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A New Species of Rhinella (Anura: Bufonidae) from Northeastern Brazil

Author(s): Igor Joventino Roberto, Lucas Brito, Maria Tereza C. Thom


Source: South American Journal of Herpetology, 9(3):190-199. 2014.
Published By: Brazilian Society of Herpetology
DOI: http://dx.doi.org/10.2994/SAJH-D-13-00028.1
URL: http://www.bioone.org/doi/full/10.2994/SAJH-D-13-00028.1

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South American Journal of Herpetology, 9(3), 2014, 190199


2014 Brazilian Society of Herpetology

A New Species of Rhinella (Anura: Bufonidae)


from Northeastern Brazil
Igor Joventino Roberto1,2,*, Lucas Brito2,3, Maria Tereza C. Thom4
1

Departamento de Cincias Fsicas e Biolgicas, Laboratrio de Zoologia, Universidade Regional do Cariri, Rua Coronel Antnio Luiz Pimenta, 1161,
CEP63105-000, Crato, CE, Brazil.
2 Laboratrio de Zoologia Experimental, Universidade Federal do Cear, Campus do Pici, CEP60455-760, Fortaleza, CE, Brazil.
3
Programa de Ps-Graduao em Ecologia e Recursos Naturais, Departamento de Biologia, Universidade Federal do Cear, Avenida Humberto Monte, 2977,
CEP60455-760, Fortaleza, CE, Brazil.
4 Departamento de Zoologia, Instituto de Biocincias, Universidade Estadual Paulista, Campus Rio Claro, Caixa Postal 199, CEP13506-900, Rio Claro, SP, Brazil.
* Corresponding author. E-mail: igorjoventino@yahoo.com.br

Abstract. We describe a new species of anuran belonging to the Rhinella crucifer species group, from a relictual Atlantic Forest fragment located at the Serra de Baturit mountain range, State of Cear, Northeastern Brazil. The new species is characterized by narrow and elongated
parotoid glands, overhanging the lateral edges of the body dorsally; a conspicuous fringe on the ventral surface of the tarsus; yellow marks
on the flanks of the posterior surface of thighs and cloaca; integument of the dorsum and limbs with round warts with many keratinized
black spines. Tadpoles have a kidney-shaped nostril, with a dorsal fin that begins low and rises acutely once passed by the body limits; oral
disc laterally emarginated, sub-marginal papillae clumped, dark papillae in some specimens. In addition, we describe call parameters of the
new species, provide information regarding its natural history, and comment on its conservation status.
Keywords. Advertisement call; Amphibian conservation; Natural history; Rhinella crucifer group; Tadpole.
Resumo. Descrevemos uma nova espcie de anuro pertencente ao grupo de Rhinella crucifer, proveniente de um fragmento de Mata Atlntica
relictual localizado na Serra de Baturit, estado do Cear, Nordeste do Brasil. Esta nova espcie caracterizada por possuir glndulas parotides estreitas e alongadas que ultrapassam os limites laterais do corpo dorsalmente; apresenta franja conspcua na superfcie ventral do tarso,
marcas amarelas nos flancos da superfcie posterior das coxas e cloaca; o tegumento do dorso e membros com verrugas redondas com muitos
espinhos queratinizados e escuros. O girino apresenta narina elptica em forma de rim, nadadeira dorsal que comea baixa e aumenta acentuadamente uma vez ultrapassados os limites do corpo; disco oral emarginado lateralmente, papilas sub-marginais agregadas, e presena de
papilas escuras. Ainda, descrevemos parmetros do canto de anncio da nova espcie, fornecemos informaes sobre sua histria natural, e
comentamos sobre o seu estado de conservao.

INTRODUCTION
The Rhinella crucifer species group is distributed
on the eastern part of South America, mostly in the Atlantic Forest of Brazil, Paraguay, and Argentina (Frost,
2014). Over the last ten years, knowledge regarding its
taxonomy has increased substantially. Baldissera et al.
(2004) conducted a taxonomic revision of the group using
morphological characters and morphometric analyses, revalidating R.ornata (Spix, 1824) and R.henseli (A. Lutz,
1934) and describing R.abei and R.pombali; the last species was synonymized with R.ornata and R.crucifer, as it
appears to be based on hybrids (Thom etal., 2012). VazSilva etal. (2012) described R.inopina, the only species of
the group that occurs outside the Atlantic Forest domain,
being restricted to Atlantic Forest enclaves and gallery
forest within the Cerrado Biome in the Brazilian states of
Bahia, Gois, and Tocantins. In a recent account, Thom
etal. (2012) used multilocus sequence data in association
to tree-based and allele frequency-based methods to describe the genetic structure within the R.crucifer species
group. Their findings included limited correspondence
between species defined in previous taxonomic studies
Submitted: 29 August 2013
Accepted: 16 October 2014
Published: December 2014

and groups delimited at the genetic level. Their study


also unveiled a genetically distinct population of R.crucifer from the Serra do Baturit mountain range, a natural
relict of the Atlantic Forest within the Caatinga biome in
Cear state, northeastern Brazil.
In this study, we examine the external morphology,
tadpole, and advertisement call of this population and describe it as a new species assigned to the Rhinella crucifer
group, endemic to a relict fragment of Atlantic Forest in
Northeastern Brazil. We also provide information regarding its natural history, geographic distribution, and conservation status.

MATERIALS AND METHODS


Type specimens are deposited at the Clio F.B.
Haddad collection in the Departamento de Zoologia
da Universidade Estadual Paulista Jlio de Mesquita
Filho, Campus de Rio Claro, SP, Brazil (CFBH). Examined specimens are housed in the following collections:
Adolpho Lutz Collection, Museu Nacional do Rio de Janeiro (MNRJ), Rio de Janeiro, Brazil; Clio F.B. Haddad

Handling Editor: Julin Faivovich


doi: 10.2994/SAJH-D-13-00028.1
ZooBank: urn:lsid:zoobank.org:pub:25D503DD-DA09-4E69-828D-58DC97DFDCDA

South American Journal of Herpetology, 9(3), 2014, 190199

Collection, Departamento de Zoologia da Universidade


Estadual Paulista Jlio de Mesquita Filho, Campus de
Rio Claro, SP, Brazil, and Herpetological Collection of Universidade Regional do Cariri (URCA-H), Crato, CE, Brazil.
Statistical summaries are reported as the mean SD.
Specimens examined for comparison are listed in the Appendix. Twenty three measurements were taken from
each specimen, following Baldissera etal. (2004) and VazSilva etal. (2012): snoutvent length (SVL); head length
(HL); head width (HW); inter-nostril distance (IND); eye
nostril distance (END); eye diameter (ED); upper eyelid
width (UEW); inter-orbital distance (IOD); eye border
to upper maxilla distance (EMD); canthal ridge length
(CRL); supra-tympanic ridge length (STR); eyetympanum distance (ETD); tympanum diameter (TD); tympanum height (TH); anterior distance between parotoid
glands (ANP); posterior distance between parotoid glands
(POP); forearm length (FAR); upper arm length (UAR);
inner carpal tubercle length (ICTL); inner carpal tubercle
width (ICTW); hand length (HAL); axillagroin distance
(AGD); thigh length (THL); tibia length (TBL); tarsal
length (TAL). We took measurements with a digital caliper to the nearest 0.1mm, and determined sex and maturity by visual inspection of secondary sexual characters
(such as nuptial pads, extended and pigmented vocal sacs
in males). Terminology for cranial crests follows Pramuk
(2006).
We analyzed 12 advertisement calls obtained from
two males (one collected; CFBH 28174) recorded at the
type locality. We recorded the calls with an OLYMPUS
S-11 digital tape recorder with internal microphone, and
digitized at 44.1 kHz, resolution of 16 bits (fast Fourier
transform =256 points resolution), using software Raven
Pro 1.1 (Bioacustic Research Program, 2011). We measured the following temporal parameters: call duration,
number of notes per call, note duration, intercall interval,
internote interval, and number of pulses per note. Measured spectral parameters include dominant, highest, and
lowest frequencies. Terminology for advertisement call
description follows Heyer et al. (1990). We collected 17
tadpoles (stages 3136; Gosner, 1960) in a small artificial lake at the type locality (see below) on 24 November
2010. We maintained some individuals in captivity until
metamorphosis to confirm species identification.
For the tadpole description we adopted measurements and terminology proposed by Altig and McDiarmid (1999): Total length (TL), body length (BL), body
width (BW), body height (BH), tail musculature height
(TMH), tail musculature width (TMW), eye diameter
(ED), inter-orbital distance (IOD), nostril diameter (ND),
inter-nostril distance (IND), eyenostril distance (END),
eyesnout distance (ESD), nostrilsnout distance (NSD),
spiraclesnout distance (SSD), and oral disc width (ODW).
We conducted all measurements with digital calipers (to
the nearest 0.1mm) with the aid of a stereomicroscope.
A New Species of Rhinella (Anura: Bufonidae) from Northeastern Brazil
Igor Joventino Roberto, Lucas Brito, Maria Tereza C. Thom

Examined tadpoles are housed in the Coleo de Girinos


da Universidade Federal do Cear (CGUFC L0137).
Stomach contents from 12 individuals of the new
species were obtained by stomach flushing, following
Sol and Rdder (2010). For details on search activity
and methods used in diet analysis, see Brito etal. (2012,
2013).

RESULTS
Rhinella casconi sp.nov.
(Figs.1,2)
Rhinella cruciferBaldissera etal., 2004: 260, 278
Rhinella cruciferBezerra and Cascon, 2011: 591
Rhinella cruciferThom etal., 2012
Holotype
CFBH28175, adult male, municipality of Guaramiranga, state of Cear, Brazil, collected on 24 November 2010 by I.J. Roberto and L. Brito (041517S,
385605W,866m above sea level [asl]).
Paratopotype
CFBH 28174, an adult male collected with the
holotype.
Paratypes
CFBH281702, three adult males, and one adult female (CFBH28173), collected by L. Brito; CFBH228635
juveniles, collected on 25 March 2009 by I.J. Roberto. All
from Parque das Trilhas, municipality of Guaramiranga,
state of Cear, Brazil (041558.97S, 385548.48W,
853masl).
Diagnosis
The species is assigned to the Rhinella crucifer group
by the presence of a row of keratinized tubercles along the
lateral edges of the body, with the first tubercle united to
the parotoid gland; presence of a row of tubercles at the
corners of mouth; presence of pre-ocular ridge; tympanum always visible; elliptical parotoid glands and granular dorsal integument; snout rounded in dorsal view;
and by phylogenetic reconstruction using mitochondrial
and nuclear data sequence data (Duellman and Schulte,
1992; Baldissera et al., 2004; Thom et al., 2012). Rhinella casconi sp.nov. is characterized by: head wider than
long; snout rounded in dorsal and lateral views; vocal sac
visible externally, not pigmented, subgular; narrow and
elongate parotoid glands overhanging lateral edges of

191

South American Journal of Herpetology, 9(3), 2014, 190199

body dorsally; hands large; presence of preorbital, postorbital, parietal, supraorbital crests; absence of suborbital
crest, presence of canthal, parietal and supratympanic
crests, absence of a pretympanic crest; thin vertebral line;
a conspicuous fringe on the ventral surface of the tarsus;

yellow marks on flanks of posterior surface of thighs and


cloaca in life and preservative; ventral region pale cream;
integument of the dorsum and limbs with round warts
with many keratinized black spines. Tadpole possess a
kidney-shaped nostril; dorsal fin begins low and gradually

Figure1. Rhinella casconi sp.nov. (CFBH28175; holotype). (A) Dorsal and (B) ventral views; (C) ventral view of left hand and arm; (D) ventral view of
left foot and leg; (E) lateral view of head and flanks.

192

A New Species of Rhinella (Anura: Bufonidae) from Northeastern Brazil


Igor Joventino Roberto, Lucas Brito, Maria Tereza C. Thom

South American Journal of Herpetology, 9(3), 2014, 190199

Figure2. Adult male of Rhinella casconi sp.nov. (CFBH28174), snout


vent length =87.9mm. Photo by Igor J. Roberto.

once passed the body limits; oral disc laterally emarginated; sub-marginal papillae clumped; presence of peculiar
darkened papillae in 35% of specimens analyzed (n=7).
The advertisement call consists of a series of multipulsed
notes, composed of 6167 notes per call, with 23 pulses
per note. Mean call duration is 2.9 s and the dominant
frequency is 861.31119.7Hz.
Comparisons with other species of the Rhinella
crucifer group
Rhinella casconi sp. nov. differs from R. ornata,
R.henseli and R.abei by possessing parotoid glands overhanging the edge of the body dorsally (not overhanging
in R. ornata, R. henseli and R. abei) and a fringe on the
ventral surface of the tarsus (vs. a row of small tubercles,
not forming a fringe in R.ornata, R.henseli and R.abei;
Baldissera et al., 2004). Rhinella casconi sp. nov. differs
from R.abei by the head being wider than long, with clear
division (vs. head slightly wider than long, without clear
division in R. abei); presence of yellow marks near the
cloaca, posterior surface of the thigh and flanks (absent
in R.abei); and immaculate ventral region (vs. sprinkled
with gray marks in R.abei; Baldissera etal., 2004). It differs from R.ornata by the presence of yellow marks near
the cloaca on the posterior surface of the thigh and on the
flanks (absent in R.ornata); and well developed vocal sac
(vs. moderately developed in R.ornata; Baldissera etal.,
2004). Rhinella casconi sp.nov. differs from R.henseli by
its larger size (vs. 51.663.9 mm in R. henseli males);
head wider than long (vs. approximately the same size in
R. henseli); first tubercle of the lateral row always fused
to the parotoid gland (vs. never fused in R.henseli); well
developed cranial crests (vs. inconspicuous in R.henseli);
and well developed vocal sac (vs. moderately developed
in R. henseli; Baldissera et al., 2004). Rhinella casconi
sp. nov. differs from R. inopina by possessing a parietal
A New Species of Rhinella (Anura: Bufonidae) from Northeastern Brazil
Igor Joventino Roberto, Lucas Brito, Maria Tereza C. Thom

crest (absent in R.inopina); well developed vocal sac (vs.


not visible externally in R.inopina); and large choanae (vs.
small in R.inopina; Vaz-Silva etal., 2012). Rhinella casconi
sp.nov. differs from R.crucifer by its well developed vocal
sac (vs. moderately developed in R.crucifer); narrow and
elongated parotoid gland (vs. wider and rounded parotoid
gland in R.crucifer), and presence of yellow marks on the
flanks, interior surface of the thighs and cloaca (absent in
R.crucifer; Baldissera etal., 2004). The tadpole of R.casconi sp.nov. can be differentiated from other described tadpoles in the group by the following aspects: presence of a
kidney-shaped nostril (oval in R.crucifer and R.abei; elliptical in R.ornata; Heyer etal., 1990; Fehlberg etal., 2012;
Ruas etal., 2012); dorsal fin begins low and rises gradually once passed the body limits (rises abruptly in R.ornata;
Heyer etal., 1990); sub-marginal papillae clumped; presence of dark papillae (unpigmented sub-marginal papillae
in other species; Heyer etal., 1990; Fehlberg etal., 2012;
Ruas etal., 2012).
Description of holotype
An adult male with body robust; clear division between head and body in dorsal view; head wider than long
(HW/HD = 1.16); snout rounded in dorsal and lateral
views; canthus rostralis well defined by a canthal crest, almost straight; loreal region slightly concave; nostrils lateral, near the snout tip; inter-nostril distance smaller than
eye-to-nostril distance (IND/END = 0.79); eye diameter
and upper eyelid width larger than tympanum diameter
(ED/TD=1.64; UEW/TD=1.48); eye-to-nostril distance
larger than eye diameter (END/ED=1.05); eye diameter
larger than upper eyelid width (ED/UEW = 1.11); preorbital and supraorbital crests developed; parietal and
post-orbital crests present; absence of suborbital crest;
tympanum large, vertically elliptical (TH/TD=1.18), with
a distinct annulus; presence of a supratympanic crest; absence of a pretympanic crest; parotoid glands large, narrow and elongated, overhanging the lateral edges of body
dorsally; first tubercle on the lateral row contacting the
parotoid gland; vocal sac visible externally, subgular, not
pigmented; choanae large, oval, widely separated; tongue
large, two times as long as wide, free behind, enlarged in
posterior portion. Forelimbs long, robust; forearm larger
than upper-arm (FAR/UAR=1.08); hands larger than forearm and upper arms (HAL/FAR=1.06; HAL/UAR=1.15);
slender fingers, not webbed, in order of size, IV<II<I<III;
lateral fringes poorly developed; finger tips slightly expanded; inner metacarpal tubercle elliptical, larger than
wide; external metacarpal tubercle rounded, smooth;
subarticular tubercle varying in size, rounded, single,
except by divided distal tubercle on Fingers III and IV, irregularly distributed on the ventral surfaces of hands and
fingers, nuptial pads on dorsal and lateral surfaces of fingers I and II, pigmented. Legs robust; tibia length greater

193

South American Journal of Herpetology, 9(3), 2014, 190199

Table1. Morphometric variables (in mm) of Rhinella casconi sp.nov. adults. Specimen numbers refer to CFBH catalogue numbers. All specimens are
paratypes except CFBH28175, which is the holotype (H). Abbreviations: Female (F); male (M); snoutvent length (SVL); head length (HL); head width
(HW); inter-nostril distance (IND); eyenostril distance (END); eye diameter (ED); upper eyelid width (UEW); inter-orbital distance (IOD); eye border
to upper maxilla distance (EMD); canthal ridge length (CRL); supra-tympanic ridge length (STR); eyetympanum distance (ETD); tympanum diameter
(TD); tympanum height (TH); anterior distance between parotoid glands (ANP); posterior distance between parotoid glands (POP); forearm length (FAR);
upper arm length (UAR); inner carpal tubercle length (ICTL); inner carpal tubercle width (ICTW); hand length (HAL); axillagroin distance (AGD); thigh
length (THL); tibia length (TBL); tarsal length (TAL).
MEASUREMENT
SVL
HL
HW
IND
END
ED
UEW
IOD
EMD
CRL
STR
ETD
TD
TH
ANP
FAR
UAR
ICTL
ICTW
HAL
AGD
THL
TBL
TAL
POP

20170 (M)
72.2
22.7
25.8
4.7
4.9
5.3
5.7
8.7
3.2
6.3
4.4
1.9
4.2
4.8
17
15.7
14.1
3.2
2.4
17.6
32.4
30.5
31.1
16.2
21.9

28171 (M)
66.3
21.1
24
4.7
5.3
4.9
5.4
8.1
3.3
5.7
3.7
1.4
3.3
4.3
14.2
14.1
13
3.2
2.2
17.4
29.5
29.3
29.9
15
23.5

28172 (M)
76.8
23.8
26.2
4.4
5.6
6.3
5.5
10.3
3.5
6.9
4.5
2.3
3.7
5.2
16.6
16.9
14.8
3.3
2.9
18.2
25.7
30.7
31.8
15.8
25.1

than thigh length (TBL/THL = 1.03); toes long; relative


lengths of toes I<II<V<III<IV; plantar webbing formula
I2-2II1-3III2-4IV-2V; inner metatarsal tubercle elliptical, protuberant; external metatarsal tubercle elongated;
conspicuous fringe along the ventral surface of the tarsus,
beginning close to the inner metatarsal tubercle and finishing before the tibia-heel articulation. Skin on dorsum,
flanks, and limbs with many irregularly distributed round
warts, with keratinized black spines on the tips.
Color of holotype in preservative
General color of body grayish light olive; thin vertebral line from the tip of the snout to cloaca light gray; bar
on the upper arm and the tibia darker gray; ventral region
cream olive; pale marks near cloaca, on posterior surfaces
of thighs, and in the lateral region from axillae to inguinal
region yellow.
Color in life (Fig.2)
General color of body brown; vertebral line inconspicuous, light gray; marks on undersurfaces of hind

194

28173 (F)
85.7
25.5
30.3
5.8
6.9
6.6
6.4
11
4.4
8.2
5.8
2.3
4.4
5.7
18.5
17.8
14.9
3
2.16
19.9
39.8
34
34
18
27.2

28174 (M)
87.9
26.6
30.4
5.3
5.6
7.4
6.3
11.8
4.2
8.3
5.1
2.6
4.2
5.9
19.8
18.6
15.3
3.26
2
20.1
36.4
31.5
37.1
19.9
30.1

28175 (M, H)
83.8
24.7
28.8
5.5
6.9
6.6
6
10.6
4.1
7.8
5.8
3
4
4.8
18.4
19.1
17.6
3.2
2
20.2
35.4
35.3
36.3
19.1
28.1

MEANSD (RANGE)
78.88.5 (66.387.9)
24.12 (21.126.6)
27.92.5 (2430.4)
5.10.5 (4.45.8)
5.90.8 (4.96.9)
6.20.9 (4.97.4)
5.90.4 (5.46.4)
10.10.5 (8.111.8)
3.80.5 (3.24.4)
7.21.1 (5.78.3)
4.90.8 (3.75.8)
2.30.6 (1.43)
40.4 (3.34.4)
5.10.6 (4.35.9)
17.41.9 (14.220)
171.9 (14.119.1)
14.91.5 (1317.6)
3.20.1 (33.3)
2.30.3 (22.9)
18.91.3 (17.420.2)
33.25.1 (25.740)
31.22.3 (29.335.3)
33.42.9 (29.937.1)
17.32 (1519.9)
263 (21.930.1)

limbs, cloaca and in the lateral line from the flanks to the
inguinal region yellow. Lateral band from behind the eyes
throughout the mid region of the body darker brown. Iris
gold. Ventral region pale cream.
Measurements of the holotype (mm)
SVL 83.8; HL 24.9; HW 28.8; IND 5.5; END 6.9;
ED6.6; UEW6.0; IOD10.6; EMD4.1; CRL7.8; STR5.8;
ETD3.0; TD4.0; TH4.8; ANP18.4; FAR19.1; UAR17.6;
ICTW 3.2; ICTL 2.0; HAL 20.2; AGD 35.4; THL 35.3;
TBL36.3; TAL19.1; POP28.10.
Variation
The variation in measurements of adults and juveniles is summarized in Tables 1 and 2. The juveniles of
Rhinella casconi sp.nov. (CFBH228637) present a more
conspicuous light vertebral line than the adults, and have
less granular tubercles on the dorsum than the adults.
The adult female (CFBH28173) has less developed keratinized warts on the skin, with a more conspicuous white
vertebral line on a brownish background.
A New Species of Rhinella (Anura: Bufonidae) from Northeastern Brazil
Igor Joventino Roberto, Lucas Brito, Maria Tereza C. Thom

South American Journal of Herpetology, 9(3), 2014, 190199

Table 2. Morphometric variables (in mm) of Rhinella casconi sp. nov.


juvenile paratypes. Abbreviations: Female (F); male (M); snoutvent
length (SVL); head length (HL); head width (HW); inter-nostril distance
(IND); eyenostril distance (END); eye diameter (ED); upper eyelid width
(UEW); inter-orbital distance (IOD); eye border to upper maxilla distance
(EMD); canthal ridge length (CRL); supra-tympanic ridge length (STR);
eyetympanum distance (ETD); tympanum diameter (TD); tympanum
height (TH); anterior distance between parotoid glands (ANP); posterior
distance between parotoid glands (POP); forearm length (FAR); upper
arm length (UAR); inner carpal tubercle length (ICTL); inner carpal
tubercle width (ICTW); hand length (HAL); axillagroin distance (AGD);
thigh length (THL); tibia length (TBL); tarsal length (TAL).
MEASUREMENT
SVL
HL
HW
IND
END
ED
UEW
IOD
EMD
CRL
STR
ETD
TD
TH
ANP
FAR
UAR
ICTL
ICTW
HAL
AGD
THL
TBL
TAL
POP

CFBH22863
44.2
13.9
15.9
3.3
3.2
3.9
3.7
5.4
1.9
3.9
2.3
0.8
2.6
2.3
8.8
9.7
8.4
1.6
1.2
11
16.5
19.2
17.9
9.5
12.2

CFBH22864
49.8
15.4
17.5
2.8
3.5
4
4.6
5.4
2.1
4
2.5
0.9
2.8
3.4
10.3
11.3
11
2.1
1.2
12.2
17.1
22.1
21.5
10.9
16.5

CFBH22865
41.3
13.7
15.3
2.6
3.4
3.9
3.2
5.3
2
3.8
2.4
0.7
3
3.1
9.2
9.1
8.3
1.5
1.2
9.3
15.5
19.6
17.6
9.5
13.7

Description of the tadpole (Fig.3)


Morphometric measurements are summarized in
Table3. The tadpoles of Rhinella casconi sp.nov. have an
oval body, being elliptical from a lateral view and compressed from a frontal view (BH/BW=0.69). The snout
is oval. Eyes are relatively small (ED/BW = 0.17) and
positioned dorso-laterally. Nostrils are relatively large
and visible both in dorsal and lateral views, closer to the
snout, and nearly oval with the inner margin with a kidney-shaped aspect; rims are slightly projected. The dorsal
fin begins with the tail musculature, increasing gradually
once past the hind part of the body. The tail musculature finishes slightly before the end tip of the tail, which
is rounded. The spiracle is short, sinistral, with an inner
wall mostly fused to the body, except near the tube opening; the inner wall is present and located at the last third
of the body (SSD/BL = 0.73). The vent tube is median;
both walls are connected to the ventral fin. The oral disk
A New Species of Rhinella (Anura: Bufonidae) from Northeastern Brazil
Igor Joventino Roberto, Lucas Brito, Maria Tereza C. Thom

Table 3. Morphometric variables (in mm) of Rhinella casconi sp. nov.


obtained from 17 tadpoles in stages 3136.
Characteristic
Tail length
Body length
Body width
Body height
Tail musculature height
Tail musculature width
Eye diameter
Interorbital distance
Nostril diameter
Inter-nostril distance
Eye-nostril distance
Eye-snout distance
Nostril-snout distance
Spiracle-snout distance
Oral disc width
A1
A2-i
A2-ii
Gap width
P1
P2
P3

MeanSD
20.071.24
7.990.61
5.590.34
3.880.34
1.720.18
1.000.12
0.960.12
2.470.17
0.410.05
1.250.09
1.300.13
2.650.20
1.330.14
5.830.42
2.100.13
2.010.13
0.830.11
0.860.09
0.170.05
1.680.09
1.640.1
1.550.11

Range
17.3422.15
6.388.86
4.686.16
3.14.44
1.292.03
0.721.21
0.741.15
2.142.74
0.330.5
1.061.38
1.031.53
2.163.04
1.081.52
4.876.57
1.842.37
1.742.16
0.570.93
0.70.95
0.120.25
1.461.79
1.471.79
1.381.73

is ventral and laterally emarginated; its width represents


37.6% of body width. Larval tooth row formula =2(2)/3;
P-2 is slightly longer than P-1 and P-3, which are similar
in size; the lower and upper jaw sheaths are V- and archshaped, respectively, both with a triangular serration; the
tip of the marginal papillae is rounded and forms a simple
row; the sub-marginal papillae are clumped. Seven individuals displayed unusually dark, almost black coloration
of some papillae (Fig.4). The exact areas presenting this
pattern varied among individuals, occurring on both marginal and/or sub-marginal papillae. Live tadpoles show
a dark brown coloration; the outer margins of the body
(snouteyes) are transparent; intestines visible; fins are
transparent; lower part of ventral tail musculature with
an uncolored stripe, except for the end of tail which is
all dark brown; after preservation tadpoles maintain the
same coloration, although becoming a bit fainter.
Advertisement call (Fig.5)
The advertisement call of Rhinella casconi sp. nov.
is a multipulsed type of call, with a mean duration of
2.9 0.4 s (2.23.8 s; n = 12; Table 4) and mean intercall interval of 8.64.3s (4.417s; n=8). The calls are
composed of 6167 notes/call, with a mean duration of
0.020.004s (0.0090.04; n=382) and mean internote
interval of 0.020.006s (0.0020.07; n=376). Each note
is composed of 23 pulses (mean=2.80.4; n=233). The
mean dominant frequency of the call is 911.677.6Hz
(861.31119.7Hz; n=12).

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South American Journal of Herpetology, 9(3), 2014, 190199

Etymology

Natural history

The specific name honors Professor Dr. Paulo Cascon, for his great contribution to the knowledge on
the amphibians of the state of Cear and the Caatinga
Biome.

Rhinella casconi was found in reproductive activity


in November of 2010, after the first heavy rains of the
2010/2011 rainy season. Males presented typical explosive breeding behavior (sensu Wells, 1977), vocalizing in
different microhabitats at the margins and inside temporary and permanent ponds and actively searching for
females. Bezerra and Cascon (2011) described the heteroespecific amplexus of Rhinella casconi with both Rhinella jimi and Leptodactylus vastus in the Serra de Baturit
mountain range.
During the remaining rainy season and next dry season, adults of R.casconi were rare. Juveniles were sometimes found at forest edges and in its interior. Our observations suggest R.casconi is a forest species, not occurring
in open environments like the congener R. jimi.
Number of prey per stomach ranged from 134.
Main prey items were insects from the family Formicidae
and order Coleoptera, accounting for 70% and 11% of all
prey, respectively. Other items were consumed, although
in lower proportions, including arthropods of the orders
Diptera, Orthoptera, Hemiptera, Isoptera, Araneae and
Acari.
Geographic distribution
Rhinella casconi sp. nov. is endemic to the Serra
de Baturit mountain range and occurs at elevations
>700masl.

DISCUSSION

Figure3. Tadpole of Rhinella casconi sp.nov. From top to bottom: lateral


(left), dorsal, and ventral views and detail of kidney-shaped nostrils.

Rhinella casconi sp. nov. differs genetically from


R.ornata, R.henseli, R.crucifer and R.abei in mitochondrial DNA by phylogenetic reconstruction and nuclear
DNA by allele frequency-based assignment analysis, and

Figure4. Oral disc of Rhinella casconi sp.nov. showing (A) unpigmented and (B) pigmented (black) papillae.

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A New Species of Rhinella (Anura: Bufonidae) from Northeastern Brazil


Igor Joventino Roberto, Lucas Brito, Maria Tereza C. Thom

South American Journal of Herpetology, 9(3), 2014, 190199

Table4. Acoustic parameters of the advertisement calls of the Rhinella casconi sp.nov. Statistical summaries given as meanSD (minimummaximum; n).
CFBH28174

Unvouchered specimen

Pooled values

Call duration (s)

Acoustic parameters

2.90.3 (2.23.2; 7)

2.90.5 (2.33.8; 5)

2.90.4 (2.23.8; 2)

Intercall interval (s)

6.72.5 (4.410.6; 6)

14.23.9 (11.517; 2)

8.64.3(4.417; 8)

Notes

64.52.5 (6167; 4)

6163

63.72.4 (6167; 6)

Pulses/note

2.70.4 (23; 120)

2.80.4 (23; 113)

2.80.4 (23; 233)

Note duration (s)

0.020.004 (0.0090.03; 262)

0.030.004 (0.020.04; 120)

0.020.004 (0.0090.04; 382)

Internote interval (s)

0.020.004 (0.010.06; 258)

0.010.008 (0.0020.07; 118)

0.020.006 (0.0020.07; 376)

861.30.12 (7)

981.977 (947.51119.7; 5)

911.677.6 (861.31119.7; 12)

Dominant Frequency (Hz)


Lower Frequency (Hz)

51050.2 (466.15877; 7)

470.878.5 (392.3549.3; 5)

493.763.4 (392.3587.7; 12)

Higher Frequency (Hz)

1167.119.6 (1134.91195.7; 7)

2087.3251.8 (16472275; 5)

1550.5497.8 (1134.92275.6; 12)

in both data by hierarchical multivariate factorial analysis (Thom et al., 2012). No phenotypic synapomorphy
is known for the R.crucifer group. Therefore, we rely on
previous genetic analyses attesting to the monophyly of
this group for the inclusion of R.casconi sp.nov. (Thom
etal., 2012).
There are many morphological and ecological similarities between Rhinella casconi sp.nov. and other species
in the group, including aspects of the advertisement call,
tadpole morphology, diet, and breeding behavior (Heyer
etal., 1994; Ferreira and Teixeira, 2009; Ruas etal., 2012).
These species also have relatively low levels of genetic divergence (Thom etal., 2010, 2012).
Morphological characters seem to be rather conserved among tadpoles of Rhinella casconi sp.nov., greatly

Figure5. Advertisement call of Rhinella casconi sp.nov. (A) Waveform


(above) and corresponding spectrogram (below) of a single call. (B)
Expanded waveform (above) and corresponding spectrogram (below)
showing six notes, each composed of three pulses.
A New Species of Rhinella (Anura: Bufonidae) from Northeastern Brazil
Igor Joventino Roberto, Lucas Brito, Maria Tereza C. Thom

resembling the tadpole of other pond-dwelling species


within the genus. Both external and cranial morphology
are extremely conservative in Rhinella tadpoles (see Kolenc etal., 2013; Oliveira etal., 2014).
Advertisement calls of the Rhinella crucifer species
group are usually not sufficient to allow differentiation
among species within the group, with overlapping occurring at most of the parameters (see Loureno etal., 2010;
Oliveira etal., 2014). The same occurs with the advertisement call of R.casconi sp.nov.
The natural relicts of the Atlantic Forest in northeastern Brazil (Serra de Baturit, Serra de Maranguape,
Serra da Aratanha, and Serra da Ibiapaba mountain ranges) shelter the most diverse and endemic herpetofauna of
Cear state (Borges-Nojosa and Caramaschi, 2003; Loebmann and Haddad, 2010). The endemic species occurring
in those forest fragments, such as Leposoma baturitensis,
Placosoma sp., Atractus Ronnie, Adelophryne baturitensis,
and Ad. maranguapensis, are more related to species in
the Amazon and Atlantic Forest biomes than to species in
the surrounding Caatinga biome (Rodrigues and Borges,
1997; Passos etal., 2007; Fouquet etal., 2012). The same
occurs with Rhinella casconi sp.nov. and its close relatives
distributed throughout the Atlantic Forest biome, reinforcing the idea that these fragments were once connected. These relicts are forest refuges probably isolated during the late Tertiary/early Quaternary period, suggesting
a role of past habitat shifts in promoting speciation in
these areas (Vanzolini, 1981).
Ribeiro etal. (2009) analyzed the spatial distribution
of the existing Brazilian Atlantic Forest, and estimated
that only 13,656 ha (ca.16%) of the original distribution
of the northeastern natural relics still remains. Currently
Rhinella casconi sp.nov. is only known for the Serra de Baturit mountain range. This species, along with the biota
of these relicts share the same major threat, which is a
combination of restricted distribution and rapid habitat
loss. At the Serra de Baturit mountain range, deforestation for construction of human settlements and banana
plantations are the major agents (I.J. Roberto, personal
observation). Conservation units in the region are mainly
in the Natural Heritage Private Reserve (RPPN) category,

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South American Journal of Herpetology, 9(3), 2014, 190199

with the majority being precariously maintained and


playing a minor role in habitat conservation. Rhinella casconi has never been found in the forest remnants of Planalto da Ibiapaba (Loebmann and Haddad, 2010), Serra de
Maranguape or Serra da Aratanha (I. J Roberto, personal
observation), and can be considered endemic to the Serra
de Baturit mountain range. Following the criteria of the
IUCN, we suggest the status of Rhinella casconi as vulnerable B1 ab (iii, iv) due to the extent of occurrence estimated being less than 20,000 km2, in severely fragmented
habitat.

ACKNOWLEDGMENTS
We are grateful to C.F.B. Haddad (UNESP), J.P. Pombal Jr. (MNRJ), and R.W. vila (URCA) for loaned specimens under their care, Taran Grant, Julian Faivovich,
and two anonymous referees for critical review and help
improving the manuscript, W.R. Heyer for reviewing the
English version of the manuscript, Mirco Sol and Renan
Oliveira for providing calls of Rhinella crucifer from Bahia,
and Felipe Monteiro for elaborating the tadpole plates.
IJR thanks FUNCAP for a scholarship. LB received a grant
from Conselho Nacional de Desenvolvimento Cientfico
e Tecnolgico (CNPq Process no. 371469/2012-0) and
scholarship from CAPES. Authorization for capture of
live individuals was provided by the Instituto Brasileiro
do Meio Ambiente (license number: 19331-1).

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Igor Joventino Roberto, Lucas Brito, Maria Tereza C. Thom

South American Journal of Herpetology, 9(3), 2014, 190199

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APPENDIX
Specimens examined
Rhinella abei: BRAZIL: Santa Catarina: Santo Amaro da Imperatriz: MNRJ 744602.
Rhinella crucifer: BRAZIL: Rio de Janeiro: Lagoa de Lima, Campo dos Goytacazes: MNRJ 570589; Pernambuco: RPPN
Pedra DAntas, Lagoa dos Gatos: URCA 4144, 4154, 4268; Alagoas: REBIO Pedra Talhada, Quebrangulo: URCA 42694271.
Rhinella henseli: BRAZIL: Rio Grande Do Sul: Parque de Agronomia, Porto Alegre: MNRJ 67231, 67234, 67242.
Rhinella ornata: BRAZIL: Rio de Janeiro: Nova Friburgo: MNRJ 61992, 61994, 62006.

A New Species of Rhinella (Anura: Bufonidae) from Northeastern Brazil


Igor Joventino Roberto, Lucas Brito, Maria Tereza C. Thom

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