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NOTES ON GEOGRAPHIC DISTRIBUTION Check List 14 (2): 303-308

https://doi.org/10.15560/14.2.303

Advertisement call and new distribution records from Brazil of
Teratohyla midas (Lynch & Duellman, 1973) (Anura, Centrolenidae)

Kassio Castro Araujo,’ André Pansonato,? Rosa Hermina Oliveira,' Drausio Honorio Morais,’
Vinicius Tadeu Carvalho,* Robson Waldemar Avila! ?

1 Programa de Pés-Graduacao em Ecologia e Recursos Naturais, Bloco 902, Centro de Ciéncias, Universidade Federal do Ceara, Campus do PICI,
Av. Humberto Monte, s/n, CEP: 60455-760, Fortaleza, CE, Brazil. 2 Programa de Pés-Graduacao em Ecologia e Conservacao da Biodiversidade,
Instituto de Biociéncias, Universidade Federal de Mato Grosso, Avenida Fernando Correa da Costa 2367, Boa Esperang¢a, 78060-900 Cuiaba, MT,
Brazil. 3 Programa de Pés-Gradua¢ao em Bioprospec¢ao Molecular, Universidade Regional do Cariri, Campus do Pimenta, Rua Cel. Anténio Luiz,
1161, Bairro do Pimenta, Crato, Brasil. 4 Universidade Federal do Amazonas, Laboratorio de Evolucgao e Genética Animal, Av. Rodrigo Otavio
Jordéo Ramos, 3000, Mini-Campus Setor Sul, Manaus, AM, 69077-000, Brazil

Corresponding author: Kassio Castro Aratjo, kassio.ufpi@gmail.com

Abstract

Data on the distribution and calls of glassfrogs are important for taxonomic and conservation purposes. Herein, we
describe the acoustic parameters of 7eratohyla midas (Anura, Centrolenidae), with notes on distribution in the Brazil-
ian states of Acre, Amapa, Amazonas, and Para. The typical advertisement call of 7’ midas consists of a single pulsed
note, with 3 pulses emitted in a very short emission. The advertisement calls of 7. midas from Ecuador and French
Guiana are distinct from those reported here.

Key words
Glassfrogs, acoustic parameters, Amazon biome.

Academic editor: Raul Fernandes Dantas Sales | Received 21 October 2017 | Accepted 18 January 2018 | Published 9 March 2018

Citation: Araujo KC, Pansonato A, Oliveira RH, Morais DH, Carvalho VT, Avila RW (2018) Advertisement call and new distribution records
from Brazil of Teratohyla midas (Lynch & Duellman, 1973) (Anura, Centrolenidae). Check List 14 (2): 303-308. https://do1.org/10.15560/14.2.303

Introduction

Glassfrogs of the family Centrolenidae Taylor, 1951 cur-
rently comprises 151 species, distributed in 12 genera
(Frost et al. 2017). They are widely distributed in South
and Central America (Cisneros-Heredia and Mcdiarmid
2007), although only the genera Teratohyla, Vitreorana,
and Hyalinobatrachium have been recorded in Brazil
(Segalla et al. 2016). Thirteen species are known to occur
in Brazil: Hyalinobatrachium cappellei (Van Lidth de
Jeude, 1904), H. carlesvilai (Castroviejo-Fisher et al.,
2009), H. iaspidiense (Ayarzagiiena, 1992), H. mondolfi
(Sefiaris & Ayarzagtiena, 2001), H. munozorum (Lynch

& Duellman, 1973), Teratohyla adenocheira (Harvey
& Noonan, 2005), 7? midas (Lynch & Duellman, 1973),
Vitreorana baliomma (Pontes et al., 2014), V. eurygnatha
(Lutz, 1925), V. franciscana (Santana et al., 2015), V.
parvula (Boulenger, 1895), V. ritae (Lutz & Kloss, 1952)
and V. uranoscopa (Miller, 1924) (Segalla et al. 2016).
Data on the distribution and calls of glassfrogs are
important for taxonomic and conservation purposes (Cas-
troviejo-Fisher et al. 2011). However, advertisement calls
have been described for fewer than 25% of species of
glassfrog (Vargas-Salinas et al. 2015), and the geographic
distribution of many species 1s poorly documented. Tera-
tohyla midas 1s distributed in Brazil, Colombia, Ecuador,

Copyright Araujo et al. This isan 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.

304

Check List 14 (2)

Figure 1. Live specimen of Teratohyla midas from Primavera, Para, Brazil (voucher specimen UFMT 11543). Collection date: 18 December
2010. Elevation: 72 m. Snout—vent length: 18.35 mm.

French Guyana, and Peru (Lynch and Duellman 1973,
Marty and Gaucher 1999, Rodriguez et al. 2004, Cis-
neros-Heredia and McDiarmid 2005, Lynch 2005, Kok
and Castroviejo-Fisher 2008, May et al. 2008, Franca
and Venancio 2010, Catenazzi et al. 2013, Malambo et
al. 2013, Warren-Thomas et al. 2013). In Brazil, 7? midas
is recorded mainly in the Amazon region (Melo-Sampaio
and Oliveira 2013, Melo-Sampaio and Souza 2015);
moreover, it was recorded in the transitional area between
Amazon and Cerrado biome, in Maranhao state (Pontes
and Mattedi 2013).

The most conspicuous morphological characteristics
of 7: midas described by Lynch and Duellman (1973) are
not sufficient to distinguish centrolenid species from one
another (Cisneros-Heredia and McDiarmid 2007, Guayas-
amin et al. 2009). Therefore, we highlight the importance
of acoustic parameters to distinguish the Centrolenidae
species, because some morphological characters are
ambiguous with other centrolenids.

Analysis of acoustic parameters of 7! midas have
not been exhaustively studied. Advertisement calls of 7
midas from French Guyana (Marty and Gaucher 1999)
and Ecuador (Read 2000) were presented with oscil-
logram and spectrogram (Kok and Castroviejo-Fisher
2008). Herein we describe the acoustic parameters of 7°
midas with notes on its distribution in the Brazilian states
of Acre, Amapa, Amazonas, and Para.

Methods

The new records of Teratohyla midas from the states of
Acre, Amapa, and Amazonas were obtained from speci-
mens preserved in the collection of the Instituto Nacional
de Pesquisas da Amaz6nia (INPA; Manaus, Amazonas,
Brazil).

Additionally, on December 18, 2010, 2 specimens of
T! midas were captured on in municipality of Primavera,
Para state, Brazil. A permit to collect voucher species was
issued by the Secretaria de Estado do Meio Ambiente e
Recursos Naturais (SEMA/PA AU No. 1080/2010. Col-
lected specimens were photographed (Fig. 1), euthanized,
preserved in 70% ethanol, and deposited in the Colecao
Zoologica de Vertebrados, Universidade Federal de Mato
Grosso (UFMT; Cuiaba, Mato Grosso, Brazil).

Advertisement calls of individual of 7? midas
described here were recorded by Robson W. Avila with
a professional digital recorder Marantz PMD 660 with
an external directional microphone Yoga EM-9600 in
municipality of Primavera, Para state, Brazil. Digital
recordings were sampled at 44.1 kHz, with 16 bits reso-
lution and saved in uncompressed wave files. Recordings
were analyzed on a personal computer using Raven
Pro 1.3 (Bioacoustic Research Program 2012), with the
following settings: Hamming window function; Hann
window type; DFT size 256-point samples; brightness

Kassio et al. | Advertisement call and new distribution records of Teratohyla midas 305

yo eens

(2)
Colombia

)
Ecuador
oO

1.000
a a
Kilometers

Figure 3. Distribution map of Teratohyla midas. Red star: Type locality (Santa Cecilia, Province of Napo, Ecuador) (Lynch and Duellman
1973). Green circles: literature records of species from Colombia, Ecuador, French Guyana, Peru and Brazil (Acre, Amazonas, Maranhao,
and Rondonia states (Cisneros-Heredia and McDiarmid 2005, Kok and Castroviejo-Fisher 2008, May et al. 2008, Franga and Venancio 2010,
Catenazzi et al. 2013, Malambo et al. 2013, Melo-Sampaio and Oliveira 2013, Warren-Thomas et al. 2013, Pontes and Mattedi 2013, Rodriguez
et al. 2014, Twomey et al. 2014, Melo-Sampaio and Souza 2015). Yellow circles: new records of T. midas for Brazil (Acre, Amapa, Amazonas,

and Para states).

= 74%; contrast = 76%; time grid overlap = 50%. To
produce audiospectrograms and waveforms, we used
the R package “Seewave” (Sueur et al. 2008) and tuneR
(Ligges et al. 2014), with the following settings: FFT size
of 512 points, Hanning window, and 90% of overlap. The
following temporal parameters were measured manually
from the waveform: duration of note, pulse, inter-note
and inter-pulse intervals; number of pulses per note. Note
repetition rates were calculated per minute. The dominant
frequency was obtained from spectrograms. Terminology
for acoustic parameters follows Kohler et al. (2017). Calls
are archived in the Banco de Registros Bioacusticos,
housed at the Laboratorio de Herpetologia do Instituto
de Biociéncias da Universidade Federal de Mato Grosso
(LH; Cuiaba, Mato Grosso, Brazil), LH 403.

Results

New records (Fig. 2). Brazil: Para: municipality of
Primavera (00°56'25" S, 047°06'59" W, WGS84 datum,
72 m elev.), 18 December 2010, Robson W. Avila
(UFMT 11543, 11544). Amapa: municipality of Vitoria
do Jari (00°34'37" S, 052°04'40" W, WGS84 datum, 51 m

elev.), 20 December 2010, Vinicius T. Carvalho (INPA-H
30632, 30633, 30634). Acre: municipality of Porto Wal-
ter (08°40'39" S, 072°46'04" W, WGS84 datum, 215 m
elev.), 11 October 2010, Vinicius T. Carvalho (INPA-H
4647, 4758, 4766, 4767). Acre: municipality of Porto
Walter (08°22'50" S, 072°49'02" W, WGS84 datum,
229 m elev.), 12 October 2010, Vinicius T. Carvalho
(INPA-H 2591, 2592 INPA-H 2591, 2592). Amazonas:
municipality of Beruri (04°35'51" S, 061°53'30" W,
WGS84 datum, 59 m elev.), 20 November 2010, Vinicius
T. Carvalho (INPA-H 11531).

Identification. Our specimens match the descriptions of
7: midas by Lynch and Duellman (1973) and Guayasamin
et al. (2009). This species is morphologically differenti-
ated from another centrolenids by having liver covered
by a transparent hepatic peritoneum, digestive tract
white, ventral parietal peritoneum white anteriorly and
transparent posteriorly, prepollical spine not protruding
and the humeral spines lacking (Guayasamin et al. 2009).

The advertisement call of 7: midas (Fig. 3) consists of
a single pulsed note, with 3 pulses in a very short emis-
sion (Table 1). Series duration varies from 0.7 to 61.8 s

306

Amplitude
(dB)

Frequency (KHz)

Amplitude

0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7

Time (s)

Figure 2. Oscillogram (A) and audiospectrogram (B) of a single
pulsed note of Teratohyla midas, with 3 non-concatenated pulses
(voucher record LH 403, from specimen UFMT 11543, recorded on
18 December 2010, 20:20 h, air temperature 24.5°C, municipality of
Primavera, Para, Brazil).

(mean 13.2 + 15.5 SD). Duration of each note (or call)
varies from 0.087 to 0.1 s (mean 0.092 + 0.004 SD), inter-
note interval from 9.3 to 25.2 s (mean 13.3 + 3.9 SD),
and the rate of notes per minute from 2.4 to 6.4 (mean
5 + 1.1 SD). Duration of each pulse varies from 10 to
24 ms (mean 15 + 2.7 SD). Mean frequency band ranges
from 5843.3 Hz (+ 182.4 SD) to 8718.8 Hz (+ 124.54
SD). Dominant frequency varies from 6837.5 to 7125 Hz
(mean 7017.8 + 91.8 SD).

Discussion

Currently, new centrolenids species are discovered almost
yearly (e.g. Harvey and Noonan 2005, Cisneros-Heredia
and McDiarmid 2007, Castroviejo-Fisher et al. 2009,
Santana et al. 2015) and most of morphological characters
are ambiguous in this family (Guayasamin et al. 2009).
The white/transparent covering of the liver by the parietal
peritoneum is shared by 7: midas and T. spinosa (Taylor,
1949) and hepatic peritoneum and white digestive tract
are present in 3 species (7° amelie Cisneros-Heredia &
Meza-Ramos, 2007, 7. midas and T. pulverata Peters,
1873; Guayasamin et al. 2009). Teratohyla adenocheira
and 7: midas are sister species (Castroviejo-Fisher 2014),
but the first one has dermal glands along its fingers and
toes, the first toe noticeably much longer than other toes,
and in preservative, the dorsum is light gray with white
markings (Harvey and Noonan, 2005).

The advertisement calls of 7) midas from Ecuador
and French Guiana are distinct from those reported here.
Calls from Ecuador presented 4 pulses/call, while in
French Guiana and Brazil, they are composed of 3 pulses/
call. However, the third pulse has a longer duration in the
French Guyana population (Kok and Castroviejo-Fisher
2008) than the Brazilian specimen (this study).

Our record of 7. midas from the municipality of

Check List 14 (2)

Primavera was the first for Para state. This new record
extends the geographic distribution of 7’ midas by approx-
imately 900 km southeast from French Guyana (Kok and
Castroviejo-Fisher 2008) and 500 km north from the
nearest reported occurrence in Maranhao state (Pontes
and Mattedi 2013). Our new record of 7’ midas from the
municipality of Vitoria do Jari is approximately 3000 km
east from the type locality of the species and 1s the first
record for Amapa state. The nearest reported occurrences
are approximately 600 km north (Kok and Castroviejo-
Fisher 2008) and 650 km southeast (Pontes and Mattedi
2013). The 2 populations of T. midas in municipality of
Porto Walter, Acre state are about 200 and 150 km south
of previously known occurrences provided by Melo-
Sampaio and Souza (2015). Finally, the new record in the
municipality of Beruri, Amazonas state, is approximately
900 km north of the nearest reported occurrence in Vista
Alegre do Abuna, municipality of Porto Velho, Rond6nia
state (Melo-Sampaio and Oliveira 2013).

Recent studies have recorded 7’ midas at distinct
locations throughout the Amazon biome, in Acre (Melo-
Sampaio and Souza 2015), Rond6énia (Melo-Sampaio
and Oliveira 2013), and Amazonas (Fran¢a and Venancio
2010). Studies have also found it in the transitional area
between the Amazon and Cerrado in Maranhao (Pon-
tes and Mattedi 2013). There are also records in other
countries, such as Colombia (Malambo et al. 2013), Peru
(Twomey et al. 2014), and French Guyana (Kok and
Castroviejo-Fisher 2008), which emphasizes the impor-
tance of herpetological studies in the Amazon region for
finding new occurrences of glassfrogs.

Glassfrogs belonging to the tribe Cochranellini present
important morphological synapomorphies (Guayasamin
et al. 2009, Castroviejo-Fisher 2014). We observed that
the acoustic parameters of 7’ midas are distinct from other
centrolenids of the same tribe, such as Vitreorana ura-
noscopa, V. franciscana, Cochranella mache Guayasamin
& Bonaccorso, 2004 and C. nola Harvey, 1996 (Kohler et
al. 2006, Ortega-Andrade and Paucar 2013, Zaracho 2014,
Santana et al. 2015). Due to the lack of information, we
could not investigate differences in acoustic parameters
between 7: midas and T. adenocheira, its sister species.

Our analysis of acoustic parameters and physical
structure of [7 midas calls shows the possibility of a spe-
cies complex. The advertisement calls could be better to
distinguish cryptic species than morphology. Therefore,
we suggest that both molecular and bioacoustics studies
may provide important data to evaluate the taxonomic
status of distinct populations.

Acknowledgements

RWA thanks Conselho Nacional de Desenvolvimento
Cientifico e Tecnologico (CNPq) for providing a research
fellowship (PQ #303622/2015-6), the Coordena¢ao de
Aperfeigoamento de Pessoal de Nivel Superior for a
postdoctoral fellowships to AP and DHM (CAPES/PNPD
20132816 and 22005013001P4, respectively) and Secre-

Kassio et al. | Advertisement call and new distribution records of Teratohyla midas 307

taria de Estado do Meio Ambiente e Recursos Naturais
(SEMA) for the collection permit.

Authors’ Contributions

KCA and RHO wrote the manuscript with support from
AP, DHM and RWZ. VTC and RWA captured and iden-
tified the specimens. AP, KCA and RHO described the
advertisement call. All authors discussed the results and
contributed to the final manuscript.

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