cuvier, 1807) | AS | 2, 3, 5, 10 | OF, DA, LK, ST (ow) |
Squamata | |||
Amphisbaenidae | |||
Amphisbaena alba Linnaeus, 1758 | AS, OR | 17, 19, 23 | OF, FF, UR (ll) |
Amphisbaena mertensi Strauch, 1881 | AS | 13 | FF (ll) |
Anguidae | |||
Ophiodes sp. (cf. striatus) (Spix, 1825) | OR | 1, 2, 22 | OF, FF (ll) |
Boidae | |||
Boa constrictor Linnaeus, 1758 | AS, OR | 5, 6, 8, 10–12, 16, 23–25 | OF, RF, FF, DA, LK, SW (ll) |
Epicrates crassus Cope, 1862 | OR | 7 | * |
Eunectes murinus (Linnaeus, 1758) | AS | 2, 5, 6, 8, 11, 12, 16, 25, 27 | OF, RF, ST, SW (ar, ll, ow) |
Colubridae | |||
Chironius flavolineatus (Jan, 1863) | AS | 13, 20 | OF, FF (ar, ll) |
Drymarchon corais (Boie, 1827) | AS | 1 | RF (ll) |
Spilotes pullatus (Linnaeus, 1758) | AS | 14, 15, 21, 24, 25 | OF, FF (ll) |
Tantilla melanocephala (Linnaeus, 1758) | AS | 18, 21 | FF (ll) |
Dipsadidae | |||
Erythrolamprus poecilogyrus (Wied-Neuwied, 1825) | OR | 1, 12, 15 | FF (ll) |
Helicops modestus Günther, 1861 | AS | 19, 22 | OF, LK (ow) |
Hydrodynastes gigas (Duméril, Bibron & Duméril, 1854) | AS, OR | 5, 6 | OF, RF, LK (ll, ow) |
Leptodeira annulata (Linneus, 1758) | OR | 28 | OF (ll) |
Oxyrhopus guibei Hoge & Romano, 1978 | AS, OR | 2, 9, 11, 13–15 | OF, FF (ll) |
Oxyrhopus trigeminus Duméril, Bibron & Duméril, 1854 | AS | 2, 6, 7, 22 | OF, FF (ll) |
Philodryas olfersii (Liechtenstein, 1823) | OR | 21 | FF (ll) |
Philodryas patagoniensis (Girard, 1858) | AS | 3 | FF (ll) |
Sibynomorphus mikanii (Schlegel, 1837) | AS | 6, 13, 22 | OF, SW (ll) |
Xenodon merremii (Wagler, 1824) | OR | 1, 2, 3, 4 | OF, FF (ll) |
Xenopholis undulatus (Jensen, 1900) | OR | 7 | OF (ll) |
Dactyloidae | |||
Norops brasiliensis (Vanzolini & Williams, 1970) | AS | 4, 6, 13, 17, 18 | RF, FF (ar, ll) |
Gekkonidae | |||
Hemidactylus mabouia (Moreau de Jonnés, 1818) | AS | 2, 6, 8, 12, 25 | OF, UR |
Gymnophthalmidae | |||
Colobosaura modesta (Reinhardt & Lütken, 1862) | AS | 28 | FF (ll) |
Mabuyidae | |||
Copeoglossum nigropunctatum (Spix, 1825) | AS | 6, 8, 9, 19, 20 | OF, RF (ll, ft) |
Notomabuya frenata (Cope, 1862) | AS, PT | 1, 11, 13, 14, 17, 18 | OF, RF (ll, ft) |
Teiidae | |||
Ameiva ameiva (Linnaeus, 1758) | AS, PT, OR | 2, 3, 5–8, 10–13, 17–21 | OF, RF, FF, UR (ll, bs) |
Cnemidophorus sp. (aff. ocellifer) | AS | 2–4, 17, 18, 20, 21 | OF, FF (ll, ft) |
Salvator merianae (Duméril & Bibron, 1839) | AS, OR | 1, 2, 5, 6, 8, 10–13, 16–22, 25–27 | OF, RF, FF (ll) |
Typhlopidae | |||
Typhlops brongersmianus Vanzolini, 1976 | PT | 7, 17, 18 | FF (ll) |
Tropiduridae | |||
Tropidurus torquatus (Wied-Neuwied, 1820) | AS, PT, OR | 1, 2, 9, 11, 17–20, 22, 25 | OF, RF, FF, UR (ll) |
Viperidae | |||
Bothrops moojeni (Hoge, 1966) | AS, OR | 1–3, 5, 6, 8, 11–15, 17–20, 22 | OF, RF, FF (ll, bs, ft) |
Crotalus durissus Linnaeus, 1758 | AS, OR | 1–3, 5–8, 11, 12, 15–19, 21, 25, 27 | OF, RF, FF (ll, bs) |
Testudinae | |||
Chelidae | |||
Phrynops geoffroanus (Schweigger, 1812) | AS | 3, 11, 16, 25 | OF, RF, DA, ST |
Among the habitats, open areas were the richest, with 35% of the amphibian and 25% of reptile species recorded. This habitat type was followed by dam and swamp for amphibians (26% both); and by fragment forest (22%) and riparian forest (13%) for reptiles. We also found some amphibians (e.g. Rhinella schneideri, Leptodactylus labyrinthicus, and Odontophrynus cultripes) and reptiles (e.g. Amphisbaena alba, Hemidactylus mabouia, Ameiva ameiva, and Tropidurus torquatus) in urban areas. For microhabitats, we recorded most amphibian richness in shrub (16%), bare soil (16%), and leaf litter (15%). The dominant reptile richness was found in leaf litter (30%).
Regarding the methods used, we captured specimens from all amphibian species using AS, while the PT registered 18% of amphibian species, and OR only 9%. Among the reptiles, AS was also the most efficient method, recovering 77% of the species, followed by OR (46%) and PT (11%). We registered 17 reptile species by the AS alone, seven by OR, and Typhlops brongersmianus was only registered by PT.
We found five populations of Dendropsophus elianeae throughout the TM region. Currently, this species is only known in the states of Mato Grosso, Mato Grosso do Sul, and São Paulo. Herein, we present the first record and a distribution map of D. elianeae in Minas Gerais State (Fig.
Geographical distribution of Dendropsophus elianeae. Literature records (black circle): Mato Grosso State in (1) Poconé (
Despite the high degree of anthropogenic disturbance in the study area (
Our study is the first to consider all reptiles (lizards, snakes, caimans, and freshwater turtles) in the TM region (
In fact, we found 35 additional species in the region compared to the previous survey. Therefore, we suggest that the checklist of the herpetofauna in the TM region is currently composed of 122 species (Suppl. material
During our field work, we made novel records of Dendropsophus elianeae (Fig.
The genus Ophiodes Wagler (1828) has a Neotropical distribution and problematic taxonomic history, mainly due to its highly cryptic diversity (e.g.
Bokermannohyla sazimai, Ololygon canastrensis, and Pithecopus azureus are classified as “data deficient” (DD) by
Herein, we recorded five other populations of P. moratoi in the interfluve of the Paranaíba River and Grande River, demonstrating the wide distribution of P. moratoi in Minas Gerais State. The specimens were found in forest patches that were altered by pasture and plantations, which indicates the resistance of P. moratoi to these type of habitat alterations; similar information was reported in other studies (e.g. Carvalho Jr. et al. 2010;
Finally, we elucidate the composition of the TM region’s herpetofauna, which is needed to understand local biodiversity and conservation strategies (
We are grateful to our partners Leonardo Gomes, Henrique Folly, Arthur Andrade, Fernando Martins, Mateus Montalvão, Rogério Vitor for their essential support during fieldwork. We would like to thank the CAPES which provides a PhD Scholarship to MON and LA and CNPQ to EAP. We also thank the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for issuing a collecting permission.
Specimens of anurans and reptiles collected at the Triângulo Mineiro region, State of Minas Gerais, Brazil: Ischnocnema sp. (gr. guentheri) (
Table S1. Amphibian and reptile species recorded in the TM region, State of Minas Gerais, Brazil
Data type: occurrence