Decarvalho 2013

Zootaxa 3701 (2): 207–237 ISSN 1175-5326 (print edition)
www.mapress.com /zootaxa /
Copyright © 2013 Magnolia Press
Article ZOOTAXA
ISSN 1175-5334 (online edition)
http://dx.doi.org/10.11646/zootaxa.3701.2.5
http://zoobank.org/urn:lsid:zoobank.org:pub:0C1F0871-E211-4BE4-9892-84B1E715B52C
Taxonomic circumscription of Adenomera martinezi (Bokermann, 1956)

(Anura: Leptodactylidae: Leptodactylinae) with the recognition of
a new cryptic taxon through a bioacoustic approach
THIAGO RIBEIRO DE CARVALHO1,2,3 & ARIOVALDO ANTONIO GIARETTA1

1Laboratório de Taxonomia, Sistemática e Ecologia Comportamental de Anuros Neotropicais. Faculdade de Ciências Integradas do
Pontal, Universidade Federal de Uberlândia (UFU), Rua 20, 1600, 38304-402, Ituiutaba, Minas Gerais, Brasil
2Programa de Pós-Graduação em Biologia Comparada, Universidade de São Paulo, Departamento de Biologia/FFCLRP. Avenida
dos Bandeirantes, 3900, 14040-901, Ribeirão Preto, São Paulo, Brasil

3Corresponding author. E-mail: thiago_decarvalho@yahoo.com.br
Abstract
In this paper, we provide a taxonomic circumscription of Adenomera martinezi from its type locality (Cachimbo, south-
western State of Pará) since its description (57 years ago) based on a newly collected series of eleven adult topotypes, and
through a bioacoustic approach, recognize an undescribed cryptic taxon under this nominal species, which is widely dis-
tributed in central and northern Brazil. Adenomera martinezi and Adenomera saci sp. nov. can be diagnosed from all con-
geners by their distinctive 4–6 symmetrically arranged rows of longitudinal dark-colored spots on dorsum. They differ
from each other through advertisement call structure, pulsed in Adenomera martinezi (audibly pulsed to the human ear),
and non-pulsed in Adenomera saci sp. nov. (a whistle to the human ear). The recognition of Adenomera saci sp. nov. has
conservation implications. Based on our assumed distribution of A. martinezi and Adenomera saci sp. nov., the IUCN con-
servation status of A. martinezi requires a reassessment, inasmuch as we herein reconsider this species, as far as we know,
as endemic to Cachimbo, southwestern State of Pará, Brazil. The 2004 extinction risk assessment included both A. mar-
tinezi and Adenomera saci sp. nov., and the conservation status category of ‘Least Concern’ might only be applied to Ad-
enomera saci sp. nov., a widely distributed and abundant species in central and northern Brazil.
Key words: Adenomera saci sp. nov., Cachimbo, Chapada dos Veadeiros, Cerrado, Conservation status, taxonomy
Introduction
The species is a widely used and fundamental unit of analysis in biology, although species concepts and delineation
of species boundaries is a longstanding biological and philosophical issue (Dayrat 2005; de Queiroz 2007; Vences
& Wake 2007). The problem of species delineation and identification can be exemplified by groups that exhibit
little morphological variation (Jaiswara et al. 2012), the so-called cryptic species. Bickford et al. (2007)
extensively discussed definitions and applicability of this term, being defined as typically closely related species
that are very similar and difficult to distinguish morphologically. Integrative taxonomy has been proposed as a
framework to bring together conceptual and methodological developments, employing non-morphological suites of
characters, as molecular phylogenetics and bioacoustics, for the unraveling of taxonomic complexity and
uncovering undetected diversity under cryptic species complexes (Heyer et al. 1996; Padial & De la Riva 2009;
Glaw et al. 2010; Padial et al. 2010).
Frogs have species recognition and mate choice systems that rely on non-morphological characteristics
(advertisement calls), and might harbor a great cryptic diversity (Bickford et al. 2007). Integrating independent
lines of evidence to proper address underlying unresolved taxonomic complexity might, thereafter, lead to
elucidation of biological identities in Adenomera, uncovering an expected cryptic diversity within this group of
frogs, whose comprising taxa share general morphology relatedness, and for which complementary datasets (e.g.
acoustic, molecular) are often needed for taxonomic resolution (Heyer 1984; Angulo & Icochea 2010).
Accepted by M. Vences: 24 Jul. 2013; published: 19 Aug. 2013 207

The genus Adenomera Steindachner currently comprises 15 recognized species distributed throughout South
America east of the Andes (Frost 2013). Several studies have revised and discussed the definition and phylogenetic
position of Adenomera, as well as the interrelationships of its comprising taxa. Historically, Lutz (1930) was the
first author to assemble Adenomera species at a lower rank under Leptodactylus, the subgenus Parvulus:
Leptodactylus (Parvulus) trivittatus (see Lutz 1926), currently under A. marmorata (Heyer 1973), and L.
(Parvulus) nanus Müller. Subsequently, Parker (1932) claimed that the older available name Adenomera had
priority, and proposed its use as a subgenus of Leptodactylus instead of Parvulus, and Parker (1935) reallocated A.
marmorata Steindachner to Leptodactylus (L. marmoratus). Heyer (1969a) followed Parker’s nomenclatural
rearrangements, and assigned the subgenus Adenomera to members of the L. marmoratus species group, both L.
marmoratus (Steidachner) and L. hylaedactylus (Cope) being included in the same group by Heyer (1969b); and
Heyer (1973) assigned three additional species [L. andreae Müller, L. bokermanni Heyer, and L. martinezi
Bokermann]. Heyer (1974a) resurrected the genus Adenomera, and recovered Adenomera + Lithodytes (imbedded
with Leptodactylus discodactylus) as sister group of the remaining Leptodactylus taxa. While there have been
additional subsequent studies, the phylogenetic position of Adenomera is still disputed based upon different lines of
evidence (external morphology, osteology, molecular biology, natural history), with two current hypotheses: i)
corroboration of the preferred phylogenetic relationship hypothesis in Heyer (1974a), placing Adenomera +
Lithodytes as sister group of Leptodactylus in the narrow sense (Frost et al. 2006; Ponssa 2008; Ponssa et al. 2010),
in spite to the phylogenetic position and generic status of Leptodactylus discodactylus (including other generic
combinations, under Lithodytes and Vanzolinius; see Heyer 1974a, b; Heyer 1998; De Sá et al. 2005; Ponssa 2008;
Pyron & Wiens 2011); rendering its comprising taxa (L. marmoratus group) paraphyletic in relation to
Leptodactylus, nested within the L. fuscus group (Heyer 1998), or placed as a subset of this species group (Giaretta
et al. 2011). It worth stressing that Frost et al. (2006) changed the generic statuses of Adenomera and Lithodytes,
synonymizing the former with the latter, which was ranked as a subgenus of Leptodactylus in an endeavor to avoid
a potential paraphyly based on Heyer’s (1998) and Kokubum and Giaretta’s (2005) evidence, discussed earlier. The
two most recent phylogenetic studies (Pyron & Wiens 2011; Fouquet et al. 2013) recovered the genera Lithodytes
and Adenomera as consisting of the sister clade of Leptodactylus in the narrow sense as well. In this respect,
Fouquet et al. (2013) tested the phylogenetic position of Adenomera martinezi, which was recovered within the
genus Adenomera, corroborating the first proposition of generic reallocation of Leptodactylus martinezi
(Bokermann, 1956) to Adenomera (Heyer 1974a). Thus, we assign the new species of the study to this genus as
well, assuming a putative close relationship between both taxa.
Bokermann (1956) described Adenomera martinezi (as Leptodactylus martinezi) from Cachimbo,
southwestern State of Pará, based on two adult specimens (holotype and allotype) collected in January 1955. This
name has subsequently been applied to several non-topotype populations of central and northern Brazil (Heyer
1973; Vitt et al. 2005; Silva Jr. et al. 2009; Kopp et al. 2010). We visited the type locality of A. martinezi 57 years
later and succeeded in obtaining a newly collected series of adult topotype specimens, as well as recording its
previously unknown advertisement call. In this paper, we bring forward the taxonomic circumscription of
Adenomera martinezi, as well as the description of its advertisement call, and through a bioacoustic approach, we
recognize an undescribed cryptic taxon previously subsumed under this nominal species.
Material and methods
Specimens and vocalizations of Adenomera martinezi were obtained at its type locality: Campo de Provas
Brigadeiro Velloso (9°22'S, 54°54'W; approximately 440 m a.s.l.), Cachimbo, Municipality of Novo Progresso,
southwestern State of Pará, northern Brazil. Specimens and/or vocalizations of the new species were obtained at
four sites in central Brazil: i) Chapada dos Veadeiros (14°10'S, 47°47'W; approximately 1030 m a.s.l.),
Municipality of Alto Paraíso de Goiás, State of Goiás; ii) Municipality of Cristalina (16°43'S, 47°33'W;
approximately 1095 m a.s.l.), State of Goiás; iii) Municipality of Pontal do Araguaia (15°58'S, 52°17'W;
approximately 320 m a.s.l.), State of Mato Grosso; and iv) Municipality of Alto Araguaia (17°22'S, 53°13'W;
approximately 730 m a.s.l.), State of Mato Grosso.
A sample of five tadpoles was collected in Cristalina (State of Goiás) in February 2013. Tadpoles were found
within shallow pools (2 cm deep) with standing water on a rocky bed at a site with scattered short grass-like
vegetation (< 30 cm tall). The new species was the only calling frog species at this study site (N = 3 fieldtrips).
208 · Zootaxa 3701 (2) © 2013 Magnolia Press CARVALHO & GIARETTA
Three tadpoles were preserved and two were raised in laboratory, one of them almost metamorphosed (Gosner’s
stage 41; well-developed hind limbs). As the general morphology of the tadpoles are in accordance with the
expected morphology for exotrophic tadpoles of Adenomera (De la Riva 1995), given that it is the only species of
this genus in the area, and that the foot features of these larvae are in compliance with those of adult specimens, we
assume that the collected sample represents tadpoles of the new species.
Type specimens and additional examined specimens (Appendix 1) are housed in the following Brazilian
zoological collections: Coleção de Anuros do Museu de Biodiversidade do Cerrado, Universidade Federal de
Uberlândia (AAG-UFU), Uberlândia, State of Minas Gerais; Coleção Herpetológica da Universidade de Brasília
(CHUNB), Brasília, Distrito Federal; Museu de Zoologia da Universidade de São Paulo (MZUSP), São Paulo,
State of São Paulo; Museu de Zoologia da Universidade Estadual de Campinas (ZUEC), Campinas, State of São
Paulo; Museu Nacional do Rio de Janeiro (MNRJ), Rio de Janeiro, State of Rio de Janeiro.
Twelve morphological measurements were taken by T.R.C from adult specimens using a micrometric ocular
piece coupled to a stereomicroscope; snout-vent length (SVL) was measured with calipers to the nearest 0.1 mm
under a stereomicroscope. Nine measurements followed Duellman (1970): snout-vent length (SVL), head length
(HL), head width (HW), eye diameter (ED), tympanum diameter (TD), eye-nostril distance (END) (= snout
length), internarial distance (IND), shank length (SL) (= tibia length), and foot length (FL). Four measurements
followed Heyer et al. (1990): hand length (HAL), forearm length (FRL), thigh length (TL), and tarsus length
(TSL). Head shape terminology followed Heyer et al. (1990). Five morphometric characters were measured from a
single tadpole using a micrometer ocular piece coupled to a stereomicroscope: interorbital distance (IOD);
internarial distance (IND), tail muscle height (TMH), maximum tail height (MTH), and tail muscle width (TMW);
three morphometric characters were measured with calipers to the nearest 0.1 mm under a stereomicroscope: total
length (TL), body length (BL), and tail length (TAL). Measurement standards followed Altig (2007);
morphological nomenclature followed Altig and McDiarmid (1999), and Altig (2007); larval staging followed
Gosner (1960). Pictures of both live and preserved specimens were slightly edited to remove flash shadows caused
by camera.
Vocalizations were recorded using digital equipment (M-Audio Microtrack II, Marantz PMD 670, Marantz
PMD 671) set at a sampling rate of 48.0 kHz and a 16-bit resolution, coupled to directional microphones
(Sennheiser K6/ME66 or K6/ME67). Calls were analyzed on a personal computer with Windows XP Professional
operating system using the software Raven Pro version 1.5, 64-bit version (Bioacoustics Research Program 2012).
Temporal variables were measured from audiospectrograms; dominant frequency was obtained in the software
(Peak Frequency measurement function). Raven Pro settings: window type = Hanning; window size = 256
samples; brightness = 50%; contrast = 50%; overlap = 85%; DFT size = 256 samples; grid spacing = 188 Hz.
Sound figures were obtained using Seewave version 1.6.4 package (Sueur et al. 2008) of the R platform version
2.15.1, 64-bit version (R Development Core Team 2012). Seewave settings: window name (Fourier transform
window) = Hanning; window length = 256 samples; overlap = 85%. Bioacoustic terminology mostly followed
Duellman and Trueb (1994). Given that the advertisement calls of the present study presented either the first
(fundamental) or the second harmonic as the dominant frequency (sensu Duellman & Trueb 1994), we opted to
refer to both the first and second harmonic frequencies as ‘peaks of sound energy’, consisting of the peaks of
greatest sound energy emphasized in both harmonics obtained in the software of bioacoustics analysis. Total mean
values of bioacoustic variables (mean and standard deviation) given in the advertisement call sections and tables
were obtained from mean individual values due to different call samples for each recorded individual, an approach
to try to reduce any bias from differential individual call samples, whereas the range of values encompassed the
minimum and maximum values of all analyzed call samples. Detailed information on figured sound files are
summarized in Appendix 2. Voucher specimens: Adenomera martinezi—AAG-UFU 1515–1520 (Cachimbo, Pará);
Adenomera sp. nov.—AAG-UFU 0109 (Chapada dos Veadeiros, Goiás); AAG-UFU 0809, 1761 (Cristalina,
Goiás); AAG-UFU 0208 (Pontal do Araguaia, Mato Grosso).
The overall thermal dependency of temporal variables of the advertisement calls of Adenomera martinezi and
Adenomera sp. nov. was tested via principal component analysis (PCA) using Fitopac 2.1 (Shepherd 2010) from
mean individual values to understand the interactions between sound variables. Then, a multiple correlation
analysis on the first component scores was performed using Systat 10.2 (Wilkinson 2000) to identify potential
temperature-dependent variables. Air temperature, mean individual values of the temporal variables of Adenomera
martinezi and Adenomera sp. nov. advertisement calls and their respective first principal component scores are
summarized in Appendix 3. This statistical approach was not likewise applied to calling male size (SVL)
dependency of spectral variables (peaks of sound energy) of the advertisement calls of both taxa due to the lack of
TAXONOMIC CIRCUMSCRIPTION OF ADENOMERA MARTINEZI Zootaxa 3701 (2) © 2013 Magnolia Press · 209
either a minimum sample of voucher males or a non-correspondence of voucher males and recordings. A second
PCA of temporal and spectral bioacoustic variables of Adenomera sp. nov. populations was performed on a
correlation matrix. The analysis was performed on log10-transformed variables. Eigenvectors, eigenvalues and
variation explained along the first three principal components are summarized in Appendix 4.
Bioacoustic data of Adenomera species were extracted from their original descriptions, or additional studies/
unpublished doctoral theses. Several works present bioacoustic data of Adenomera species, yet we made an effort
to only make use of bioacoustic variables from topotype specimens or information available from the nearest point
to type localities, so as to make unequivocal comparisons with respect to A. martinezi and the new species,
inclusive of bioacoustic diagnoses, since we faced several species identity problems in literature, with populations
either unassigned to a nominal species or under uncertain taxonomic status. Comparative bioacoustic variables and
their respective sources are listed in Table 3.
Results
Taxonomic accounts
Redescription of Adenomera martinezi (Bokermann)
Leptodactylus martinezi Bokermann, 1956: Type locality: Cachimbo (9°22'S, 54°54'W), southwestern Pará, Brazil.
Revised diagnosis. Adenomera martinezi is assigned to the genus (L. marmoratus species group and Adenomera
genus definitions; sensu Heyer 1973, 1974, respectively) by the following set of characters: 1) small body size (up
to 34.1 mm; sensu Kok et al. 2007); 2) toes lacking fringing or webbing; 3) adult males lacking thumb spines; 4)
first and second fingers of approximately equal length. Adenomera martinezi is diagnosed from the other 14
species of Adenomera by the following combination of characters: 1) presence of 4–6 symmetrically arranged rows
of longitudinal dark-colored spots on dorsum; 2) medium-sized species (adult male SVL 21.9–24.2 mm); 3)
vertebral pin-stripe always present; 4) toe tips unexpanded and unflattened; 5) long advertisement call (63–151 ms)
with 15–21 pulses (audibly pulsed to the human ear).
Comparison with other species. Adenomera martinezi can be diagnosed from all congeners by its distinctive
4–6 symmetrically arranged rows of longitudinal dark-colored spots on dorsum (figs. 1, 2A).
Adenomera martinezi (adult male SVL 21.9–24.2 mm; Table 1) can additionally be diagnosed from A.
ajurauna, A. araucaria, and A. nana (combined adult male SVL 16.3–20.0 mm; Kwet & Angulo 2002; Kwet 2007;
Berneck et al. 2008) by its larger size, and from A. lutzi and A. simonstuarti by its smaller size (combined adult
male SVL 25.9–34.1 mm; Kok et al. 2007; Angulo & Icochea 2010). Adenomera martinezi always has a vertebral
pin-stripe, whereas no specimens of A. bokermanni (Heyer 1973), A. engelsi (Kwet et al. 2009), and almost no
specimens of A. andreae (Heyer 1973) do. Adenomera martinezi is diagnosed from A. thomei by not presenting a
mask-like pattern on the inverted triangle of the interorbital region (Almeida & Angulo 2006). Adenomera
martinezi has neither expanded nor flattened toe tips, whereas specimens of A. andreae, A. marmorata, and A. nana
do (Heyer 1973; Kwet 2007); from A. lutzi, by lacking tubercles on forearms, posterior surface of thighs black with
distinct yellow, orange or red spotting or mottling, and males with yellow to orangish yellow throat and belly
(Heyer 1975; Kok et al. 2007).
The advertisement call (fig. 3; Tables 2–3) distinguishes Adenomera martinezi from A. ajurauna, A. engelsi, A.
heyeri, A. lutzi, and A. nana, by possessing a pulsed call structure (non-pulsed structure in all aforementioned
comparative species). Adenomera araucaria was reported to possess calls with 5–11 severe amplitude modulations
(see Kwet & Angulo 2002), and A. simonstuarti to possess 3–4 pulse-like, strong amplitude modulations (see
Angulo & Icochea 2010), whereas A. martinezi calls possess 15–21 pulse calls (see fig. 3); from A. andreae, A.
hylaedactyla, and A. lutzi (combined value range 16–62 ms) by a longer call duration (63–151 ms); from A.
marmorata (dominant frequency 4.50–5.60 kHz), as well as A. andreae, A. diptyx, A. nana, and A. thomei
[combined value range: 2.15–3.05 kHz (1st harmonic); 4.20–5.56 kHz (2nd harmonic)] by lower peaks of sound
energy [1.88–2.06 kHz (1st harmonic); 3.38–4.13 kHz (2nd harmonic)]; from A. andreae, A. coca, and A.
hylaedactyla (combined value range 2–15 pulses/call) by a greater number of pulses per call (15–21 pulses/call).
FIGURE 1. Live adult topotype specimens (Cachimbo, Pará) of Adenomera martinezi: (A) Voucher male AAG-UFU 1517
(SVL 23.7 mm); (B) Voucher male AAG-UFU 1515 (SVL 23.7 mm); (C) Voucher male AAG-UFU 1516 (SVL 24.2 mm); (D).
Voucher male AAG-UFU 1520 (SVL 21.9 mm); (E) Male AAG-UFU 1522 (SVL 23.5 mm); (F) Female AAG-UFU 1521
(SVL 25.7 mm).
Description. Reference specimen: AAG-UFU 1517 (figs. 1A, 2A–B, 4), adult male. Body slender in dorsal
view. Snout pointed in dorsal view (fig. 4A), acuminate in lateral view (fig. 4B). Snout tip with a well-developed
shovel-like fleshy ridge. Nostrils positioned dorsolaterally, closer to snout tip than to eyes; canthus rostralis
indistinguishable; loreal region concave; upper eyelids smooth. Supratympanic folds extending from posterior
margin of eyes, passing over tympani, and extending to base of arms. A discrete, elongated post-commissural
gland. Vocal sac subgular, internal. Vocal slits present; vomerine teeth in two straight rows posterior to choanae;
tongue elongated, free behind. Relative finger lengths I ~ II ~ IV < III; finger tips rounded, not expanded, and with
no webbing or fringing. Inner metacarpal tubercle elongated; outer metacarpal tubercle nearly rounded (fig. 4D);
subarticular and supernumerary tubercles rounded. No thumb asperities. Posterior half of dorsum glandular; dorsal
surface of shanks, and dorsal and posterior surfaces of tarsi covered with minute tubercles. Vertebral pin-stripe
present. Four longitudinal rows of symmetrically arranged spots. Flanks with longitudinal granular rows from
posterior half of body towards groin. Throat and belly smooth. Ventral surface of thighs areolate. Posterior surface
of thighs striped. Relative toe lengths I < II < V ~ III < IV; toe tips rounded, not expanded (pointed toe tips:
character state A; see fig. 1A in Heyer 1973); toes ridged laterally, with no webbing. Inner metatarsal tubercles
ovoid, outer conical (fig. 4C); subarticular and supernumerary tubercles rounded. Tarsal folds extending from inner
metatarsal tubercle to 1/2 length of tarsi, ending in a very slightly enlarged tubercle. Heel smooth.
FIGURE 2. Dorsal (A) and ventral (B) views of an adult male topotype of Adenomera martinezi (AAG-UFU 1517; SVL 23.7
mm); and dorsal (C) and ventral (D) views of the holotype of Adenomera saci sp. nov. (AAG-UFU 1339; SVL 22.5 mm).
Coloration in alcohol (figs. 2A–B). Faded white shovel-like fleshy ridge on snout tip. Tympani reddish
brown. Upper jaw with sinuous cream-colored stripes, and a white-colored post-commissural gland. Dorsum with
four longitudinal rows of symmetrically arranged black spots on a very dark brown background, some portions
faded gray. Flanks with cream-colored longitudinal row of granules on a light gray background. Green-colored
vertebral stripe with some portions faded. White-tipped tubercles scattered on posterior half of dorsum, dorsal
surface of shanks, and dorsal and posterior surfaces of tarsi. Dorsal surface of limbs with black stripes/blotches on
a brownish gray background. Throat, belly, and ventral limb surfaces cream, with melanophores, but no distinctive
color pattern. Posterior surface of thighs with cream-colored and black longitudinal stripes.
Coloration in life (fig. 1A). Iris bronze, upper eyelids bordered by an ill-outlined silver stripe. Tympani
reddish brown. Dorsum with black longitudinal rows of spots on a moss green background. Spots and blotches on
lateral of head and flanks with a whitish silver coloration. Flanks with orange longitudinal granular rows on a
medium brown background. Vertebral stripe cream, with some portions tending toward an orange coloration.
Dorsal surface of limbs with black stripes/blotches on a golden or moss green background. Throat and ventral
surface of limbs cream, belly uniformly yellow.
Variation. Morphometric variation is summarized in Table 1. Variation within the topotype series is restricted
to dorsal texture (smooth or glandular), and color pattern (medium gray to very dark brown background); the four
to six longitudinal rows of symmetrically arranged black spots are variable due to the dorsal coloration, which
might become evident or barely indistinguishable in preserved specimens. Posterior surface of thighs vary from a
spotted or mottled pattern, which can form ill-defined and fragmented stripes (AAG-UFU 1515, 1522–1523, 1525)
or a well-defined striped pattern (AAG-UFU 1516, 1518–1520, 1524). All specimens (except the female AAG-
UFU 1521) have a well-defined faded white shovel-like fleshy ridge. Specimens in life presented some variation
with respect to coloration, such as dorsal coloration (light gray/medium brown to moss green/dark brownish gray),
vertebral stripe (cream to golden), granular rows on flanks (pale yellow to orange) (fig. 1).
Description of female. Reference specimen: AAG-UFU 1521 (fig. 1F), adult female. Body robust in dorsal
view. Snout sub-acuminate in dorsal view, acuminate in lateral view. Snout tip lacks a well-developed shovel-like
fleshy ridge. Nostrils closer to snout tip than to eyes; canthus rostralis indistinguishable; loreal region concave;
upper eyelids smooth. Supratympanic folds extending from posterior margin of eyes, passing over tympani, and
extending to base of arms. A discrete, elongated post-commissural gland. Vocal sac and vocal slits absent;
vomerine teeth in two straight rows posterior to choanae; tongue elongated, free behind. Relative finger lengths I <
II ~ IV < III; finger tips rounded, not expanded, and with no webbing or fringing; inner metacarpal tubercle
elongated; outer metacarpal tubercle nearly rounded; subarticular and supernumerary tubercles rounded. No thumb
asperities. Dorsum smooth; dorsal surface of shanks, and posterior surface of tarsi with minute tubercles. Vertebral
pin-stripe present. Four longitudinal rows of symmetrically arranged spots. Flanks with longitudinal granular rows
from posterior half of body towards groin. Throat and belly smooth. Ventral surface of thighs areolate. Posterior
surface of thighs mottled, forming ill-defined stripes. Relative toe lengths I < II < V < III < IV; toe tips rounded, not
expanded (pointed toe tips: character state A; see fig. 1A in Heyer 1973); toes ridged laterally, with no webbing.
Inner metatarsal tubercles rounded, outer conical; subarticular and supernumerary tubercles rounded. Tarsal folds
extending from inner metatarsal tubercle to almost the entire length of tarsi, ending in a very slightly enlarged
tubercle. Heel smooth.
Coloration in alcohol of the female. Upper jaw with sinuous cream-colored stripes. Tympani reddish brown.
Dorsum with longitudinal rows of black spots on a gray background. Flanks with cream-colored row of granules on
a light gray background. Cream-colored vertebral stripe. White-tipped tubercles scattered on the dorsal surface of
shanks, and posterior surface of tarsi. Dorsal surface of limbs with black stripes/blotches on a brownish gray
background. Posterior surface of thighs mottled, with cream and dark-colored spots/blotches, forming ill-defined
cream longitudinal stripes. Throat, belly, and ventral surface of limbs cream-colored, with melanophores, but with
no distinctive color pattern.
Coloration in life of the female (fig. 1F). Iris bronze, upper eyelids bordered by an ill-outlined bluish silver
stripe. Tympani reddish brown. Dorsum with black longitudinal rows of spots on a grayish brown background.
Flanks with golden/yellow longitudinal granular rows on a grayish brown background. Vertebral stripe cream, with
some portions tending to an orange coloration. Dorsal surface of limbs with black stripes/blotches on a golden or
grayish brown background. Throat and ventral surface of limbs cream, belly uniformly yellow.
FIGURE 3. Advertisement call of two male topotypes (Cachimbo, Pará) of Adenomera martinezi. (A) A waveform section (2
seconds) with five calls; (B) Audiospectrogram (ab(ove) and respective oscillogram (below) of the fourth call highlighted by a
red outline. Voucher specimen: AAG-UFU 1517; (C) A waveform section (2 seconds) with five calls; (D) Audiospectrogram
(above) and respective oscillogram (below) of the second call highlighted by a red outline. Unvouchered recording.
FIGURE 4. Adenomera martinezi, adult male topotype re-described (AAG-UFU 1517). Dorsal (A) and lateral (B) views of
head, and ventral views of foot (C) and hand (D).
Advertisement call. Fifteen males recorded (N = 750 calls analyzed). Voucher topotypes (figs. 1A–D).
Advertisement call (fig. 3; Table 2) consists of a pulsed (audible to the human ear) signal with deep and regular
amplitude modulation. Calls have up to 6 visible harmonics and possess no or a very slight ascendant frequency
modulation along their extent. Calls have 15–21 pulses (mean 18.3, SD = 1.3), and are emitted at a rate of 1–3
calls/second (mean 2.1; SD = 0.3), and at a rate of 97–142 calls/minute (mean 121.7; SD = 15.2). Call duration
varies from 63–151 ms (mean 116.8; SD = 11.4), and intercall interval from 200–1000 ms (mean 391.2; SD =
80.2). Dominant frequency coincides with either the first (60%) or the second harmonic (13%) among the recorded
individuals, or can alternate between the first and second harmonics (27%) among analyzed calls of the same
individual. Peak of sound energy varies from 1.88–2.06 kHz (mean 1.93 kHz; SD = 0.08) in the first harmonic,
and/or from 3.38–4.13 kHz (mean 3.74 kHz; SD = 0.18) in the second harmonic. The other harmonics, if present,
are increasingly weaker in sound energy.
Natural history. Adenomera martinezi occurs in grassy field environments associated with rock outcrops in
sandy/muddy soil. Males call within underground chambers or from exposed calling sites, most times among
grassy tufts. The species was heard only after nightfall.
Geographic distribution. Adenomera martinezi is known only from its type locality (Cachimbo, southwestern
State of Pará, Brazil), a transitional Cerrado/Amazonian region (see Bokermann 1956).
Remarks. Bokermann (1956) stated that Adenomera martinezi had a very large tongue, occupying almost the
entire mouth, almost double the dimension of those of A. marmorata and A. hylaedactyla. Topotype specimens
showed no evidence of an exceptionally larger tongue in comparison with congeners, or even a potential distinctive
shape of tongue. The type specimens re-examined by us and additional examined specimens (see Appendix I) are
in compliance with our redescription with respect to the previously expected dimension of tongue for Adenomera
species. Regarding dimorphic morphometric variables, such as larger tympanum (see Bokermann 1956), no
evident differences were found either. Tympanum diameter of the allotype was indicated in the original description
as the same of that of the holotype (1.0 mm). Values of this morphometric variable were greater both for adult
males (1.3–1.6 mm; N=10) and adult female (1.7 mm; N=1). Morphological measurements of the adult female
topotype were larger than those of the adult male topotypes, most probably explained by isometric differences due
to the larger SVL. Our small sample (N=1 female) hampers any proper statistical approach to assess the
significance of morphometric differences, as well as to seek potential allometric differences related to sexual
dimorphism.
Examined material. Holotype (MZUSP 73695); Allotype (MZUSP 73684); Topotype specimens—BRAZIL:
PARÁ: Novo Progresso, Cachimbo (AAG-UFU 1515–1525; CHUNB 40218–40221).
Adenomera saci, new species

Figures 2C–D, 5–8
Holotype. AAG-UFU 1339, adult male, collected at the Parque Nacional da Chapada dos Veadeiros (14°10'S,
47°47'W; approximately 1030 a.s.l.), Municipality of Alto Paraíso de Goiás, northern State of Goiás, central Brazil,
on 10–15 November 2012, by T. R. de Carvalho, B. F. V. Teixeira, and L. B. Martins.
Paratopotypes. Five adult males: AAG-UFU 0108–0109, on 2–3 December 2010, by A. A. Giaretta; AAG-
UFU 0762–0763, on 13–19 November 2011, by A. A. Giaretta and K. G. Facure; ZUEC 3287, on 10 January 1974,
by W. C. A. Bokermann, all collected at the Chapada dos Veadeiros, northern State of Goiás, central Brazil.
Referred specimens. Non-topotype specimens under the name Adenomera martinezi: Heyer 1973; Vitt et al.
2005; Cintra et al. 2009; Moreira et al. 2009; Oda et al. 2009; Silva Jr. et al. 2009; Kopp et al. 2010; Morais et al.
2011; Valdujo et al. 2012.
Diagnosis. Adenomera saci sp. nov. is assigned to the genus (L. marmoratus species group and Adenomera
genus definitions; sensu Heyer 1973, 1974, respectively) by the following set of characters: 1) small body size (up
to 34.1 mm; sensu Kok et al. 2007); 2) toes lacking fringing or webbing; 3) adult males lacking thumb spines; 4)
first and second fingers of approximately equal length. The new species is diagnosed from the other 15 species of
Adenomera by the following combination of characters: 1) presence of four-six symmetrically arranged rows of
longitudinal dark-colored spots on dorsum; 2) medium-sized Adenomera (adult male SVL 19.7–22.6 mm); 3)
vertebral pin-stripe always present; 4) toe tips unexpanded and unflattened; 5) non-pulsed (a whistle to the human
ear), long advertisement call (72–241 ms).
Comparison with other species. Adenomera saci sp. nov. is diagnosed from all congeners (except A.
martinezi) by its distinctive 4–6 symmetrically arranged rows of longitudinal dark-colored spots on dorsum (figs.
2C–D, 5–7).
Adenomera saci sp. nov. (adult male SVL 19.7–22.6 mm; Table 1) can additionally be diagnosed from A.
araucaria, and A. nana (combined adult male SVL 16.3–19.4 mm; Kwet & Angulo 2002; Kwet 2007) by its larger
size, and from A. lutzi, and A. simonstuarti by its smaller size (combined adult male SVL 25.9–34.1 mm; Kok et al.
2007; Angulo & Icochea 2010). Adenomera saci sp. nov. has always a vertebral pin-stripe, whereas no specimens
of A. bokermanni (Heyer 1973), A. engelsi (Kwet et al. 2009), and almost no specimens of A. andreae (Heyer
1973) do. Adenomera saci sp. nov. is diagnosed from A. thomei by not presenting a mask-like pattern on the
inverted triangle of the interorbital region (Almeida & Angulo 2006); from A. lutzi, by lacking tubercles on
forearms, posterior surface of thighs black with distinct yellow, orange or red spotting or mottling, and males with
yellow to orangish yellow throat and belly (Heyer 1975; Kok et al. 2007). Adenomera saci sp. nov. has neither
expanded nor flattened toe tips, whereas specimens of A. andreae, A. marmorata, and A. nana do (Heyer 1973;
Kwet 2007).
FIGURE 5. Live adult male specimens of Adenomera saci sp. nov. from the type locality (Chapada dos Veadeiros, Goiás): (A)
Holotype AAG-UFU 1339 (SVL 22.5 mm); (B) Voucher paratopotype AAG-UFU 0109 (SVL 22.5 mm); (C) Paratopotype
AAG-UFU 0108 (SVL 20.1 mm); (D) Paratopotype AAG-UFU 0762 (SVL 20.5 mm); (E) Paratopotype AAG-UFU 0763
(SVL 22.0 mm).
FIGURE 6. Live adult specimens of Adenomera saci sp. nov. from Cristalina, Goiás: (A) Voucher male AAG-UFU 1761 (SVL
20.5 mm); (B) Voucher male AAG-UFU 0809 (SVL 20.4 mm); (C) Male AAG-UFU 1673 (SVL 21.0 mm).
FIGURE 7. Live adult specimens of Adenomera saci sp. nov. from Pontal do Araguaia, Mato Grosso: (A) Voucher male AAG-
UFU 0208 (SVL 21.5 mm); (B) Male AAG-UFU 1747 (SVL 22.2 mm); (C) Male AAG-UFU 1745 (SVL 22.6 mm); (D)
Female AAG-UFU 1748 (SVL 24.2 mm).
The advertisement call (figs. 9–11; Tables 2–3) distinguishes Adenomera saci sp. nov. from A. andreae, A.
coca, A. hylaedactyla, A. martinezi (present study), and A. thomei, by its non-pulsed structure, pulsed call structure
in all aforementioned species (see Table 3). Adenomera araucaria was reported to possess calls with 5–11 severe
amplitude modulations (see Kwet & Angulo 2002), and A. simonstuarti to possess 3–4 pulse-like, strong amplitude
modulations (see Angulo & Icochea 2010), whereas Adenomera saci sp. nov. calls lack any strong amplitude
modulations forming ‘pulse-like’ sections along their extent (see figs. 9–11). Adenomera saci sp. nov. can also be
diagnosed from A. andreae, A. hylaedactyla, A. lutzi, and A. simonstuarti (combined value range 16–71 ms) by its
longer call duration (72–241 ms); from A. marmorata (dominant frequency 4.50–5.60 kHz), as well as A. andreae
and A. nana [combined value range: 2.30–3.05 kHz (1st harmonic); 4.61–5.44 kHz (2nd harmonic)] by its lower
peaks of frequency [1.69–2.25 kHz (1st harmonic); 3.38–4.41 kHz (2nd harmonic)]. Bioacoustic values of A. diptyx
from Santa Cruz, Bolivia (Marquez et al. 1995; see Table 3) had a marginal overlap with those of Adenomera saci
sp. nov. in call duration, and peaks of sound energy of the first and second harmonics, but different from each other
taking mean values into consideration. Furthermore, specimens recorded from Paraguay and Argentina (V.H.
Zaracho doctoral thesis) and from the State of Mato Grosso do Sul, western Brazil (T.R. de Carvalho unpubl. data),
assigned to A. diptyx had a pulsed call, which can help diagnose this species from the non-pulsed advertisement call
pattern of Adenomera saci sp. nov.
Adenomera saci sp. nov. can additionally be diagnosed from A. andreae (Hero 1990; Menin & Rodrigues
2013), A. hylaedactyla (Heyer & Silverstone 1969; Menin et al. 2009), A. marmorata (Heyer et al. 1990), and
Adenomera sp. (Kokubum & Giaretta 2005), by having exotrophic larvae, with tooth rows on oral papillae, and
FIGURE 8. Adenomera saci sp. nov., holotype (AAG-UFU 1339), adult male. Dorsal (A) and lateral (B) views of head, and
ventral views of foot (C) and hand (D).
FIGURE 9. Advertisement call of two male specimens of Adenomera saci sp. nov. from the type locality. (A) A waveform
section (2 seconds) with five calls from the Parque Nacional da Chapada dos Veadeiros (Goiás); (B) Audiospectrogram (above)
and respective oscillogram (below) of the third call highlighted by a red outline. Unvouchered recording. (C) A waveform
section (2.5 seconds) with five calls from Alto Paraíso de Goiás (Goiás); (D) Audiospectrogram (above) and respective
oscillogram (below) of the third call highlighted by a red outline. Voucher paratopotype: AAG-UFU 0109.
FIGURE 10. Advertisement call of two male specimens of Adenomera saci sp. nov. from Cristalina (Goiás). (A) A waveform
section (2 seconds) with five calls; (B) Audiospectrogram (above) and respective oscillogram (below) of the fourth call
highlighted by a red outline. Voucher specimen: AAG-UFU 1761. (C) A waveform section (2 seconds) with five calls; (D)
Audiospectrogram (above) and respective oscillogram (below) of the second call highlighted by a red outline. Voucher
specimen: AAG-UFU 0809.
FIGURE 11. Advertisement call of two male specimens of Adenomera saci sp. nov. from the State of Mato Grosso. (A) A
waveform section (2.5 seconds) with five calls from Pontal do Araguaia; (B) Audiospectrogram (above) and respective
oscillogram (below) of the second call highlighted by a red outline. Voucher specimen: AAG-UFU 0208. (C) A waveform
section (3.5 seconds) with five calls from Alto Araguaia; (D) Audiospectrogram (above) and respective oscillogram (below) of
the third call highlighted by a red outline. Unvouchered recording.
FIGURE 12. A scatterplot on the first two principal components (PCs) of bioacoustic variables of Adenomera saci sp. nov.
populations. Open triangles (N = 7 individuals from the type locality, Chapada dos Veadeiros, Goiás); Filled triangles (N = 4
individuals from Cristalina, Goiás); Circles (N = 7 individuals from Pontal do Araguaia, Mato Grosso); Square (N = 1
individual from Alto Araguaia, Mato Grosso).
spiracle (fig. 12) (endotrophic larvae with both tooth rows and spiracle absent in all aforementioned species; except
A. marmorata larvae, which was reported to have a spiracle). Among Adenomera species with exotrophic larvae,
Adenomera saci sp. nov. larvae are distinguished from those of A. thomei (first posterior tooth row with no gaps;
Almeida & Angulo 2006) by having a short gap in the first posterior tooth row (fig. 13). Morphological features of
A. diptyx mouthparts (see fig. 2 in De la Riva 1995) agree with those of Adenomera saci sp. nov. (fig. 13C) by
having marginal papillae with a dorsal gap, and two anterior and three posterior tooth rows sharing the following
labial tooth row formula: [LTFR 2(2)3/(1)].
Description of holotype. AAG-UFU 1339 (figs. 2C–D, 5A, 8). Adult male. Snout pointed in dorsal view (fig.
8A), acuminate in lateral view (fig. 8B). Weakly developed shovel-like fleshy ridge on snout tip. Nostrils
positioned dorsolaterally, closer to snout tip than to eyes; canthus rostralis indistinguishable; loreal region concave;
upper eyelids glandular. Supratympanic folds extending from posterior margin of eyes, passing over tympani, and
extending to base of arms. A discrete, elongated post-commissural gland. Vocal sac subgular, internal. Vocal slits
present; vomerine teeth in two straight rows posterior to choanae; tongue ovoid, free behind. Relative finger
lengths I ~ II ~ IV < III; finger tips rounded, not expanded, and with no webbing or fringing; inner metacarpal
tubercle elongated; outer metacarpal tubercle nearly rounded (fig. 8D); subarticular and supernumerary tubercles
rounded. No thumb asperities. Dorsum and dorsal surface of shanks glandular; posterior half of body, dorsal
surface of shanks, and posterior surface of tarsi with minute tubercles. Vertebral pin-stripe present. Four
longitudinal rows of symmetrically arranged spots. Flanks with longitudinal granular rows from posterior margin
of tympani to groin. Throat and belly smooth. Ventral surface of thighs areolate. Posterior surface of thighs spotted.
Relative toe lengths I < II < V ~ III < IV; toe tips rounded, not expanded (pointed toe tips: character state A; see fig.
1A in Heyer 1973); toes ridged laterally, with no webbing. Inner metatarsal tubercles ovoid, outer conical (fig. 8C);
subarticular and supernumerary tubercles rounded. Tarsal folds formed by ill-defined rows of tubercles, extending
from inner metatarsal tubercle to approximately 1/2 length of tarsi. Heel smooth.
Measurements of holotype. Morphological measurements (mm) and ratios (%) in relation to SVL (22.5 mm):
HL 8.8 (39.1), HW 7.1 (31.6), ED 2.3 (10.2), TD 1.6 (7.1), END 2.0 (8.9), IND 2.1 (9.3), FRL 4.8 (21.3), HAL 5.6
(24.9), TL 9.9 (44.0), SL 10.5 (46.7), TSL 6.8 (30.2), FL 12.3 (54.7).
Coloration of holotype in alcohol (fig. 2C–D). Snout tip has a faded coloration. Tympani reddish brown.
Upper jaw with sinuous cream-colored stripes, white spots/blotches, and a white-colored gland. Dorsum with four
longitudinal rows of symmetrically arranged black spots barely distinguishable from the very dark brown
background. Flanks with cream-colored longitudinal row of granules on a black background. Pale gray vertebral
stripe. White-tipped tubercles scattered on posterior half of dorsum, dorsal surface of shanks, and outer surface of
tarsi. Dorsal surface of limbs with brown blotches on a very dark brown background. Posterior surface of thighs
with white spots on a very dark brown background. Throat and belly cream, and ventral surface of limbs cream-
colored, with melanophores, but with no distinctive color pattern.
Coloration of holotype in life (fig. 5A). Iris copper, upper eyelids bordered by an ill-outlined cream stripe.
Tympani reddish brown. Dorsum with black longitudinal rows of spots on a moss green and grayish brown
background. Spots and blotches on lateral of head and flanks with a whitish silver or yellow coloration. Flanks with
cream-colored longitudinal granular rows on a grayish brown background. Vertebral stripe cream, with some
portions tending to an orange coloration. Dorsal surface of limbs with black stripes and/or blotches on a brown
background. Throat, belly, and ventral surface of limbs cream.
Variation. Morphometric variation is summarized in Table 1. Variation within the type series is restricted to
dorsal texture (smooth or glandular), and color pattern (dark gray to very dark brown background), considering that
the four to six longitudinal rows of symmetrically arranged black spots are variable due to the dorsal coloration
itself, which might become evident or barely indistinguishable in preserved specimens. Posterior surface of thighs
vary from a spotted or mottled pattern, and which can form ill-defined and fragmented stripes (AAG-UFU 0109,
0762–63, 0809, 1673, 1761–63, 2671, and ZUEC 3287) or a well-defined striped pattern (AAG-UFU 0108). Lower
jaw can be dark-colored coinciding with the lateral expansion of vocal sac. Besides the melanophores scattered on
ventral surface, specimens AAG-UFU 0109, 0809, 1673, 1761–63, have throat, belly, and ventral surface of thighs
finely covered with white dots and/or spots.
Non-topotype specimens also vary in dorsal texture (smooth or glandular), and color pattern (dark gray to very
dark brown background). Four to six longitudinal rows of symmetrically arranged black spots on dorsum are
variable due to the dorsal coloration itself, which might become evident or barely indistinguishable in preserved
specimens. Specimens AAG-UFU 0809, 1745–46, and 1761 have a faded white, well-developed shovel-like fleshy
ridge on snout. Dorsal surface of thighs have spotted or mottled pattern in all specimens (AAG-UFU 0208, 1745–
48).
The adult female AAG-UFU 1748 has a robust body shape, head sub-elliptical in dorsal view, with no shovel-
like fleshy ridge on snout tip, as in the case of the adult female topotype of A. martinezi (AAG-UFU 1521).
Specimens in life have some variation with respect to coloration, such as dorsal coloration (olive green to black),
vertebral stripe (cream to brownish orange), granular rows on flanks (cream to yellow) (figs. 5–7).
Advertisement call from the type locality (Chapada dos Veadeiros). Seven males recorded (N = 343
analyzed calls). Advertisement call (fig. 9; Table 2) consists of a non-pulsed signal (a whistle to the human ear)
with up to nine harmonics and with a slight ascendant frequency modulation, emitted at a rate of 1–3 calls/second
(mean 2.2; SD = 0.3), and at a rate of 111–132 calls/minute (mean 123.2; SD = 10.3). Call duration varies from 90–
139 ms (mean 112.1; SD = 11.0), and intercall interval from 220–513 ms (mean 361.4; SD = 77.4). Dominant
frequency coincides with either the first (14%) or the second harmonic (72%) among the recorded individuals, or
can alternate between the first and second harmonics (14%) among analyzed calls of the same individual. Peak of
sound energy varies from 1.69–2.06 kHz (mean 1.85 kHz; SD = 0.07) in the first harmonic, and/or from 3.38–3.94
kHz (mean 3.67 kHz; SD = 0.18) in the second harmonic. The other harmonics, if present, are increasingly weaker
in sound energy.
Bioacoustic comparisons. Dominant frequency of non-topotype populations of A. saci sp. nov. coincides with
either the first (75%) or the second harmonic (15%) among the recorded individuals from Cristalina (N = 4; fig.
10); with either the first (57%) or the second harmonic (43%) among the recorded individuals from Pontal do
Araguaia (N = 7; figs. 11A–B); and with the second harmonic among the analyzed calls of the individual from Alto
Araguaia (N = 1; figs. 11C–D).
Bioacoustic data of topotypes of Adenomera martinezi, and Adenomera saci sp. nov. from the type locality and
of comparative non-topotype populations are summarized in Table 2. There was no correlation between the first
principal component, taking all three temporal variables tested into account, and the temperature [r = 0.13 (r2 <
2%), p = 0.463; N = 34], in other words, temperature did not affect the temporal variables and did not explain the
variability found in the calls of topotypes of A. martinezi and all four populations of A. saci sp. nov.
The first three principal components (PCs) accounted for around 96% of the overall bioacoustic variability
among the populations of A. saci sp. nov. A scatterplot of bioacoustic variables on the first two principal
components (fig. 12) showed that the topotype (Chapada dos Veadeiros) and Cristalina populations were almost
completely distinguished from the populations from Pontal do Araguaia and Alto Araguaia along the PC1, an
expected result based on bioacoustic differences previously observed by us in the quantitative data comparisons
(see Table 2) of populations from Goiás (topotypes and Cristalina) and Mato Grosso (Pontal do Araguaia). The
insufficient call sample of the single recorded individual from Alto Araguaia (Mato Grosso) did not allow us to
assume that the bioacoustic characteristics of this population are similar to that of Pontal do Araguaia, or different
from both Pontal do Araguaia and populations from Goiás (topotypes and Cristalina).
Tadpole (fig. 13). Stage 37. Body tending to ovoid in dorsal view, compressed dorsoventrally. Eyes and nares
positioned dorsally, just nearer the eyes than the snout tip, with a slight rim, but lack any papillae or ornamentations
(fig. 13B). Oral disc positioned anteroventrally. Spiracle singular, sinistral. Spiracular opening with its inner wall
as a slight ridge adhered to body (fig. 13A). Right wall of vent tube displaced dorsally and anteriorly. Dorsal fin
originates at body-tail juncture; ventral fin originates at the vent tube. Tail height just greater than body height.
Dorsal and ventral fins with the same height. Tail tip with a narrow and pointed shape. Oral disc lacks tooth rows
(see variation below). Marginal papillae with a wide dorsal gap surround the oral disc. Presence of keratinized of
both upper (arched) and lower jaw (v-shaped) sheaths with serrated cutting edges. Dorsal surface of body dark
brown, ventral surface cream. Tail with dark brown blotches on both dorsal and ventral fins, and on tail muscle.
Measurements (mm): TL 34.8; BL 10.1; TAL 24.6; IOD 3.4; IND 1.6; TMH 2.4; MTH 3.9; TMW 2.5.
Variation of tadpoles. Two tadpoles (Gosner’s stages 36–37) have well-defined tooth rows: LTRF 2(2)/3(1)
(fig. 13C). The second anterior tooth row has a wide medial gap, approximately 1/3 length of the entire row. The
first posterior tooth row has a very slight medial gap.
FIGURE 13. Lateral (A) and dorsal (B) views, and schematic diagram of the oral disc (C) of a tadpole (stage 37) of Adenomera
saci sp. nov. from Cristalina, State of Goiás.
FIGURE 14. Geographic distribution of Adenomera martinezi and Adenomera saci sp. nov. on a topographic map. Type
localities: Circle—A. martinezi (Cachimbo, Pará); Square—Adenomera saci sp. nov. (Chapada dos Veadeiros, Goiás).
Triangles correspond to the distributional records for Adenomera saci sp. nov.: (1) Sonora, State of Mato Grosso do Sul; (2)
Alto Araguaia, (3) Pontal do Araguaia, (4) Ribeirão Cascalheira, and (5) Santa Terezinha, State of Mato Grosso; (6) Mineiros/
Chapadão do Céu, (7) Cristalina, (8) Brasília, (9) Niquelândia, (10) Minaçu, and (11) Buritinópolis, State of Goiás/Distrito
Federal; (12) Formoso do Araguaia/Ilha do Bananal, (13) Almas, and (14) Rio da Conceição/Jalapão, State of Tocantins.
Records were based on our data and extracted from Heyer (1973); Vitt et al. (2005); Cintra et al. (2009); Moreira et al. (2009);
Oda et al. (2009); Silva Jr. et al. (2009); Kopp et al. (2010); Morais et al. (2011); Valdujo et al. (2012).
Natural history. Adenomera saci sp. nov. occurs in montane (> 1000 m a.s.l.) rock fields with sandy/muddy
soil, or lowland (~ 350 m a.s.l.) grassy fields with sandy/muddy soil that are almost always associated with palm
grove marshes (Veredas). Males call within underground chambers or from exposed calling sites, most times
among grassy tufts. The species is mainly active during the night, but males may also be heard during daylight in
rainy days.
Geographic distribution. The widespread pattern of distribution of Adenomera saci sp. nov. encompasses
both rocky Cerrado environments of central Brazil and transitional Amazonian regions of the Araguaia River and
Xingu River basins, central-western and northern Brazil (see fig. 14 for a distribution map and references).
Etymology. The proper name ‘saci’ in Portuguese (sa’si, sassy perere, or matintape’re in Tupi indigenous
language) stands for a kind of whistling imp, which according to the native Tupi ethnic groups in Brazil, is an
annoying prankster to whoever sees him. The name of the species, an invariant noun in apposition, is an allusion to
the whistle call pattern emitted by the species that we associate to this well-known character in Brazilian folklore.
Remarks. It is noteworthy to add that the advertisement calls of A. martinezi and A. saci sp. nov. are
distinguishable to each other to the ear. Specimens reported from other localities/regions in addition to those
discussed earlier in the geographic distribution section (Vitt et al. 2005; Silva Jr. et al. 2009; Morais et al. 2011)
compared either to our study areas (Chapada dos Veadeiros, Cristalina, Alto Araguaia, and Pontal do Araguaia) or
to localities from where we have bioacoustic information available (Formoso do Araguaia and Santa Terezinha)
were assigned to Adenomera saci sp. nov. (see fig. 14). Specimens reported from the Ilha do Bananal, southwestern
State of Tocantins, and the Xingu River basin, State of Mato Grosso (Heyer 1973), were unambiguously assigned
to Adenomera saci sp. nov. based on digitized recordings of Adão J. Cardoso available at the Fonoteca Neotropical
Jacques Vielliard from Formoso do Araguaia, State of Tocantins, and Santa Terezinha, State of Mato Grosso,
respectively (sound files FNJV 11223–11224). Taking also the proximity of those localities into account,
reinforced by the widespread distribution pattern of the species against a putative ‘Cachimbo endemic’, restricted
distribution pattern of A. martinezi, we tentatively assigned the specimens reported from the State of Mato Grosso
do Sul (Silva Jr et al. 2009), and the Jalapão and nearby localities, southeastern State of Tocantins (Vitt et al. 2005;
Morais et al. 2011) to Adenomera saci sp. nov. as well (fig. 14).
Regardless of the bioacoustic differences (fig. 12; Table 2) and geographic distance (fig. 14) among
populations of Adenomera saci sp. nov. discussed earlier, our results are still not conclusive. We believe that these
populations ought to benefit from a molecular evidence, as well as additional efforts to increase call sample,
combining two datasets to properly address the taxonomic status of populations from Mato Grosso and uncover a
potential cryptic diversity among the widely distributed populations currently assigned to Adenomera saci sp. nov.
through a bioacoustic evidence.
Examined material. Topotype specimens—GOIÁS: Alto Paraíso de Goiás (CHUNB 42537, 49506–49509,
58405, 58884, 58886); Non-topotype specimens –DISTRITO FEDERAL: Brasília (AAG-UFU 2671; CHUNB
58358); GOIÁS: Colinas do Sul (CHUNB 44706); Cristalina (AAG-UFU 0809, AAG-UFU 1673, AAG-UFU
1761–1763); MATO GROSSO: Alto Araguaia (CHUNB 65849); Nova Xavantina (CHUNB 64343–64344); Novo
Santo Antônio (CHUNB 57787, 57861, 57982, 57985); Pontal do Araguaia (AAG-UFU 0208, 1745–1748);
Ribeirão Cascalheira (ZUEC 7496–7498); Santa Terezinha (ZUEC 7459–7460); MATO GROSSO DO SUL:
Cassilândia (CHUNB 58798); TOCANTINS: Caseara (CHUNB 45600); Colinas do Tocantins (CHUNB 50969,
50972–50975, 52822–52825, 53140–53141); Guaraí (CHUNB 52446–52447); Lagoa da Confusão (CHUNB
58135, 58140, 58186); Mateiros (CHUNB 27314–27320, 27322, 27324–27327, 41764, 41766, 42005–42006,
42008–42017); Palmas (CHUNB 11245–11249, 14702, 24266, 24407–24412, 24415–24420, 24435–24436,
24439–24440, 48094–48097); Porto Nacional (CHUNB 47732).
Discussion
Bokermann (1956) suggested a terrestrial reproductive mode with non-feeding larvae for A. martinezi based on
presumably large-sized ovarian eggs (0.8 mm) from the allotype. We refute his assumption considering that, in fact,
endotrophic Adenomera species have much larger ovarian eggs (e.g. Adenomera sp.: 2.6–3.7 mm; Kokubum &
Giaretta 2005). Still, we could not neglect the possibility of the female of A. martinezi examined by Bokermann
(1956) bearing immature ovarian eggs. De la Riva (1995), likewise, attributed a mean mature ovarian egg size of
1.8 mm to the Bolivian Buenavista-Amboró population of A. diptyx, which possesses a reproductive mode with
exotrophic larvae (population referred as A. bokermanni or an unnamed species by De la Riva 1995). An additional
consideration is that Adenomera saci sp. nov., a morphologically cryptic species in relation to A. martinezi, has
exotrophic tadpoles, as described earlier. With the description of Adenomera saci sp. nov. larvae, it is possible to
recognize an overall morphological similarity with those of A. diptyx (De la Riva 1995), and the presumably
similar morphology to its sibling species A. martinezi, suggesting that all three species could share the same
general reproductive mode with exotrophic larvae. Comparisons with larvae of A. bokermanni (Heyer 1973) were
avoided, since there are no comments about the locality of the tadpole described by Heyer (1973). Later, Heyer
(1977, 1984) suggested that the type series of A. bokermanni might actually be a composite of at least two
morphologically similar species, leading us to believe that the described tadpole in Heyer (1973) might not
correspond to the tadpole of A. bokermanni.
An available specific name prior to our description, Leptodactylus glandulosus, was described by Cope (1887)
from the Chapada dos Guimarães, State of Mato Grosso, and is currently a junior synonym of A. diptyx (see De la
Riva 1996 for nomenclatural history). Heyer (1973) re-examined L. glandulosus type series, referring to them as
possibly being composed of juvenile specimens, and stated that some individuals had a vertebral pin-stripe, in
addition to dorsum with indistinct spots. This superficial resemblance with A. martinezi and A. saci sp. nov. based
solely on coloration pattern is not enough to assign them to L. glandulosus. The character state of vertebral pin-
stripe is always present in all specimens of both A. martinezi and A. saci sp. nov., whereas it varied among the
specimens re-examined by Heyer (1973). Additionally, Heyer (1973) assigned this morphotype to what he called
‘form II species’, clustered with the general similar morphotype of A. hylaedactyla (including A. diptyx as a junior
synonym) and A. bokermanni, whereas A. martinezi was the only morphotype assigned to ‘form III species’, which
would also encompass the morphotype of A. saci sp. nov., morphologically cryptic to A. martinezi. Populations of
one species of Adenomera currently under uncertain taxonomic status is known to occur at the Chapada dos
Guimarães and on its outskirts (Municipality of Cuiabá, and District of São Vicente), whose morphological and
bioacoustic features fit those of A. diptyx or a closely related form (V.H. Zaracho unpublished doctoral thesis; T.R.
de Carvalho unpubl. data; see Appendix I for examined specimens of this region), so that these specimens should
eventually correspond to the available name L. glandulosus instead of A. diptyx, but this name neither is applicable
to A. martinezi nor A. saci sp. nov., which share the distinctive four to six longitudinal rows of symmetrically
arranged black spots on dorsum and a vertebral pin-stripe.
The recognition of Adenomera saci sp. nov. also has conservation implications. Based on our assumed
distribution of A. martinezi and A. saci sp. nov. (fig. 14), the IUCN Red List of Threatened Species extinction risk
assessment of A. martinezi (Bastos et al. 2004) requires a reassessment, inasmuch as we reconsidered this species,
as far as we know, as endemic to Cachimbo, southwestern State of Pará so far. The 2004 conservation status
assessment in fact encompassed both A. martinezi and A. saci sp. nov., while this conservation status category of
‘Least Concern’ might only be applied to A. saci sp. nov. as a widely distributed and abundant species in central
and northern Brazil. On the other hand, Adenomera martinezi is known to occur only at its type locality
(Cachimbo, southwestern State of Pará, northern Brazil), supporting priorities for conservation actions of this
region, as well as the necessity of more extensive taxon sampling efforts in the region to corroborate a potential
micro-endemism of A. martinezi, with distribution restricted to a single location. Based on its very restricted
distribution, we suggest classifying Adenomera martinezi as a ‘Near Threatened’ species according to IUCN
guidelines for the next Red List of Threatened Anuran Species (IUCN 2011). This species partially fits the
requirements of criteria B and D to belong to a near threatened category: ‘a very small extent of occurrence (< 100
km2), and in existing only in one location’, and ‘Restricted area of occupancy or number of locations with a
plausible future threat that could drive the taxon to CR or EX in a very short time’. Other criteria can not be applied
to this species for as much as our micro-endemism suspicion is not thoroughly addressed by other evidence, such
as studies on population fluctuations to assess a potential decline in the future, and a better taxon sampling in the
region to reinforce the hypothesis of Cachimbo micro-endemism distribution pattern of Adenomera martinezi.
Hence, revealing insights into additional conservation priorities and actions of the region and the species, and a
reappraisal of this preliminary IUCN threat category proposal.
The bioacoustic approach has been employed in recent works studying the taxonomy of Cerrado anuran taxa,
and has proven very useful in the unraveling and/or reassessing unresolved species identities, revealing new
species under morphologically cryptic taxa (Carvalho et al. 2010; Carvalho 2012; Andrade & Carvalho 2013) or at
least sharing similar overall morphological patterns (Giaretta et al. 2007; Martins & Giaretta 2011; Carvalho et al.
2012). It is worth stressing that this study represents one more case of the use of bioacoustics addressing cryptic
species complexes, in this case a species that is widely distributed in central Brazil, under similar overall
morphology shared with A. martinezi.
Acknowledgments
Special thanks go to B. F. V. Teixeira, K. G. Facure, and L. B. Martins for assistance in the field, G. R. Colli, H.
Zaher, L. F. Toledo, and J. P. Pombal Jr. for making available specimens under their care, L. F. Toledo for making
available recordings from the Fonoteca Neotropical Jacques Vielliard under his care, K. G. Facure for statistical
support, Miguel Vences and two anonymous reviewers, whose comments greatly improved the manuscript. We are
indebted to Tenente Coronel Aviador Francalacci and his team for providing facilities at Cachimbo. This work was
supported by FAPESP, FAPEMIG and CNPq. FAPESP provided a research grant to T.R.C, CNPq to A.A.G.
Collection permits: ICMBio/SISBIO 29954–3 and 02015.008064/02–51.
References
Almeida, A.P. & Angulo, A. (2006) A new species of Leptodactylus (Anura: Leptodactylidae) from the state of Espírito Santo,
with remarks on the systematics of associated populations. Zootaxa, 1334, 1–25.
Altig, R. (2007) A primer for the morphology of anuran tadpoles. Herpetological Conservation and Biology, 2 (1), 71–74.
Altig, R. & McDiarmid, R.W. (1999) Body plan: development and morphology. In: McDiarmid, R.W. & Altig, R. (Eds.),
Tadpoles: the biology of anuran larvae. The University of Chicago Press, Chicago, pp. 24–51.
Andrade, F.S. & Carvalho, T.R. (2013) A new species of Pseudopaludicola Miranda-Ribeiro (Leiuperinae: Leptodactylidae:
Anura) from the Cerrado of southeastern Brazil. Zootaxa, 3608 (5), 389–397.
Angulo, A., Cocroft, R.B. & Reichle, S. (2003) Species identity in the genus Adenomera (Anura: Leptodactylidae) in
southeastern Peru. Herpetologica, 59 (4), 490–504.
http://dx.doi.org/10.1655/20-104
Angulo, A. & Icochea, J. (2010) Cryptic species complexes, widespread species and conservation: lessons from Amazonian
frogs of the Leptodactylus marmoratus group (Anura: Leptodactylidae). Systematics and Biodiversity, 8 (3), 357–370.
http://dx.doi.org/10.1080/14772000.2010.507264
Angulo, A. & Reichle, S. (2008) Acoustic signals, species diagnosis, and species concepts: the case of a new cryptic species of
Leptodactylus (Amphibia, Anura, Leptodactylidae) from the Chapare Region, Bolivia. Zoological Journal of the Linnean
Society, 152, 59–77.
http://dx.doi.org/10.1111/j.1096-3642.2007.00338.x
Bastos, R.P., Pavan, D. & Silvano, D. (2004) Leptodactylus martinezi. IUCN Red List of Threatened Species, version 2012.2.
Available from: www.iucnredlist.org (Accessed on 20 Mar. 2013)
Berneck, B.V.M., Costa, C.O.R. & Garcia, P.C.A. (2008) A new species of Leptodactylus (Anura: Leptodactylidae) from the
Atlantic Forest of São Paulo State, Brazil. Zootaxa, 1795, 46–56.
Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a
window on diversity and conservation. Trends in Ecology and Evolution, 22 (3), 148–155.
http://dx.doi.org/10.1016/j.tree.2006.11.004
Bioacoustics Research Program (2012) Raven Pro: Interactive Sound Analysis Software, version 1.5. Ithaca, New York: The
Cornell Lab of Ornithology. Available from: http://www.birds.cornell.edu/raven (Accessed 11 Dec 2012)
Boistel, R., Massary, G.C. & Angulo, A. (2006) Description of a new species of the genus Adenomera (Amphibia, Anura,
Leptodactylidae) from French Guyana. Acta Herpetologica, 1, 1–14.
Bokermann, W.C.A. (1956) Sobre una nueva especie de Leptodactylus del Brasil (Amphibia). Neotropica, 2 (8), 37–40.
Carvalho, T.R. (2012) A new species of Pseudopaludicola Miranda-Ribeiro (Leiuperinae: Leptodactylidae: Anura) from the
Cerrado of southeastern Brazil with a distinctive advertisement call pattern. Zootaxa, 3328, 47–54.
Carvalho, T.R., Giaretta, A.A. & Facure, K.G. (2010) A new species of Hypsiboas Wagler (Anura: Hylidae) closely related to
H. multifasciatus Günther from southeastern Brazil. Zootaxa, 2521, 37–52.
Carvalho, T.R., Giaretta, A.A. & Magrini, L. (2012) A new species of the Bokermannohyla circumdata group (Anura: Hylidae)
from southeastern Brazil, with bioacoustic data on seven species of the genus. Zootaxa, 3321, 37–55.
Cintra, C.E.D., Silva, H.L.R. & Silva Jr., N.J. (2009) Herpetofauna, Santa Edwiges I and II hydroelectric power plants, state of
Goiás, Brazil. Check List, 5 (3), 570–576.
Cope, E.D. (1887) Synopsis of the Batrachia and Reptilia obtained by H.H. Smith in the Province of Mato Grosso, Brazil.
Proceedings of the American Philosophical Society, 24, 44–60.
Dayrat, B. (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society, 85, 407–415.
http://dx.doi.org/10.1111/j.1095-8312.2005.00503.x
De la Riva, I. (1995) A new reproductive mode for the genus Adenomera (Amphibia: Anura: Leptodactylidae): taxonomic
implications for certain Bolivian and Paraguayan populations. Studies on Neotropical Fauna and Environment, 30 (1), 15–29.
http://dx.doi.org/10.1080/01650529509360937
De la Riva, I. (1996) The specific name of Adenomera (Anura: Leptodactylidae) in the Paraguay River Basin. Journal of
Herpetology, 30 (4), 556–558.
http://dx.doi.org/10.2307/1565706
De la Riva, I., Köhler, J., Lötters, S. & Reichle, S. (2000) Ten years of research on Bolivian amphibians: updated checklist,
distribution, taxonomic problems, literature and iconography. Revista Española de Herpetología, 14, 19–164.
De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology, 56 (6), 879–886.
http://dx.doi.org/10.1080/10635150701701083
De Sá, R.O., Heyer, W.R. & Camargo, A. (2005) A phylogenetic analysis of Vanzolinius Heyer, 1974 (Amphibia, Anura,
Leptodactylidae): taxonomic and life history implications. Arquivos do Museu Nacional, 63 (4), 707–726.
Duellman, W.E. (1970) The hylid frogs of Middle America. Monographs of the Museum of Natural History of the University of
Kansas, Lawrence, 753 pp.
Duellman, W.E. & Trueb, L. (1994) Biology of Amphibians. The John Hopkins University Press, Baltimore, Maryland, 670 pp.
Fouquet, A., Blotto, B.L., Maronna, M.M., Verdade, V.K., Juncá, F.A., De Sá, R. & Rodrigues, M.T. (2013) Unexpected
phylogenetic positions of the genera Rupirana and Crossodactylodes reveal insights into the biogeography and
reproductive evolution of leptodactylid frogs. Molecular Phylogenetics and Evolution, 67, 445–457.
http://dx.doi.org/10.1016/j.ympev.2013.02.009
Frost, D.R. (2013) Amphibian Species of the World: an Online Reference. version 5.6. American Museum of Natural History,
New York, USA. Available from: http://research.amnh.org/vz/herpetology/amphibia/ (Accessed 30 Jan 2013)
Frost, D.R., Grant, T., Faivovich, J., Bain, R.H., Haas, A., Haddad, C.F.B., De Sá, R.O., Channing, A., Wilkinson, M.,
Donnellan, S.C., Raxworthy, C.J., Campbell, J.A., Blotto, B.L., Moler, P., Drewes, R.C., Nussbaum, R.A., Lynch, J.D.,
Green, D.M. & Wheeler, W.C. (2006) The amphibian tree of life. Bulletin of the American Museum of Natural History,
297, 1–371.
http://dx.doi.org/10.1206/0003-0090(2006)297[0001:tatol]2.0.co;2
Giaretta, A.A., Freitas, F.G., Antoniazzi, M.M. & Jared, C. (2011) Tadpole buccal secretory glands as new support for a
Neotropical clade of frogs. Zootaxa, 3011, 38–44.
Giaretta, A.A., Toffoli, D. & Oliveira, L.E. (2007) A new species of Ischnocnema (Anura: Eleutherodactylinae) from open
areas of the Cerrado Biome in southeastern Brazil. Zootaxa, 1666, 43–51.
Glaw, F., Köhler, J., De la Riva, I., Vieites, D.R. & Vences, M. (2010) Integrative taxonomy of Malagasy treefrogs:
combination of molecular genetics, bioacoustics and comparative morphology reveals twelve additional species of
Boophis. Zootaxa, 2383, 1–82.
Gosner, K.L. (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16
(3), 183–190.
Hero, J.M. (1990) An illustrated key to tadpoles occurring in the central Amazonia rainforest, Manaus, Amazonas, Brasil.
Amazoniana, 11 (2), 201–262.
Heyer, W.R. (1969a) Studies on the genus Leptodactylus (Amphibia, Leptodactylidae) III. A redefinition of the genus
Leptodactylus and a description of a new genus of leptodactylid frogs. Contributions in Science, Los Angeles County
Natural History Museum, 155, 1–14.
Heyer, W.R. (1969b) The adaptive ecology of the species groups of the genus Leptodactylus (Amphibia, Leptodactylidae).
Evolution, 23 (3), 421–428.
http://dx.doi.org/10.2307/2406697
Heyer, W.R. (1973) Systematics of the marmoratus group of the frog genus Leptodactylus (Amphibia, Leptodactylidae).
Contributions in Science, Los Angeles County Natural History Museum, 251, 1–50.
Heyer, W.R. (1974a) Relationships of the marmoratus species group (Amphibia, Leptodactylidae) within the subfamily
Leptodactylinae. Contributions in Science, Los Angeles County Natural History Museum, 253, 1–45.
Heyer, W.R. (1974b) Vanzolinius, a new genus proposed for Leptodactylus discodactylus (Amphibia, Leptodactylidae).
Proceedings of the Biological Society of Washington, 87 (11), 81–90.
Heyer, W.R. (1975) Adenomera lutzi (Amphibia: Leptodactylidae), a new species of frog from Guayana. Proceedings of the
Biological Society of Washington, 88 (28), 315–318.
Heyer, W.R. (1977) A discriminant function analysis of the frogs of the genus Adenomera (Amphibia: Leptodactylidae).
Proceedings of the Biological Society of Washington, 89, 581–592.
Heyer, W.R. (1984) The systematic status of Adenomera griseigularis Henle, with comments on systematic problems in the
genus Adenomera (Amphibia: Leptodactylidae). Amphibia-Reptilia, 5, 97–100.
http://dx.doi.org/10.1163/156853881x00186
Heyer, W.R. (1998) The relationships of Leptodactylus diedrus (Anura, Leptodactylidae). Alytes, 16 (1–2), 1–24.
Heyer, W.R., García-Lopez, J.M. & Cardoso, A.J. (1996) Advertisement call variation in the Leptodactylus mystaceus complex
(Amphibia: Leptodactylidae) with a description of a new sibling species. Amphibia-Reptilia, 17, 7–31.
http://dx.doi.org/10.1163/156853896x00252
Heyer, W.R., Rand, A.S., Cruz, C.A.G., Peixoto, O.L. & Nelson, C.E. (1990) Frogs of Boracéia. Arquivos de Zoologia, 31(4),
231–410.
Heyer, W.R. & Silverstone, P.A. (1969) The larva of the frog Leptodactylus hylaedactylus (Leptodactylidae). Fieldiana,
Zoology, 51 (11), 141–145.
http://dx.doi.org/10.5962/bhl.title.3047
IUCN (2011) IUCN Standards and Petitions subcommittee. Guidelines for using the IUCN Red List Categories and Criteria.
Version 9.0. Available from: http://www.iucnredlist.org/documents/RedListGuidelines.pdf (Accessed 20 Jun. 2013)
Jaiswara, R., Balakrishnan, R., Robillard, T., Rao, K., Cruaud, C. & Desutter-Grandcolas, L. (2012) Testing concordance in
species boundaries using acoustic, morphological, and molecular data in the field cricket genus Itaropsis (Orthoptera:
Grylloidea, Gryllidae: Gryllinae). Zoological Journal of the Linnean Society, 164, 285–303.
http://dx.doi.org/10.1111/j.1096-3642.2011.00769.x
Kok, P.J.R., Kokubum, M.N.C., MacCulloch, R.D. & Lathrop, M. (2007) Morphological variation in Leptodactylus lutzi
(Anura, Leptodactylidae) with description of its advertisement call and notes on its courtship behavior. Phyllomedusa, 6
(1), 45–60.
Kokubum, M.N.C. (2008) Ecologia reprodutiva e diversidade acústica de espécies de Leptodactylus do grupo marmoratus
(Anura: Leptodactylidae). Tese de Doutorado, Universidade de Brasília (UnB), 212 pp.
Kokubum, M.N.C. & Giaretta, A.A. (2005) Reproductive ecology and behaviour of a species of Adenomera (Anura,
Leptodactylinae) with endotrophic tadpoles: systematic implications. Journal of Natural History, 39 (20), 1745–1758.
http://dx.doi.org/10.1080/00222930400021515
Kopp, K., Signorelli, L. & Bastos, R.P. (2010) Distribuição temporal e diversidade de modos reprodutivos de anfíbios anuros
no Parque Nacional das Emas e entorno, estado de Goiás, Brasil. Iheringia, Série Zoologia, 100 (3), 192–200.
http://dx.doi.org/10.1590/s0073-47212010000300002
Kwet, A. (2007) Bioacoustic variation in the genus Adenomera in southern Brazil, with revalidation of Leptodactylus nanus
Müller, 1922 (Anura, Leptodactylidae). Mitteilungen aus dem Museum für Naturkunde in Berlin, Zoologische Reihe
Supplement, 83, 56–68.
http://dx.doi.org/10.1002/mmnz.200600027
Kwet, A. & Angulo, A. (2002) A new species of Adenomera (Anura, Leptodactylidae) from the Araucaria forest of Rio Grande
do Sul (Brazil), with comments on the systematic status of southern populations of the genus. Alytes, 20 (1–2), 28–43.
Kwet, A., Steiner, J. & Zillikens, A. (2009) A new species of Adenomera (Amphibia: Anura: Leptodactylidae) from the
Atlantic rain forest in Santa Catarina, southern Brazil. Studies on Neotropical Fauna and Environment, 44 (2), 93–107.
http://dx.doi.org/10.1080/01650520902901659
Lutz, A. (1926) Observações sobre Batrachios brasileiros. Memórias do Instituto Oswaldo Cruz, 19 (2), 139–174.
http://dx.doi.org/10.1590/s0074-02761930000900001
Lutz, A. (1930) Second paper on brasilian and some closely related species of the genus Leptodactylus. Memórias do Instituto
Oswaldo Cruz, 23 (1), 21–34.
http://dx.doi.org/10.1590/s0074-02761930000100001
Marquez, R., De la Riva, I. & Bosch, J. (1995) Advertisement calls of Bolivian Leptodactylidae (Amphibia, Anura). Journal of
Zoology, London, 237, 313–336.
http://dx.doi.org/10.1111/j.1469-7998.1995.tb02765.x
Martins, L.B. & Giaretta, A.A. (2011) A new species of Proceratophrys Miranda-Ribeiro (Amphibia: Anura: Cycloramphidae)
from central Brazil. Zootaxa, 2880, 41–50.
Menin, M., Almeida, A.P. & Kokubum, M.N.C. (2009) Reproductive aspects of Leptodactylus hylaedactylus (Anura:
Leptodactylidae), a member of the Leptodactylus marmoratus species group, with a description of tadpoles and calls.
Journal of Natural History, 43 (35–36), 2257–2270.
http://dx.doi.org/10.1080/00222930903097707
Menin, M. & Rodrigues, D.J. (2013) The terrestrial tadpole of Leptodactylus andreae (Anura, Leptodactylidae), a member of
the Leptodactylus marmoratus species group. Zootaxa, 3683 (1), 92–94.
Morais, A.R., Côrtes, L.G. & Bastos, R.P. (2011) Queimadas podem alterar as assembleias de anuros? O caso das veredas na
Estação Ecológica Serra Geral do Tocantins. Revista de Biologia Neotropical, 8 (2), 32–39.
Moreira, L.A., Fenolio, D.B., Silva, H.L.R. & Silva Jr., N.J. (2009) A preliminar list of the Herpetofauna from termite mounds
of the Cerrado in the upper Tocantins River valley. Papéis Avulsos de Zoologia, São Paulo, 49 (15), 183–189.
Oda, F.H., Bastos, R.P. & Lima, M.A.C.S. (2009) Taxocenose de anfíbios anuros no Cerrado do Alto Tocantins, Niquelândia,
Estado de Goiás: diversidade, distribuição local e sazonalidade. Biota Neotropica, 9 (4), 219–232.
http://dx.doi.org/10.1590/s1676-06032009000400022
Padial, J.M. & De la Riva, I. (2009) Integrative taxonomy reveals cryptic Amazonian species of Pristimantis (Anura:
Strabomantidae). Zoological Journal of the Linnean Society, 155, 97–122.
http://dx.doi.org/10.1111/j.1096-3642.2008.00424.x
Padial, J.M., Miralles, A., De la Riva, I. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7(16),
1–14.
http://dx.doi.org/10.1186/1742-9994-7-16
Parker, H.W. (1932) The systematic status of some Frogs in the Vienna Museum. Annals and Magazine of Natural History, 10
(10), 341–344.
http://dx.doi.org/10.1080/00222933208673582
Parker, H.W. (1935) The frogs, lizards, and snakes of British Guiana. Proceedings of the Zoological Society of London, 3, 505–
530.
http://dx.doi.org/10.1111/j.1096-3642.1935.tb01678.x
Ponssa, M.L. (2008) Cladistic analysis and osteological descriptions of the frog species in the Leptodactylus fuscus species
group (Anura, Leptodactylidae). Journal of Zoological Systematics and Evolutionary Research, 46 (3), 249–266.
http://dx.doi.org/10.1111/j.1439-0469.2008.00460.x
Ponssa, M.L., Jowers, M.J. & De Sá, R.O. (2010) Osteology, natural history notes, and phylogenetic relationships of the poorly
known Caribbean frog Leptodactylus nesiotus (Anura, Leptodactylidae). Zootaxa, 2646, 1–25.
Pyron, R.A. & Wiens, J.J. (2011) A large-scale phylogeny of Amphibia including over 2800 species, and a revised
classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution, 61 (2), 543–583.
http://dx.doi.org/10.1016/j.ympev.2011.06.012
R Development Core Team (2012) The R Project for Statistical Computing. Vienna, Austria. Available from: http://www.r-
project.org/ (Accessed 30 Jan. 2013)
Shepherd, G.J. (2006) Fitopac 1.6: Manual de usuário. Departamento de Botânica, Universidade Estadual de Campinas,
Campinas.
Silva Jr., N.R., Cintra, C.E.D., Silva, H.L.R., Costa, M.C., Souza, C.A., Pachêco Jr., A.A. & Gonçalves, F.A. (2009)
Herpetofauna, Ponte de Pedra Hydroelectric Power Plant, states of Mato Grosso and Mato Grosso do Sul, Brazil. Check
List, 5 (3), 518–525.
Straughan, I.R. & Heyer, W.R. (1976) A functional analysis of the mating calls of the neotropical frog genera of the
Leptodactylus complex (Amphibia, Leptodactylidae). Papéis Avulsos de Zoologia, São Paulo, 29 (23), 221–245.
Sueur, J., Aubin, T. & Simonis, C. (2008) Seewave: a free modular tool for sound analysis and synthesis. Bioacoustics, 18,
213–226.
http://dx.doi.org/10.1080/09524622.2008.9753600
Valdujo, P.H., Silvano, D.L., Colli, G. & Martins, M. (2012) Anuran species composition and distribution patterns in Brazilian
Cerrado, a Neotropical Hotspot. South American Journal of Herpetology, 7 (2), 63–78.
http://dx.doi.org/10.2994/057.007.0209
Vences, M. & Wake, D.B. (2007) Speciation, species boundaries and phylogeography of amphibians: In: Heatwole, H. (Ed.),
Amphibian Biology. Vol.7. Surrey Beatty & Sons, Chipping Norton, NSW, Australia, pp. 2613–2671.
Vitt, L.J., Caldwell, J.P., Colli, G.R., Garda, A.A., Mesquita, D.O., França, F.G.R., Shepard, D.B., Costa, G.C., Vasconcellos,
M.M. & Novaes-e-Silva, V. (2005) Uma atualização do guia fotográfico dos répteis e anfíbios da região do Jalapão no
Cerrado brasileiro. Special Publications in Herpetology, 2, 1–24.
Wilkinson, L. (2000) Systat Statistics version 10.0 for Windows. SPSS, Chicago, Illinois.
Zaracho, V.H. (2011) El género Adenomera Steindachner, 1867 (Anura: Leptodactylidae) en Argentina. Tesis Doctoral,
Universidad Nacional del Nordeste (UNNE), 195 pp.
APPENDIX 1. Additional examined specimens.
Adenomera ajurauna—BRAZIL: SÃO PAULO: Santo André (ZUEC 6377); Adenomera andreae—BRAZIL: PARÁ: Porto
Trombetas (MNRJ 52886-87); Adenomera cf. andreae—BRAZIL: RONDÔNIA: Cacoal (AAG-UFU 2550-56); Espigão
d’Oeste (AAG-UFU 2284-85); Adenomera bokermanni—BRAZIL: PARANÁ: Morretes (ZUEC 4722); Adenomera cf.
diptyx—BRAZIL: MATO GROSSO: Chapada dos Guimarães (AAG-UFU 2138–39); Cuiabá (AAG-UFU 2123); Santo
Antônio do Leverger (AAG-UFU 1435-38); Adenomera engelsi—BRAZIL: SANTA CATARINA: Rancho Queimado
(MNRJ 72637, 72543–44); Adenomera cf. hylaedactyla—BRAZIL: MATO GROSSO: Rondolândia (AAG-UFU 2621);
Adenomera marmotara—BRAZIL: RIO DE JANEIRO: Bangu (MNRJ 51091, 53817-18, 53820, 54081-82, 55684,
58132-38, 58140-42); Macaé (AAG-UFU 0529; 0756-57); Saquarema (MNRJ 76775, 76778–79); Adenomera cf.
marmorata—BRAZIL: MINAS GERAIS: Chiador (AAG-UFU 0688); SÃO PAULO: Santo André (AAG-UFU 3031);
São Sebastião (AAG-UFU 3007); Adenomera sp.—BRAZIL: MATO GROSSO: Pontal do Araguaia (AAG-UFU 0201,
0203); MINAS GERAIS: Perdizes (AAG-UFU 0609); Uberlândia (AAG-UFU 4633); GOIÁS: Caldas Novas (AAG-UFU
0018); Adenomera thomei—BRAZIL: BAHIA: Itabuna (ZUEC 998); Lithodytes lineatus—BRAZIL: AMAZONAS:
Itacoatiara (MNRJ 56699); Barcelos (MNRJ 36243); PARÁ: Piçarra (MNRJ 67289-90).
APPENDIX 2. Additional information on figured sound files.
FIGURE 3. A–B) Adeno_martinCachimboPA11TRC_AAGm671; 19:50 h, 29 Nov 2012; Cachimbo, State of Pará, Brazil; air
27.1°C; C–D) Adeno_martinCachimboPA2bTRC_AAGm671; 20:36 h, 28 Nov 2012; Cachimbo, State of Pará, Brazil; air
26.7°C;
FIGURE 9. A–B) Adeno_saciVeadGO6TRC_AAGm671; 00:40 h, 13 Nov 2012; Parque Nacional da Chapada dos Veadeiros,
State of Goiás, Brazil; air 21.3°C; C–D) Adeno_saciVeadGO3dAAGm; 18:25 h, 2 Dec 2010; Municipality of Alto Paraíso de
Goiás, State of Goiás, Brazil; air 23.3°C;
FIGURE 10. A–B) Adeno_saciCristalinaGO4aAAGm671; 18:20 h, 12 Feb 2013; Municipality of Cristalina, State of Goiás,
Brazil; air 26.0°C; C–D) Adeno_saciCristalinaGO1aAAGm671; 19:24 h, 20 Nov 2011; Municipality of Cristalina, State of
Goiás, Brazil; air 21.0°C;
FIGURE 11. A–B) Adeno_saciPontAragMT3eAAGm; 17:48 h, 18 Jan 2011; Municipality of Pontal do Araguaia, State of
Mato Grosso, Brazil; air 36.0°C; C–D) Adeno_saciAltoAragMT1TRC_AAGm671; 21:51 h, 24 Jan 2013; Municipality of Alto
Araguaia, State of Mato Grosso, Brazil; air 23.4°C.
APPENDIX 3. Mean individual values of the advertisement call temporal variables of topotypes (Cachimbo, Pará) of
Adenomera martinezi (mart) and four populations of Adenomera saci sp. nov. (saci) and their respective first principal
component scores (PC1). CD = call duration; II (intercall interval); CS = call rate (seconds); T = air temperature.
Individuals of Adenomera saci sp. nov. from the type locality (Chapada dos Veadeiros, Goiás) are in bold type. Values
were rounded to three decimal places.
CD (s) II (s) CS T (°C) PC1
mart1 0.107 0.393 1.778 26.7 0.28842443
mart2 0.106 0.353 2.182 26.7 -0.738348601
mart3 0.128 0.346 2.1 26.7 -0.327237565
mart4 0.134 0.414 2.111 26.7 0.172357479
mart5 0.112 0.434 2.0 24.6 0.181314505
mart6 0.108 0.481 1.9 24.6 0.612072058
mart7 0.125 0.530 1.7 24.6 1.534750878
mart8 0.112 0.394 2.0 24.6 -0.061385867
mart9 0.103 0.412 1.7 27.1 0.491545486
mart10 0.111 0.346 2.222 27.1 -0.791942721
mart11 0.120 0.541 2.2 27.1 0.59954086
mart12 0.142 0.342 2.1 27.1 -0.159742375
mart13 0.106 0.280 2.7 27.0 -2.179317965
mart14 0.121 0.322 2.3 24.8 -0.945991958
mart15 0.117 0.281 2.5 24.8 -1.637170398
saci1 0.117 0.304 2.333 25.3 -1.179614465
saci2 0.107 0.481 2.286 27.0 -0.134090913
saci3 0.133 0.418 1.889 25.3 0.597567371
saci4 0.116 0.345 2.0 25.3 -0.307357345
saci5 0.105 0.257 2.8 24.9 -2.518000721
saci6 0.103 0.408 1.8 21.3 0.280123952
saci7 0.103 0.318 2.4 20.0 -1.414140647
saci8 0.132 0.383 2.0 21.0 0.150086692
saci9 0.078 0.371 2.1 23.0 -0.862681307
saci10 0.116 0.263 2.667 26.0 -2.075013981
saci11 0.116 0.218 2.667 26.0 -2.349687639
saci12 0.139 0.473 2.0 27.0 0.805755531
saci13 0.195 0.349 2.0 36.0 0.813097476
saci14 0.185 0.354 1.7 26.0 1.281357695
saci15 0.164 0.403 2.0 27.5 0.724514872
saci16 0.178 0.508 1.8 27.5 1.956706363
saci17 0.186 0.317 2.0 28.0 0.486969434
saci18 0.224 0.382 1.6 28.0 2.182677989
saci19 0.188 0.686 1.1 23.4 4.522861399
APPENDIX 4. Eigenvectors, eigenvalues, and explained variation of the first three principal components of bioacoustic
variables of Adenomera saci sp. nov. populations.
BIOACOUSTIC VARIABLES PC1 PC2 PC3
CALL DURATION 0.4667 -0.0291 -0.8002
INTERCALL INTERVAL 0.3972 -0.5150 0.5027
RATE (CALLS/MINUTE) -0.4527 0.5048 0.0569
st
1 HARMONIC 0.4675 0.4572 0.2875
nd
2 HARMONIC 0.4483 0.5197 0.1452
EIGENVALUES 2.818 1.394 0.124
EXPLAINED VARIATION (%) 56.361 27.882 11.509

Decarvalho 2013

Uploaded by

Copyright:

Available Formats

Decarvalho 2013

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Decarvalho 2013

Uploaded by

Copyright:

Available Formats

Zootaxa 3701 (2): 207–237 ISSN 1175-5326 (print edition)

Taxonomic circumscription of Adenomera martinezi (Bokermann, 1956)

THIAGO RIBEIRO DE CARVALHO1,2,3 & ARIOVALDO ANTONIO GIARETTA1

dos Bandeirantes, 3900, 14040-901, Ribeirão Preto, São Paulo, Brasil

Accepted by M. Vences: 24 Jul. 2013; published: 19 Aug. 2013 207

Material and methods

Redescription of Adenomera martinezi (Bokermann)

Adenomera saci, new species

APPENDIX 1. Additional examined specimens.

APPENDIX 2. Additional information on figured sound files.

You might also like