Identification key for anuran amphibians in a protected area in the northeastern Atlantic Forest

Abstract

The identification of anuran amphibians is still a challenge in megadiverse assemblages. In the Neotropics, the Atlantic Forest harbors more than 600 anuran species, and many studies in this ecoregion report anuran assemblages surpassing 30 species. Taxonomic keys facilitate the identification of biological diversity, however only a few are available for anuran assemblages in the Atlantic Forest. Herein we present an identification key for 40 anuran species distributed across 20 genera and nine families, occurring in the Environmental Protection Area of Catolé and Fernão Velho, northeastern Atlantic Forest. Thirty-five morphological characteristics were used in the key, all of which can be easily observed in living and museum specimens. This pioneer study provides the first identification key for an amphibian assemblage in the northeastern Atlantic Forest and this baseline information acts as the starting point for the development of evolutionary and ecological research in this conservation unit.

Keywords Conservation Unit; Hotspot; Environmental Protection Area of Catolé and Fernão Velho; Dichotomous key; Taxonomic key

INTRODUCTION

To accurately identify a species, the first step is to assess the diversity of an area, which acts as the baseline for further ecological and evolutionary studies (e.g.,Narvaes & Rodrigues, 2009; Pereyra et al., 2016). Furthermore, species lists can be used for conservation purposes (ICMBio, 2018). The correct identification of a species can be facilitated when taxonomic keys are available. These tools use the diagnostic characteristics of species to guide the user, whose goal is to identify the lowest hierarchical level to which that individual belongs.

The identification of anuran amphibians in megadiverse assemblages is very challenging (Fouquet et al., 2007a; Cassini et al., 2013; Peloso et al., 2014, 2018; Taucce et al., 2018). Anurans display a great morphological similarity between species and cryptic species (those marked by pronounced morphological conservatism) are commonly found in this group (Camargo et al., 2006; Fouquet et al., 2007a, 2007b; Walker et al., 2018; Taucce et al., 2018). Additionally, the imprecise diagnostic characteristics for some species, along with a plethora of polymorphic traits hamper the accurate diagnosis of many taxa.

Despite the importance of taxonomic keys in facilitating the identification of biological diversity, these tools are still a greatly lacking for Neotropical anurans. For example, the Brazilian Atlantic Forest ecoregion harbors over 600 anuran species (Rossa-Feres et al., 2017), and currently there are only six available identification keys for adult anurans that are published in books or scientific journals (Eterovick & Sazima, 2004 for Serra do Cipó, Minas Gerais state; Loebmann, 2005 for the coastal region of southernmost Brazil, Rio Grande do Sul state; Ribeiro et al., 2005 for the Serra do Japí, São Paulo state; Kwet et al., 2010 for the Serra Gaúcha, Rio Grande do Sul state; Provete et al., 2011 for the northwest region of São Paulo state; and Pimenta et al., 2014 for the municipalities of Alvorada de Minas, Conceição do Mato Dentro and Dom Joaquim, Minas Gerais state). All these keys include anuran assemblages from the southern part of Atlantic Forest.

The aim of the present study was to develop an identification key for 40 anuran species occurring in the Environmental Protection Area of Catolé and Fernão Velho in the northeastern Atlantic Forest of Brazil.

MATERIAL AND METHODS

The elaboration of identification keys was based on adult anurans obtained in the Environmental Protection Area of Catolé and Fernão Velho (EPACFV), a conservation unit in the Northeastern Atlantic Forest. The area covers 37.12 km² and presents a mosaic of phytophysiognomies that vary from ombrophylous forest to mangroves (sensuAssis, 2000; Oliveira et al., 2014). All specimens were collected from 1994 to 2018 and are housed in the Herpetological Collection of the Museu de História Natural da Universidade Federal de Alagoas (MUFAL; ^{Appendix 1}).

The discrete characteristics followed the nomenclature proposed or modified from Myers & Duellman (1982), Heyer et al. (1990), Kwet & Di-Bernardo (1999), Kok & Kalamandeen (2008) and Napoli & Pimenta (2009). All specimens were analyzed using a Coleman^© NSZ 405 stereomicroscope. Additionally, the available literature for each species description was used.

The identification key was designed to separate species groups in a taxonomically inclusive manner, including family and genus level terminals wherever possible. The taxonomic nomenclature followed the current phylogenetic proposals (e.g.,Faivovich et al., 2005; De-Sá et al., 2014; Duellman et al., 2016). The key was tested by people with varying degrees of knowledge on anuran morphology, ranging from undergraduate biology students (not familiar with herpetology) to expert taxonomists of this group.

RESULTS AND DISCUSSION

A total of 280 adult specimens from 40 species of 20 genera and nine families of anurans (^{Appendix 1}) were obtained from EPACFV (Dubeux et al., 2020). Hylidae was the richest family with 19 species followed by Leptodactylidae (nine spp.), Bufonidae (four spp.), Microhylidae and Phyllomedusidae (two spp. each), Aromobatidae, Craugastoridae, Hemiphractidae and Odontophrynidae (one species each; Dubeux et al., 2020).

Thirty-five morphological characteristics were used in the key, as follows: 14 related to the presence/absence of structures, five related to shape, six related to proportion (size), nine related to color patterns, and one related to skin texture. The characteristics used can be easily observed in both living individuals or preserved specimens and apply to both sexes. Some of these traits may vary with ontogeny and defining characteristics were determined for adult individuals and thus, may not be easily applicable to juvenile individuals. Species terminals are highlighted in bold.

Taxonomic key for the anuran amphibians of Environmental Protection Area of Catolé and Fernão Velho, Alagoas state, northeastern Brazil

1a. Dorsum showing a warty or spiculate texture (Fig. 1A-B) Bufonidae 2

Figure 1
Discrete characters used in the identification key for the anuran amphibians occurring in the Environmental Protection Area of Catolé and Fernão Velho, Alagoas state, northeastern Brazil. Dorsal skin texture. (A) warty; (B) spiculate; (C) granular; (D) smooth; (E) shagreened; (F) tubercular.

1b. Dorsum showing a smooth, tubercular, shagreened or granular texture (Fig. 2C-F) 5

Figure 2
Discrete characters used in the identification key for the anuran amphibians occurring in the Environmental Protection Area of Catolé and Fernão Velho, Alagoas state, northeast Brazil. The details of characters are mentioned in the taxonomic key.

2a. (1a) Parotoid gland evident (Fig. 2A-white arrow); belly and digits showing homogeneous coloration Rhinella Fitzinger, 1826 3

2b. Parotoid gland not evident; yellowish-orange color distributed in points on the ventral portion of the thighs and on the most proximal digits Frostius pernambucensis (Bokermann, 1962)

3a. (2a) Square shaped snout in ventral view, extends past the end of the lower jaw (Fig. 2B); strongly keratinized cephalic crests Rhinella granulosa (Spix, 1824)

3b. Rounded shaped snout in ventral view, does not extend past the end of the lower jaw (Fig. 2C); poorly keratinized or non-keratinized cephalic crests 4

4a. (3b) Paracnemic gland present (Fig. 2A-black arrow); forearm and external foot glands developed; parotoid gland triangular-shape (Fig. 2D) Rhinella diptycha (Cope, 1862)

4b. Paracnemic, forearm and external feet glands absents; parotoid gland elliptical/elongate-shape (Fig. 2E) Rhinella crucifer (Wied-Neuwied, 1821)

5a. (1b) Fingertip dilated forming a disc (Fig. 2F) 6

5b. Fingertip not dilated (Fig. 2G) 28

6a. (5a) Presence of a black lateral band extending from the snout to the inguinal region (Fig. 2H) Aromobatidae: Allobates olfersioides (Lutz, 1925)

6b. Absence of a black lateral band 7

7a. (6b) Webbing absent between all toes 8

7b. Posterior webbing present between at least two toes 10

8a. (7a) Head shape longer than wide; pointed snout in dorsal view (Fig. 2I); dark band on supratympanic fold Craugastoridae: Pristimantis ramagii (Boulenger, 1888)

8b. Head shape wider than long; rounded or square snout in dorsal view (Fig. 2B or 2C); dark band on supratympanic fold absent Phyllomedusidae 9

9a. (8b) Toe II shorter than toe I (Fig. 2J) Pithecopus gonzagai Andrade et al., 2020

9b. Toe II longer than toe I Hylomantis granulosa (Cruz, 1989)

10a. (7b) Finger I longer than finger III (Fig. 2K) Hemiphractidae: Gastrotheca fissipes (Boulenger, 1888)

10b. Finger I shorter than finger III Hylidae 11

11a. (10b) Axillary membrane present (Fig. 2L) 12

11b. Axillary membrane absent 18

12a. (11a) Rounded shaped snout in dorsal view (Fig. 2C); tympanum diameter smaller than third finger disc diameter Dendropsophus Fitzinger, 1843 13

12b. Semicircular snout shape in dorsal view (Fig. 2M); tympanum diameter larger than third finger disc diameter Trachycephalus mesophaeus (Hensel, 1867)

13a. (12a) A light colored band anteriorly delimited from the snout to the intraorbital region and extending laterodorsally (Fig. 2N) 14

13b. Absence of a distinct light-colored band in intraorbital region 16

14a. (13a) Presence of light-colored spots on the dorsal surface of the thighs (Fig. 2O); light-colored dorsolateral bands joining in the posterior portion of the body Dendropsophus elegans (Wied-Neuwied, 1824)

14b. Absence of light-colored spots on the dorsal surface of the thighs; light-colored dorsolateral bands do not come together 15

15a. (14b) A distinct laterodorsal light-colored band extending to inguinal region (Fig. 3A) Dendropsophus oliveirai (Bokermann, 1963)

Figure 3
Discrete characters used in the identification key for the anuran amphibians occurring in the Environmental Protection Area of Catolé and Fernão Velho, Alagoas state, northeast Brazil. The details of characters are mentioned in the taxonomic key.

15b. A distinct laterodorsal light-colored band extending to the mid body (Fig. 3B) Dendropsophus haddadi (Bastos & Pombal, 1996)

16a. (13b) Presence of distinct white spot in suborbital region (Fig. 3C); distinct dorsal and dorsolateral coloration clearly delimited Dendropsophus branneri (Cochran, 1948)

16b. Absence of distinct white spot in suborbital region; similar dorsal and dorsolateral coloration 17

17a. (16b) Presence of discrete ulnar and carpal dermal fringe (Fig. 3D) Dendropsophus soaresi (Caramaschi & Jim, 1983)

17b. Absence of ulnar and carpal dermal fringe Dendropsophus minutus (Peters, 1872)

18a. (11b) Protruding snout in lateral view (Fig. 3E) Ololygon skuki (Lima, Cruz, & Azevedo, 2011)

18b. Rounded or truncated snout in lateral view (Fig. 3F or 3G) 19

19a. (18b) Palmar tubercle absent Boana Gray, 1825 20

19b. Palmar tubercle present (Fig. 3H) 23

20a. (19a) Calcar appendage present (Fig. 3I) 21

20b. Calcar appendage absent 22

21a. (20a) Sub-cloacal fold and prepolex absent Boana semilineata (Spix, 1824)

21b. Sub-cloacal fold and prepolex present (Fig. 3J) Boana albomarginata (Spix, 1824)

22a. (20b) Marked supratympanic fold extending to axillary region (Fig. 3k) Boana crepitans (Wied-Neuwied, 1824)

22b. Unmarked supratympanic fold extending posteriorly (Fig. 3L) Boana atlantica (Caramaschi & Velosa, 1996)

23a. (19b) Calcar appendage present (Fig. 3I) Scinax nebulosus (Spix, 1824)

23b. Calcar appendage absent 24

24a. (23b) Pointed-snout in dorsal view (Fig. 2I); a light-colored band anteriorly delimited on the intraorbital region and extending laterodorsally Scinax auratus (Wied-Neuwied, 1821)

24b. Rounded snout in dorsal view (Fig. 2C); absence of a distinct light-colored band on the intraorbital region 25

25a. (24b) Tympanic annulus distinct (Fig. 3M) 26

25b. Tympanic annulus indistinct (Fig. 3N) Phyllodytes edelmoi Peixoto, Caramaschi & Freire, 2003

26a. (25a) Presence of marbled spots on inguinal region and lateral of thighs (Fig. 3O) 27

26b. Absence of marbled spots on inguinal region and lateral of thighs Scinax eurydice (Bokermann, 1968)

27a. (26a) Pigmented ventral region (Fig. 4A); tympanum diameter larger than third finger disc diameter; snout length less than half of head length Scinax fuscovarius (Lutz, 1925)

Figure 4
Discrete characters used in the identification key for anuran amphibians occurring in the Environmental Protection Area of Catolé and Fernão Velho, Alagoas state, northeastern Brazil. The details of characters are mentioned in the taxonomic key.

27b. Unpigmented ventral region (Fig. 4B); tympanum diameter smaller than third finger disc diameter; snout length larger than half of head length Scinax x-signatus (Spix, 1824)

28a. (5b) Posterior webbing present between at least two toes; finger I shorter than finger II Microhylidae 29

28b. Webbing absent between all toes; finger I longer than finger II 30

29a. (28a) Presence of a post-cephalic fold projected anteriorly (Fig. 4C); interorbital distance is half the width of the body in the region of the forelimbs Dermatonotus muelleri (Boettger, 1885)

29b. Absence of post-cephalic fold; interorbital distance similar to the width of the body in the region of the forelimbs Chiasmocleis alagoana Cruz, Caramaschi & Freire, 1999

30a. (28b) Tympanic annulus indistinct (Fig. 3N) 31

30b. Tympanic annulus distinct (Fig. 3M) 33

31a. (30a) Truncated-snout in lateral view (Fig. 3G) Macrogenioglottus alipioi Carvalho, 1946

31b. Rounded-snout in lateral view (Fig. 3F) 32

32a. (31b) Supratympanic fold extending halfway down the body ventrally limited by a dark band (Fig. 4D) Physalaemus cuvieri Fitzinger, 1826

32b. Supratympanic fold and lateral dark band absent Pseudopaludicola mystacalis (Cope, 1887)

33a. (30b) Presence of longitudinal dorsal crests, extending from the supratympanic region to the inguinal region (Fig. 4E and 4F) 34

33b. Absence of longitudinal dorsal crests 36

34a. (33a) Only one pair of longitudinal crests willing dorsolaterally (Fig. 4E); black band extending laterally from the tip of the snout to the posterior region of the tympanum Leptodactylus mystaceus (Spix, 1824)

34b. More than one pair of longitudinal crests willing in back (Fig. 4F); no black band on the snout 35

35a. (34b) Pointed-snout in lateral view (Fig. 4G); dark interorbital spot in inverted triangle shape Leptodactylus fuscus (Schneider, 1799)

35b. Rounded-snout in lateral view (Fig. 3F); dark interorbital spot absent Leptodactylus macrosternum Miranda-Ribeiro, 1926

36a. (33b) Presence of marbled spots on gular and pectoral regions (Fig. 4H) 37

36b. Absence of marbled spots on gular and pectoral regions (Fig. 4I) 38

37a. (36a) Reddish coloration on lateral thigh and inguinal region (Fig. 4J) Leptodactylus vastus Lutz, 1930

37b. Indistinct coloration on lateral thigh and inguinal region Leptodactylus natalensis Lutz, 1930

38a. (36b) Tympanum diameter half the eye diameter; presence of semicontinuous tuberculous distinctly colored extending from the supratympanic fold to the inguinal region (Fig. 4K) Adenomera hylaedactyla (Cope, 1868)

38b. Tympanum diameter a little smaller to the eye diameter; absence of a distinct colored semicontinuous tuberculous Leptodactylus troglodytes Lutz, 1926

The Environmental Protection Area of Catolé and Fernão Velho contain important forest remnants in the state of Alagoas. Of the 40 species recorded, three are topotypical of this conservation unit (Chiasmocleis alagoana, Phyllodytes edelmoi and Ololygon skuki), four are currently considered threatened (Allobates olfersioides, Chiasmocleis alagoana, Hylomantis granulosa, and Ololygon skuki) and one species are lacking sufficient data for the assessment of their threatened status (Gastrotheca fissipes;Dubeux et al., 2020). This area represents one of the few forest remnants of the northeastern Atlantic Forest, with a long term herpetofauna survey and approximately 26 years of research led by different researchers.

This pioneer study provides the first identification key for an anuran assemblage in the northeastern Atlantic Forest. This study will certainly facilitate the identification of anurans in this Environmental Protection Area. Moreover, this baseline information can act as a starting point for the development of evolutionary and ecological research as well as providing a framework for the improved management of the fauna found in this conservation unit.

ACKNOWLEDGMENTS

The authors thank the Museu de História Natural da Universidade Federal de Alagoas for their support in research and the availability of material for studies; to the researchers L. Lima, J. Almeida, L. Correia, G. Rodrigues, I. Santos, B. Lisboa, A. Valencia-Aguilar, G. Ruano-Fajardo, E. Freire, M. Lima, N. Vieira, K. Vieira and G. Skuk (in memoriam) who through their commitment and dedication help and/or aid in the advancement of amphibian knowledge in the Alagoas state; to the Batalhão de Polícia Ambiental do Estado de Alagoas for the support in the field trips; MANEFAU LTDA., Instituto do Meio Ambiente do Estado de Alagoas, MJMD thanks FACEPE (IBPG-1117-2.04/19) and TM thanks CNPq (309904/2015-3 and 312291/2018-3) and FAPEAL for assistance in research and financial support.

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APPENDIX 1

Specimens examined.

AROMOBATIDAE

Allobates olfersioides: (n = 9) MUFAL 2325-26, 2684, 2687, 14148, 14183, 14192, 14195, 14250.

BUFONIDAE

Frostius pernambucensis: (n = 4) MUFAL 4273, 4278, 8048, 14262.

Rhinella crucifer: (n = 1) MUFAL14189.

Rhinella granulosa: (n = 12) MUFAL 3105, 3999, 8130, 14218-24, 14226-27.

Rhinella dypticha: (n = 4) MUFAL 14172, 14179-80, 14266.

CRAUGASTORIDAE

Pristimantis ramagii: (n = 9) MUFAL 2773-74, 7823, 8015, 14168, 14212, 14216-17, 14228.

HEMIPHRACTIDAE

Gastrotheca fissipes: (n = 6) MUFAL 4675, 5488, 14191, 14209, 14242, 14260.

HYLIDAE

Boana albomarginata: (n = 12) MUFAL 6132-33, 8348, 11020, 14143-44, 14157-60, 14247, 14249.

Boana atlantica: (n = 17) MUFAL 2500-04, 2696, 2698, 2705, 6729, 14145, 14181-82, 14198-99, 14206, 14253-54.

Boana crepitans: (n = 1) MUFAL 2353.

Boana semilineata: (n = 7) MUFAL 14188, 14190, 14255-59.

Dendropsophus branneri: (n = 10) MUFAL 8463, 8465-66, 8468, 14170-71, 14176, 14178, 14263-64.

Dendropsophus elegans: (n = 1) MUFAL 2912.

Dendropsophus haddadi: (n = 5) MUFAL 8799, 11014, 14211, 14213, 14232.

Dendropsophus minutus: (n = 4) MUFAL 5508, 5516, 5517, 5518.

Dendropsophus soaresi: (n = 3) MUFAL 8740, 8741, 9618.

Ololygon skuki: (n = 1) MUFAL 12390.

Phyllodytes edelmoi: (n = 7) MUFAL 14155-56, 14167, 14231, 14243, 14248.

Scinax auratus: (n = 4) MUFAL 14177, 14200, 14270-71.

Scinax eurydice: (n = 4) MUFAL 14185-86, 14197, 14201.

Scinax fuscovarius: Adults (n = 1) MUFAL 8759.

Scinax nebulosus: (n = 14) MUFAL 6407-09, 6413-15, 11868-70, 14142, 14165, 14175, 14214, 14261.

Scinax x-signatus: (n = 16) MUFAL 2424-29, 14164, 14166, 14173, 14202-03, 14205, 14272-75.

Trachycephalus mesophaeus: (n = 6) MUFAL 1982, 2117, 2151, 2193, 7362, 7363.

LEPTODACTYLIDAE

Adenomera hylaedactyla: (n = 12) MUFAL 3307, 3315, 3321-24, 3590, 3592, 4194, 14169, 14174, 14245.

Leptodactylus fuscus: (n = 11) MUFAL 2476-77, 8671, 14184, 14187, 14276-81.

Leptodactylus macrosternum: (n = 3) MUFAL 14153-54, 14265.

Leptodactylus mystaceus: (n = 7) MUFAL 4192, 8764, 14149, 14193-94, 14204, 14246.

Leptodactylus natalensis: (n = 15) MUFAL 2689-90, 6441-44, 6446-49, 14147, 14161-62, 14229, 14241.

Leptodactylus troglodytes: (n = 1) MUFAL 2946.

Leptodactylus vastus: (n = 6) MUFAL 14150, 14163, 14225, 14233-34, 14236.

Physalaemus cuvieri: (n = 13) MUFAL 3125, 3435, 3469, 3473, 3478, 3586, 3955, 3997, 4607, 6450, 14146, 14196, 14207.

Pseudopaludicola mystacalis: (n = 7) MUFAL 2513-16, 14267-69.

MICROHYLIDAE

Chiasmocleis alagoana: (n = 8) MUFAL 10963-67, 10969, 11274-75.

Dermatonotus muelleri: (n = 12) MUFAL 2567, 3316, 3392, 3398, 3439, 3447, 3476, 3585, 3591; 3938, 4007, 4008.

ODONTOPHRYNIDAE

Macrogenioglottus alipioi: (n = 20) MUFAL 5483-84, 5493-94, 8165-66, 10940-42, 14151-52, 14208, 14230, 14235, 14237-40, 14244.

PHYLLOMEDUSIDAE

Hylomantis granulosa: (n = 5) MUFAL 8486, 8798, 12106, 14210, 14215, 14252.

Pithecopus gonzagai: (n = 1) MUFAL 14251.

Edited by

• Edited by: Luís Fábio Silveira

Publication Dates

• Publication in this collection
  04 Oct 2021
• Date of issue
  2021

History

• Received
  02 Dec 2019
• Accepted
  11 July 2021