Journal of Herpetology, Vol. 41, No. 4, pp. 566–580, 2007
Copyright 2007 Society for the Study of Amphibians and Reptiles
Taxonomic Review of Allobates (Anura, Aromobatidae) from the
Atlantic Forest, Brazil
VANESSA K. VERDADE1
AND
MIGUEL T. RODRIGUES
Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Caixa Postal 11461, CEP 05422–970,
São Paulo, Brazil
ABSTRACT.—We present the results of a taxonomic review of the four species of Allobates endemic to the
Atlantic Forest Domain in Brazil. A total of 880 preserved specimens from 29 localities covering their range in
Atlantic Forest were studied based on external attributes. Characters formerly described as diagnostic in
original descriptions and others cited for dendrobatids in the literature were studied along the total
geographic range of the populations of these species, including the type localities. We found no discrete
characters, qualitative or quantitative, capable of differentiating the species. Most local and geographic
variation was limited to snout-vent length and color pattern. Considering the lack of evidence otherwise, we
use the results of our morphological analysis to allocate all Atlantic Forest species of Allobates to synonymy
with Allobates olfersioides.
Dendrobatids are a monophyletic group of
frogs that are mostly known for their bright
color and poisonous skin. Nevertheless, about
half of the species are cryptically and dull
colored, presumably nontoxic and until recently
(Grant et al., 2006) placed in the genus Colostethus sensu lato. There had been about a hundred recognized species in the genus ranging
from Nicaragua to southeastern Brazil (Frost,
2006). The systematics of the family has recently
gone through significant changes (Grant et al.,
2006) supported by a molecular and morphological based phylogeny. The family Dendrobatidae, as previously known, corresponds now to
Dendrobatoidea, which includes the families
Aromobatidae and Dendrobatidae. The four
species of Colostethus from Atlantic Forest,
now allocated to the genus Allobates, are placed
in the family Aromobatidae.
The Brazilian species of Allobates are leaf litter
inhabitants of forests and can be found throughout the Amazon Basin, Brazilian Savannas, and
Atlantic Forest. Most of the 17 currently
recognized species are Amazonian and described recently, probably as a consequence of
a vast and poorly sampled territory along with
increased knowledge of the natural history of
these frogs (e.g., Morales, 2000; Lima and
Caldwell, 2001; Caldwell and Lima, 2003). There
are four species in eastern Brazil, endemic to the
Atlantic Forest Domain (Ab’Saber, 1977): Allobates alagoanus (Bokermann, 1967), Allobates
capixaba (Bokermann, 1967), Allobates carioca
(Bokermann, 1967), and Allobates olfersioides
(Lutz, 1925).
1
Corresponding Author. E–mail: [email protected]
Allobates olfersioides was described as Eupemphix olfersioides Lutz, 1925 from the coastal
region of the state of Rio de Janeiro (RJ).
Cochran (1955) considered it a synonym of
Phyllobates brunneus Cope, 1887. Bokermann
(1966) restricted the type locality of A. olfersioides to Angra dos Reis (RJ) and, in 1967,
described the other three Atlantic Forest species:
Phyllobates alagoanus from Usina Sinimbu, Mangabeiras, state of Alagoas; Phyllobates capixaba
from Lagoa do Macuco, Refúgio Sooretama,
Linhares, state of Espı́rito Santo; and Phyllobates
carioca from Represa Rio Grande, Jacarepaguá,
Rio de Janeiro, state of Rio de Janeiro. Bokermann (1967) also considered P. olfersioides related to P. alagoanus, P. capixaba and P. carioca.
Edwards (1974) placed these four species in
Colostethus, as did Silverstone (1975). Grant et al.
(2006) based on an extensive sampling and
molecular plus morphological based phylogeny
allocated them to the genus Allobates.
The four species are very similar in external
attributes and were described based on small
and geographically remote samples. The characters used by Bokermann (1967) to separate
these species were basically color pattern,
length of limbs and fingers, size of carpal and
tarsal tubercles, shape of head, and snout-vent
length. All of these characters are presumably
subject to geographical variation, a possibility
that could not be tested at that time.
Bokermann (1967) also presented information
on call variation, pointing out that the calls of A.
capixaba and A. carioca were distinct from that of
A. olfersioides, but, except for saying that the call
of A. capixaba was more spaced than those of A.
olfersioides, no further description was given.
Besides, the putative call differences between
TAXONOMIC REVIEW OF ALLOBATES FROM THE ATLANTIC FOREST
species were reported by the collector (F. M.
Oliveira) and not based on the authors’ field
experiences or knowledge. The main characteristics of the advertisement call of Allobates (a trill
or an acute buzz) can vary in fundamental
frequency, number of pulses and spacing,
according to environmental conditions and
sometimes, as a function of population density
(Coloma, 1995; Juncá, 1998; Grant and Rodriguez, 2001; Caldwell et al., 2002a). Considering
the subjective call differences reported and their
variation, we think that the evidence alone is
weak to keep the Atlantic Forest species of
Allobates separated. Moreover, the observations
on vocalization pointed out in the species
description refer only to the surroundings of
the type locality, and geographical variation of
call should be considered. Unfortunately, we
were unable to find available calling records in
collections, either institutional or personal, and
our attempts to get new ones failed. Because
this problem will probably persist in the future,
because the Atlantic Forest species of Allobates
are showing declines (Weygoldt, 1989; Izecksohn and Carvalho-e-Silva, 2001), specimens
gathered in collections will be the main source
for studying species limits of this complex in the
Atlantic Forest. Indeed, the samples collected
during the last 40 years are a source of new data
on morphological variation that could clarify
the similarities and differences among the four
species of Allobates from Atlantic Forest.
We present, herein, a detailed study of the
morphological variation of these populations
along a latitudinal gradient that includes the
type localities of the presently recognized
species. We assume that external morphology
is the strongest available source of data sustaining the Atlantic Forest species of Allobates, and,
if we found no discrete differences in morphological characters among populations, they
should be considered synonyms until new
sources of data can be explored.
MATERIALS AND METHODS
To cover their total range, 880 preserved
specimens of Allobates from 29 localities were
studied (Fig. 1, Appendices 1 and 2). All specimens were observed regarding external morphology. We measured and classified 396
individuals to be used in the statistical analysis.
This number comprises all individuals from
localities with N below 100 and 100 randomly
picked up individuals from localities with N
above 100. Twenty-two measurements were
obtained for the specimens included in the
analysis: snout-vent length (SVL); thigh length
(THL) from the middle of the cloacal opening to
the outer edge of the flexed knee; tibia length
567
FIG. 1. Geographic distribution of Atlantic Forest
Allobates. Open circles represent the type localities of
the four currently admitted species. Numbers are the
localities sampled (see Appendix 2). The OTUs
studied are indicated by OTU1, 2, 3, and 4.
(TIL) from the outer edge of the flexed knee to
the heel; foot length (FOL) from the heel to the
tip of toe IV; head width (HW) between the
angle of jaws; head length (HL) perpendicular
to the imaginary line linking the angle of jaws to
the tip of the snout; internarial distance (IND)
between the inner edge of the nares; eye-nostril
distance (END) from the anterior corner of the
eye to the outer edge of the nostril; eye diameter
(ED) from posterior to anterior corners; tympanum diameter (TD) from posterior to anterior
edges; interorbital distance (IOD) between the
inner edges of the eyelids; hand length (HAL)
dorsally from the junction of radio-ulna and
carpal to the tip of the finger III; thumb length
(TBL); second, third, and fourth fingers length
(FL2, FL3, FL4) dorsally from the base to the tip
of the finger; third finger diameter (TFD)
dorsally at the distal edge of the second finger
tubercle; greatest length of the inner and outer
carpal tubercles (ICT, OCT); and greatest length
of the inner and outer metatarsal tubercles
(IMT, OMT).
All measurements were taken on the left side
of the specimens. The measurements were
obtained with a stereomicroscope except for
SVL, taken by a dial caliper, to the nearest of
0.01 mm. The axis of the greatest length at ICT,
OCT, IMT, and OMT variables was the same for
all specimens.
Qualitative characters studied were: shape of
the snout (dorsal, ventral, and lateral views);
pattern of the lateral dark stripe between the
568
V. K. VERDADE AND M. T. RODRIGUES
FIG. 2. Schematic drawing of an Allobates with the
nomenclature used for the study of color pattern of
the specimens.
nares and the eyes; color pattern of the upper
lip; presence of a median lingual process (Grant
et al., 1997, 2006); color pattern of the belly;
color pattern on dorsal view; pattern of distribution of tubercles; pattern of dark stripes on
groin; pattern of the dorsolateral and lateral
light stripes; pattern of the lateral dark stripe
(Fig. 2); cloacal stains; color pattern of the thigh;
presence/absence and extension of metatarsal
fold; and toe webbing.
To make sure that there were no extralimital
specimens belonging to other species in our
sample, and that the Atlantic Forest species
were restricted to the study area, we diagnosed
them from all other Brazilian species (Sociedade
Brasileira de Herpetologia, 2005) previously
placed in the genus Colostethus (now in the
genera Allobates, Anomaloglossus, and Hyloxalus),
based on literature and direct examination
when possible: Allobates brunneus (Cope, 1887);
Allobates caerulodactylus, (Lima and Caldwell,
2001); Allobates conspicuus (Morales, 2000); Allobates crombiei (Morales, 2000); Allobates fuscellus
(Morales, 2000); Allobates gasconi (Morales,
2000); Allobates goianus (Bokermann, 1975);
Allobates granti (Kok et al., 2006); Allobates
marchesianus (Melin, 1941); Allobates masniger
(Morales, 2000); Allobates nidicola (Caldwell and
Lima 2003); Allobates sumtuosus (Morales, 2000);
Allobates vanzolinius (Morales, 2000); Anomaloglossus beebei (Noble, 1923); Anomaloglossus
stepheni (Martins, 1989); Anomaloglossus tamacuarensis (Myers and Donnelly 1997); and
Hyloxalus peruvianus (Melin, 1941). We decided
to diagnose them also from Allobates trilineatus
(Boulenger, ‘‘1883’’ 1884) and Anomaloglossus
degranvillei (Lescure, 1975), considering their
distribution close to Brazil (Grant and Rodriguez, 2001; Frost, 2006).
The abbreviations for the herpetological collections consulted for preserved specimens and
call records are presented throughout the text as
follows: EI (Eugênio Izechson collection, Universidade Federal Rural do Rio de Janeiro,
UFRRJ); JJ (Jorge Jim collection, Universidade
Estadual de São Paulo, UNESP); MNRJ (Museu
Nacional do Rio de Janeiro); MUFAL (Museu da
Universidade Federal de Alagoas); MZUSP
(Museu de Zoologia da Universidade de São
Paulo, currently including the Werner Bokermann collection, WCAB); UEFS (Universidade
Estadual de Feira de Santana); UFPB (Universidade Federal da Paraı́ba); UFRJ (Universidade
Federal do Rio de Janeiro); USNM (United
States National Museum); ZUEC (Museu de
História Natural, Universidade de Campinas,
UNICAMP).
There were no obvious secondary sexual
characters to differentiate males and females
among the four species studied. To avoid
damage caused by dissection we checked for
morphometric differentiation between sexes
only in a sample from Tijuca, Rio de Janeiro.
Forty-four adult individuals (checked by maturity of gonads) from a total of 400 were
dissected, and 20 males and 20 females were
compared under a Student t-test at a 95%
interval of confidence.
Three samples of tadpoles identified by the
presence of nursery adults or young metamorphs were available for study—Ilhéus (Ba),
Una (Ba), and Tijuca (RJ). These samples
contained specimens in different developmental
stages and were not suitable for geographical
comparison. Tadpoles from Tijuca (RJ) were
used to describe the larvae following Altig and
McDiarmid (1999) standard measurements and
descriptive terminology.
Statistical Analysis.—Specimens were first
observed and compared within localities to
detect possible cases of sympatry, and then
observed and compared among localities following a north-south transect. In addition, we
ran a preliminary stepwise Discriminant Analysis to assess differences among localities
treated as individual operational taxonomic
units (OTUs) and considering the only case of
sympatry suggested in the literature (Allobates
olfersioides and A. carioca; Bokermann, 1967) as
individual units. The observational and statistical results were subsequently considered to
group the specimens in four OTUs, based on
overall similarity and geographical distribution.
The OTUs are also congruent to the gaps
observed in the geographical distribution of
the four species considered together (Fig. 1).
The specimens from the states of Alagoas and
Sergipe were treated as OTU1 (N 5 57), specimens from the state of Bahia as OTU2 (N 5 68),
specimens from the state of Espı́rito Santo as
OTU3 (N 5 11), and specimens from the state of
Rio de Janeiro as OTU4 (N 5 260; Fig. 1).
Statistics were obtained for each OTU.
The absence of obvious sexual characters
made it difficult to classify the specimens as
TAXONOMIC REVIEW OF ALLOBATES FROM THE ATLANTIC FOREST
young or adults. To minimize deviations of the
means, we chose not to use very small specimens. As a criterion of SVL exclusion, we used
the SVL average less the standard deviation of
the OTU 1, which presented the smallest
individuals. The value obtained was 11.4 mm.
All the specimens with SVL equal to or smaller
than 11.4 mm were excluded from the subsequent quantitative analysis, which left us with
372 specimens to be statistically analyzed: OTU
1 (N 5 44), OTU 2 (N 5 66), OTU 3 (N 5 10),
and OTU 4 (N 5 252). None of the samples
presented normal distributions for all variables,
even with data log-transformed, but deviations
were not severe enough to prevent parametric
tests.
As an attempt to express differences in shape
among individuals in different samples, some
body ratios were used in addition to the raw
measurements. They are THL/SVL, HAL/SVL,
FOL/SVL, HW/HL, END/HL, ED/HL, TD/
HL, TD/ED, IND/HW, TBL/FL2, FL2/HAL,
and FL4/HAL.
To classify the specimens, three stepwise
Discriminant Analyses were run separately
based on the morphological measurements,
body ratios, and qualitative data. The number
of steps was unspecified, and all groups were
assigned to equal probabilities before analysis.
Sexual dimorphism for the Tijuca sample was
assessed by the Student t-test on each variable
and body ratio at a confidence interval of 95%.
Means are given 6 1 SD.
RESULTS
All localities sampled are restricted to the
coastal region of eastern Brazil. The locality
farthest north is Novo Dino, state of Alagoas
and the farthest south is Angra dos Reis, state
of Rio de Janeiro. The farthest west locality is
Baixo Guandu in state of Espı́rito Santo. There
are two major gaps along the north-south
transect. One between Areia Branca in the state
of Sergipe and Elı́sio Medrado, state of Bahia,
and the other between Santa Teresa, state of
Espı́rito Santo and Teresópolis, state of Rio de
Janeiro. These areas correspond to drier environments. In the north, the coastal region is
composed by fixed sand dunes, but there are
many forested regions that could conceal the
species. The southern region is still covered by
forests. It seems more probable that the absence
of samples of Allobates from these areas is an
artifact of collection (Heyer, 1988).
Qualitative Data.—All individuals present
a rounded snout tip in dorsal and lateral views
with nares slightly prominent and an upper jaw
projecting slightly above the lower jaw. The
general shape of the snout in dorsal view
569
resembles a trapezoid; the body is slender and
elliptical (Fig. 3A, B). The dorsal skin is generally smooth, but inconspicuous tubercles may
be present at the inguinal region or throughout
the entire dorsum.
Dorsal pattern consists of a reddish-brown
background over which are darker stripes that
cross once or more at the middle of the dorsum,
suggesting intercrossing Xs. Dorsal pattern can
vary from uniform to highly pigmented (Fig. 4;
for summary, see Table 1). Individuals with
a uniform dorsum are more frequent (about
15%) in samples from the state of Bahia (OTU 2)
but still occur in lower rates in other samples (,
1% from the State of Rio de Janeiro, OTU 4).
Individuals with a single X on the dorsum are
more common (74%) in the states of Alagoas
and Sergipe (OTU 1), but specimens with
multiple X also occur in these samples (24%).
The multiple-X pattern is the most common in
OTU 2, 3, and 4, present in about 40, 80, and
90% of the individuals, respectively (Table 1).
There is some variation in this pattern. Sometimes the largest X has longer arms that barely
touch each other. This variation is found in
individuals from samples from the states of
Espı́rito Santo (OTU 3) and Rio de Janeiro (OTU
4) and is more common among the former
(45%). The dorsal parts of the thigh and tibia
have two or three dark stripes bordered by
lighter ones in almost all specimens examined.
In some individuals, the dark stripes are much
narrower, almost a line, in others the stripes are
absent.
Laterally, all individuals present a dark stripe
from the tip of the snout to the groin, involving
the nares and partially the eyes along the side of
the body (Fig. 5). Apparent north-south variation exists in the width and definition of this
stripe. Following the north-south transect, there
is a tendency of the dark lateral stripe to become
wider with a crescent reticulation toward the
venter and inguinal region (Fig. 6). Individuals
from the state of Espı́rito Santo (OTU 3) are the
ones in which this characteristic is more pronounced. To the south, the dark lateral stripe
reverses to solid in individuals from northern
Rio de Janeiro (OTU 4), but it is still wide. At the
southernmost localities, the lateral stripe is
narrower and solid, as observed in individuals
from the state of Alagoas, Sergipe (OTU 1) and
Bahia (OTU 2).
The dark lateral stripe can be dorsally
bordered by a narrow pale stripe that varies in
length and continuity. Most of the individuals
(97%) from the state of Alagoas (OTU 1) do not
present the pale dorsolateral stripe (Table 1).
When it occurs, it is present from the eyes to the
arms. The pale dorsolateral stripe is not present
in 57% of the individuals from the state of Bahia
570
V. K. VERDADE AND M. T. RODRIGUES
FIG. 3. Allobates olfersioides (MNRJ 5094): (A) dorsal and (B) lateral views of head, ventral views of (C) right
hand and (D) left foot.
(OTU 2) and can be observed from the eyes to
the arms in 36% of them and from the eyes to
the groin in 7%. In the state of Espı́rito Santo
(OTU 3), all individuals present the pale
dorsolateral stripe. It is observed from the eyes
to the arms in 9% of them and from the eyes to
the groin in 91% of them. To the south, only
16% of the individuals from the state of Rio de
Janeiro (OTU 4) present the pale dorsolateral
stripe.
Individuals from the states of Alagoas and
Sergipe (OTU 1) commonly (62%) have venter
pigmentation restricted to the throat, never
extending from throat to groin (Table 1). Samples of state of Bahia (OTU 2) specimens with an
immaculate venter are more frequent (57%).
There are two equally common patterns of
venter pigmentation in individuals from the
states of Espı́rito Santo (OTU 3) and Rio de
Janeiro (OTU 4). Venter pigmentation extends
to the pectoral or inguinal regions in about 30%
of individuals in both states. The general color
pattern is highly variable, and we did not find
any geographical consistency or discrete local
variation to justify partitioning of the samples.
Quantitative Data.—It was impossible to diagnose populations studied and refer them to
any of the recognized species based on body
proportions or the following diagnostic characters pointed out in literature: SVL, ratio of
length of the thumb and the second finger,
absolute length of the fourth finger, and shape
of the tarsal tubercle (Bokermann, 1967; Edwards, 1974; Rivero, 1988; Morales, 2000).
Table 2 presents the descriptive statistics for
the main measurements taken for individuals in
the four OTUs.
Individuals from the states of Alagoas and
Sergipe (OTU 1) are smaller (t df 5 107 5 26.316,
P 5 0.000) than those from the state of Bahia
TAXONOMIC REVIEW OF ALLOBATES FROM THE ATLANTIC FOREST
571
on body ratios are presented in Figure 8. The
first and second discriminant functions explain
98% of the differences among the OTUs. The
most important variable on function 1 is TBL/
FL2 and on function 2 is FL4/HAL. The
variation of the values of the TBL/FL2 and
FL4/HAL for each locality from north to south
can be seen in Figure 9. The shape of the tarsal
tubercle shows variation, and individuals from
the same sample can have a lump, or a straightor comma-shaped ridge.
We tried to rearrange the localities into
different OTUs, following, for example, the main
river barriers (e.g., São Francisco, Jequitinhonha,
Doce, and Paraı́ba do Sul), but the results were
always similar. None of the measurements or
proportions studied presented evidence to separate specimens into different groups.
FIG. 4. Dorsal view of adult Allobates olfersioides
showing variation on dorsal color pattern.
(OTU 2; Table 2). Individuals from the state of
Bahia (OTU2) are larger (t df 5 74 5 22.324, P 5
0.023) than individuals from the state of Espı́rito
Santo (OTU 3). Mean of SVL of individuals from
the states of Espı́rito Santo (OTU3) and Rio de
Janeiro (OTU 4) are not different (t df 5 260 5
20.042, P 5 0.389). Despite statistically significant OTUs, differences in individuals SVL
among localities are not clear when visualized
in a graphic of dispersion (Fig. 7). The smallest
maximum sizes are found among individuals
from the State of Espı́rito Santo, but it represents
the smallest OTU (N 5 10), with localities
poorly sampled.
The results of the discriminant analysis based
on both raw measurements and body ratios
show overlap among the four operational units.
The results for the discriminant analysis based
TAXONOMIC CONCLUSION
Our study of Allobates from the Atlantic
Forest made it clear that the characters currently
used to differentiate the recognized species
were not useful in our sample (Bokermann,
1967; Edwards, 1974; Rivero, 1988; Morales,
2000). Variation in SVL throughout their distributions is probably a result of restricted
sampling in some of the localities (Fig. 7). The
data also show that the relative lengths of the
thumb, second, and fourth fingers are highly
variable, as already found for other species of
Allobates (Grant and Castro, 1998). Diagnostic
differences between species are probably misinterpretations based on limited series.
The only record of sympatry among the
Atlantic Forest Allobates was published by
Bokermann (1967) from Represa Rio Grande,
state of Rio de Janeiro, where A. olfersioides and
A. carioca were found. This sample, presently at
MZUSP, includes 19 specimens, three of which
were identified by Bokermann as A. carioca (the
holotype and the two paratypes). At first, these
specimens look slightly different from the
typical A. olfersioides, presenting a larger size
and uniform dorsum. However, difference in
size detected visually is not significant when the
mean SVL is compared (t df 5 16 5 1.62, P 5
0.12). In addition, although very rare (less than
1%), the uniform dorsum is present in other
samples of A. olfersioides from the state of Rio de
Janeiro. Izecksohn and Carvalho-e-Silva (2001)
have already suggested the possibility that these
two taxa are actually synonyms. When compared with individuals from other OTUs, these
individuals are very similar to those from the
state of Bahia (OTU 2) presenting the same
general characteristics in size and color pattern.
Unfortunately, vocalization, the only other
argument used to justify this species could not
572
V. K. VERDADE AND M. T. RODRIGUES
TABLE 1. Frequencies of dorsal and ventral color patterns taken from adults of Atlantic Forest Allobates
included in the four operational taxonomic units (OTU; see text for definitions of OTUs).
Central dorsal pattern
Uniform
Single X
Multiple Xs
Long arm X
Dorsolateral pale stripe
Absent
From eye to arm
From eye to inguinal region
Venter pigmentation
Absent
Restricted to throat
From throat to chest
From throat to inguinal region
OTU 1
(N 5 57)
OTU 2
(N 5 68)
OTU 3
(N 5 11)
OTU 4
(N 5 260)
1 (2%)
42 (74%)
14 (24%)
0
9 (13%)
2 (3%)
57 (84%)
0
0
0
5 (45%)
6 (55%)
1 (, 1%)
0
240 (92%)
19 (7%)
55 (97%)
2 (3%)
0
39 (57%)
24 (36%)
5 (7%)
0
1 (9%)
10 (91%)
15 (26%)
35 (62%)
7 (12%)
0
29
16
19
4
(42%)
(24%)
(28%)
(6%)
1
2
4
4
(9%)
(19%)
(36%)
(36%)
219 (84%)
15 (6%)
26 (10%)
50
34
84
92
(19%)
(14%)
(32%)
(35%)
be tested here because there are no available
calling records and the attempt to get new
records did not succeed.
According to the data presented above, there
is no external morphological evidence to keep
the four species of Allobates known from the
Atlantic Forest as separate units. It is possible
that new ecological, behavioral, cytogenetic, or
molecular evidence could contribute to our
understanding of the systematics of this group.
Until such time as additional evidence is available, we suggest a more conservative posture
and treat A. alagoanus, A. capixaba, and A. carioca
as synonyms of Allobates olfersioides.
Allobates olfersioides (Lutz, 1925)
Figure 3
Eupemphix olfersioides Lutz, 1925: 138.
Holotype.—MNRJ 783 (currently exists only as
a piece of flesh), collected on the coast of the
state of Rio de Janeiro, Brazil; Angra dos Reis,
state of Rio de Janeiro, according to Bokermann
(1966).
FIG. 5. Allobates olfersioides, live specimen from
Maceió, state of Alagoas (Photograph: G. Skuk).
FIG. 6. Lateral view of adult Allobates olfersioides
showing variation on dark lateral stripe.
TAXONOMIC REVIEW OF ALLOBATES FROM THE ATLANTIC FOREST
573
TABLE 2. Descriptives for the main measurements taken from adults of Atlantic Forest Allobates included in the
four operational taxonomic units (OTU; see text for definitions of OTUs). Data are presented as mean 6 SD (N) range.
Snout–vent length (SVL)
Thigh length (THL)
Tibia length (TIL)
Hand length (HAL)
Thumb length (TBL)
Head length (HL)
Foot length (FOL)
Second finger length (FL2)
Head width (HW)
Fourth finger length (FL4)
OTU 1
OTU 2
OTU 3
OTU 4
14.5 6 1.4 (43)
11.5–17.2
6.5 6 0.6 (43)
5.0–7.7
6.8 6 0.5 (42)
5.5–7.5
2.9 6 0.4 (43)
2.2–3.8
1.5 6 0.2 (43)
1.1–1.8
3.7 6 0.3 (43)
3.1–4.4
5.8 6 0.7 (43)
2.9–6.8
1.1 6 0.1 (43)
0.8–1.3
4.7 6 0.3 (44)
3.7–5.4
0.6 6 0.1 (43)
0.4–1.0
16.5 6 1.7 (66)
11.5–18.8
7.8 6 0.7 (65)
5.5–8.8
7.8 6 0.7 (65)
5.2–8.8
3.4 6 0.4 (66)
2.0–4.7
1.8 6 0.3 (66)
1.1–2.4
3.7 6 0.3 (66)
2.8–4.7
6.9 6 0.7 (66)
4.2–8.1
1.4 6 0.2 (66)
0.7–1.9
5.3 6 0.5 (66)
3.8–6.2
0.9 6 0.1 (66)
0.6–1.2
15.1 6 1.5 (10)
13.3–17.2
6.7 6 0.6 (10)
5.7–7.5
7.0 6 0.3 (10)
6.5–7.6
3.0 6 0.2 (10)
2.8–3.3
1.5 6 0.2 (10)
1.2–1.8
3.5 6 0.3 (10)
3.1–4.1
6.1 6 0.3 (10)
6.8–7.2
1.2 6 0.2 (10)
0.9–1.4
4.8 6 0.3 (10)
4.3–5.2
0.8 6 0.1 (10)
0.7–0.9
15.5 6 1.4 (252)
11.5–18.6
7.1 6 0.6 (249)
3.8–8.5
7.2 6 0.6 (249)
4.8–9.0
3.3 6 0.4 (252)
2.0–4.1
1.6 6 0.2 (252)
0.9–2.2
3.7 6 0.3 (252)
2.9–4.9
6.6 6 0.6 (252)
4.2–7.6
1.4 6 0.2 (251)
0.8–1.8
4.9 6 0.4 (252)
3.9–5.7
0.9 6 0.1 (252)
0.4–1.2
Phyllobates capixaba Bokermann, 1967: 349.
Holotype.—WCAB 19252 (MZUSP 73752), collected at Refúgio Sooretama, Linhares, state of
Espı́rito Santo, Brazil.
Phyllobates alagoanus Bokermann, 1967: 351.
Holotype.—WCAB 2801 (MZUSP 73707), collected at Mangabeiras, state of Alagoas, Brazil.
Phyllobates carioca Bokermann, 1967: 352.
Holotype.—WCAB 38610 (MZUSP 76653), collected at Represa Rio Grande, Jacarepaguá, Rio
de Janeiro, state of Rio de Janeiro, Brazil.
Allobates olfersioides Grant, Frost, Caldwell,
Gagliardo, Haddad, Kok, Means, Noonan,
Schargel, and Wheeler, 2006.
FIG. 7. Values of the snout–vent length (SVL) measured in each sample of Atlantic Forest Allobates studied.
Dots represent maximum SVL values, the squares are mean, and the bars, the standard error for each sample.
Localities are presented with shortened names (see Appendix 2) from north (left) to south (right). The names
above the graphic are the states to which the localities belong.
574
V. K. VERDADE AND M. T. RODRIGUES
FIG. 8. Graphic representation of the results of the
Discriminant analyses based on the Atlantic Forest
Allobates body ratios divided in four operational
taxonomic units (OTU). The OTUs are congruent to
the political limits of the states of Alagoas/Sergipe,
Bahia, Espı́rito Santo, and Rio de Janeiro, Brazil (for
detailed distribution see Fig. 1).
Diagnosis.—A small species of dendrobatid
(maximum SVL 5 19 mm in males and
females); thumb slightly longer than second
finger (FL2 on average 85% of TBL); third finger
not swollen in adult males (TFD 0.3 mm in
average); throat, chest, and belly light cream,
almost unpigmented; toes III–IV basally
webbed; dorsum brown, generally adorned
with a pattern of intercrossing Xs; pale dorso-
FIG. 9. Ratios of thumb length by length of finger 2
(upper graphic) and length of finger 4 by hand length
(lower graphic) of Atlantic Forest Allobates studied for
each locality. Squares are mean and bars are the
standard errors for each sample. The localities are
presented with shortened names (see Appendix 2)
from north (left) to south (right). The names above the
graphic are the states to which the localities belong.
lateral stripe absent or present; dark lateral
stripe continuous extending from tip of snout to
groin; ventrolateral stripe present, poorly defined; skin of dorsum smooth or slightly
granular in sacral region; skin of venter smooth;
paracloacal ‘‘C’’ like light stains present; cloacal
tubercles absent; median lingual process absent.
Testis unpigmented in adult males.
Comparison with Other Species.—Given their
overall similarity, in the following section we
compare Allobates olfersioides with all species of
Allobates, Anomaloglossus, and Hyloxalus recorded from Brazil, and those likely to be found
in Brazilian territory. Allobates brunneus differs
by presenting a wider and diffuse dark lateral
stripe, vocal sacs visible in males, and a dorsum
with dark blotches; A. caerulodactylus differs by
possessing blue coloration on digits and toe
discs, and basal web between toes II, III and IV;
A. conspicuus, A. crombiei, and A. gasconi present
reduced fringes on toes. The abdomen is
granulated in A. conspicuus; A. crombiei have
second and fourth fingers of same size (FL2 .
FL4 in A. olfersioides) and dark blotches on
dorsum; the males of A. gasconi and A. fuscellus
present a swollen third finger and sexual
dimorphism in color with venter darker in
males than females; A. goianus differs by the
absence of a conspicuous dark lateral stripe,
toes fringed and webbed and dorsal color
pattern formed by four reddish-brown blotches;
A. granti differs by presenting dorsal color
pattern uniform with brown flecks, anal flap,
hind limbs with granular skin, reduced webbing between toes II, III, and IV (between III and
IV in A. olfersioides), narrow and longer head
(HL 88% of HW, HL 30% of SVL; 80% and 24%
in A. olfersioides), larger hands (HAL 30% of
SVL; 21% in A. olfersioides), and longer legs (TIL
47% of SVL; 44% in A. olfersioides); A. marchesianus differs from A. olfersioides by having
a uniform dorsum scattered with darker spots,
by the dark lateral stripe which is wider at the
inguinal region and can be seen dorsally, by the
thumb distinctively longer than the second
finger (FL2 about 70% of TBL; 85% in A.
olfersioides), and by the gray throat in males; A.
masniger has a more robust body, the dorsum is
uniformly brown with some dark spots in two
parallel lines, and the males have a dark throat;
A. nidicola differs from A. olfersioides by its larger
maximum size (to 21.4 mm), presence of basal
web between toes II, III, and IV, presence of
a dark lateral stripe short and diffuse and throat
and chest black to light gray in males; A.
sumtuosus differs by presenting reduced fringes
on toes II, III, and IV, and swollen third finger in
males; A. trilineatus differs from A. olfersioides
mainly by males presenting finger III and often
finger II strongly swollen, venter stippled with
TAXONOMIC REVIEW OF ALLOBATES FROM THE ATLANTIC FOREST
gray and by the dark lateral stripe along flank
that becomes diffuse at the midbody to the
inguinal region; A. vanzolinius differs from A.
olfersioides by its larger maximum size (to
22.9 mm) and by males presenting a darker
throat than females; Anomaloglossus beebei by
presenting dorsum uniformly brown with scattered dark dots, by the presence of median
lingual process, swollen third finger, reduced
web between toes II, III, and IV, and by the
presence of a well defined tarsal fold; A.
degranvillei has a pigmented and marbled
venter, a more dorsally located lateral dark
stripe with borders less defined, a dark cloacal
region, the median lingual process is present,
the toes are fringed and a dermal fold is present
at the outer margin of the feet; A. stepheni differs
by presenting a wider and robust body shape,
median lingual process, a swollen digit III in
males, toes II and III webbed and a conspicuous
light dorsolateral stripe from eyelid to the
inguinal region; A. tamacuarensis differs by
reaching a larger size (to 25 mm), by presenting
median lingual process, dorsal blotched pattern,
inner tarsal fold and fringes along side of
fingers; Hyloxalus peruvianus differs by reaching
a larger size (to 21 mm), by presenting finger II
and toe IV fringed, by the presence of an outer
tarsal fold, and toes II, III, and IV webbed.
Description.—Based on MNRJ 5094 from the
type locality Angra dos Reis, state of Rio de
Janeiro. Head slightly wider than long (HL 80%
of the HW); head length 24% of the SVL; snout
rounded in dorsal and lateral views, with nares
slightly prominent located and opening laterally; upper jaw slightly projected; canthus rostralis rounded; loreal region slightly concave,
almost flat; internarial distance 39% of the HW;
eye-nostril distance 62% of the eye diameter
(ED); tympanum 42% of the ED with the
anteroventral margin distinct and the posterodorsal obscured by the depressor musculature;
tongue attached anteriorly; median lingual process absent; vocal slits present; dorsal surface
smooth with low, inconspicuous granules restricted to sacral region; dorsal surfaces of thigh
and shanks smooth; although discolored there is
indication of a pattern of intercrossing exes on
dorsum; a dark lateral stripe extends from the
tip of snout, involving the nares and partially
the eyes, to the groin; ventral surface smooth;
belly light cream; no anal flap above vent; no
enlarged tubercles near anus; forelimb slender,
skin smooth; dark bands present mainly at the
outer margin of arms; no ulnar fold, hand
length 21% of SVL; appressed thumb slightly
longer than finger II (FL2 87% of TBL); finger II
longer than IV (FL4 77% of FL2); relative finger
size when appressed III . II 5 I . IV; outer
metacarpal tubercle nearly round, diameter 16%
575
of HAL; inner metacarpal tubercle elliptical,
slightly smaller than the former; supernumerary
tubercle absent; one subarticular tubercle on
fingers I, II and IV and two on finger III; no
fringes on fingers; finger III not swollen;
webbing between fingers absent; tips of digits
expanded (width of finger about 75% of the
width of the disc); discs with distinct dorsal
scutes; thighs and tibia brown with two dark
stripes that form a continuum when hind limbs
are in natural position; tibia length 44% of SVL;
relative length of appressed toes IV . III . V .
II . I; discs on toes larger than the width of toes
(as for fingers); rudimentary webbing present
only between toes III and IV; inner metatarsal
tubercle elliptical, outer metatarsal tubercle
rounded; one subarticular tubercle on toes I
and II, two on toes III and V, and three on toe
IV; toes not fringed; metatarsal fold absent;
tarsus smooth with an inconspicuous tubercle;
tarsal fold absent.
Measurements of the Specimen Described (mm).—
SVL 16.9; HL 4.1; HW 5.1; ED 2.4; END 1.5; IOD
2.2; HAL 3.5; TBL 1.5; FL2 1.3; FL4 1.0; THL 7.8;
TIL 7.5; FOL 7.4.
Color Variation in Preservative (N 5 880).—In
most specimens, the dorsum shows a pattern of
dark brown intercrossing Xs, with branches that
can vary in length and width in a lighter
background (Fig. 4). It is uniformly light brown
in some individuals where intercrossing Xs are
absent. A dark lateral stripe extending from the
tip of the snout, through the eyes to the inguinal
region is always present. This stripe is narrower
at the nares level, becoming gradually wider
through the lateral of the body narrowing again
at the inguinal region. The tympanum is
covered by the dark stripe dorsally (about
a third). The lateral stripe can be uniformly
dark throughout the length or present scattered
white spots at the inguinal region, being diffuse
toward the venter and inguinal region (Fig. 6).
At the end of the stripe, there is an oblique
narrow light stripe that divides it from the short
dark stripes present at the dorsum. The belly is
light cream, and some tiny spots of dark brown
pigmentation of some individuals can be seen in
the throat and chest or through the entire belly.
The arms and legs present the same background
color of the dorsum. The arms present some
dark bands mainly at its outer margin, and the
dorsum of the thigh and tibia generally show
two or three dark brown stripes that vary in
width and form a continuum when the leg is
flexed. The palms of hands and sole of feet are
pigmented as the general background color. At
the end of the fingers and toes, there are light
transversal stripes. There are C-like light cream
stains at each side of the cloacal aperture. The
576
V. K. VERDADE AND M. T. RODRIGUES
color pattern does not seem to vary ontogenetically.
Color in Life.—Based on MZUSP 132193–95
from Una, state of Bahia, and photographs of an
individual from Porto Seguro, state of Bahia, an
individual from Maceió, state of Alagoas
(Fig. 5), and an individual from Rio de Janeiro,
State of Rio de Janeiro (Izecksohn and Carvalhoe-Silva, 2001:fig. 78). The iris is bronze. The
general color pattern follows that described for
preserved specimens. The light cream parts look
more bright and white in live specimens, and the
contrast between the background color and the
darker pattern is more evident.
Sexual Dimorphism.—The data obtained from
Tijuca, state of Rio de Janeiro suggested no
marked sexual dimorphism. Females are slightly larger (SVL) than males (t df 5 39 5 22.15, P 5
0.04; female 5 16.4 6 0.7 mm [N 5 20]; male 5
16.0 6 0.6 mm [N 5 20]) and present an
immaculate belly more frequently. Fifty percent
of the females examined had an immaculate
belly, 35% a belly pigmented from throat to
chest, and 15% a belly pigmented from throat to
inguinal region. No males had an immaculate
belly, 15% had a belly pigmented from throat to
chest, and 85% a belly pigmented from the
throat to the inguinal region. Males and females
did not differ in any other variable. These
results agree with the general pattern of color
dimorphism observed for the genus (Savage,
1968; Edwards, 1974; Coloma, 1995; Kok et al.,
2006).
Advertisement Call.—The vocalization of Allobates olfersioides was described as an acute trill
(Lutz, 1954; Izecksohn and Carvalho-e-Silva,
2001), but unfortunately we were unable to find
any recordings of their calls at the collections
consulted (WCAB, ZUEC, and UFRJ) or with
colleagues herpetologists.
Larval Definition (Fig. 10).—Based on 22 tadpoles (stages 25 to 41) and six metamorphs
(stages 42 to 46) from Tijuca, state of Rio de
Janeiro (MNRJ 23729), reared in captivity by B.
Lutz. Larval definition follows Altig and
McDiarmid (1999), and the stages are identified
following Gosner (1960). All the qualitative
characters studied do not vary among the
tadpoles. The characteristics presented belong
to a single stage-36 individual. The measurements taken were total length (TL); body length
(BL); greatest body width (GBW), measured
behind the eyes in dorsal view; greatest body
height (GBH), measured at the plane of the
center of the coiled intestine; tail length (TAL);
tail musculature height (TMH); tail muscle
width (TMW); maximum tail height (MTH);
dorsal (DFH) and ventral (VFH) fin height,
measured at 6mm from the body terminus; and
ventral internarial distance (IND); interorbital
distance (IOD); eye diameter (ED); distance
between nostril and spiracle aperture (DNS);
and length of the upper (LUJ) and lower (LLJ)
jaw sheaths.
Body depressed (GBH 78% of GBW), elliptical
in dorsal view, oval in lateral view; snout
broadly rounded in dorsal and ventral views,
oval in lateral view; eyes located dorsally,
oriented dorsolaterally; nares dorsolateral with
rounded apertures, located twice as close to the
tip of snout than to the eyes; spiracle single,
lateral, sinistral, aperture lateral; vent tube
medial with lateral displacement, aperture
dextral; tail long (TAL twice as long as BL); tail
fins low (DFH plus VFH 47% of MTH); ventral
fin near parallel to tail musculature, dorsal fin at
an angle of 30u to tail musculature; tail tip
narrowly rounded, forming an internal angle of
approximately 60u; origin of dorsal fin 0.5 mm
anterior to the body terminus; origin of ventral
fin 0.6 mm posterior to the junction of the body
wall and the ventral margin of the tail muscle;
oral disc transversally elliptical, positioned
anteroventrally, forming an angle of about 45u
with the midsagittal plan; lateral emargination
present; anterior labium with five papillae in
each side, separated by a large dorsal gap;
posterior labium with 24 papillae with no gap;
papillae in a uniserial row, with pointed tip; two
straight labial ridges at the anterior labium, the
first with a central gap; three straight labial
ridges at the posterior labium, without gaps;
each labial ridge with a single row of labial
teeth; dental formula 2(1)/3.
The preserved larvae are faded, but some
brown reticulations over the body that become
rounded blotches toward the end of the tail are
still visible. Izecksohn and Carvalho-e-Silva
(2001) described the life color pattern of larvae
as body blackish with a white spot at the end of
the snout.
Metamorphosis appears to take place with
individuals measuring a SVL 7.4 6 0.09 mm on
average (N 5 6), almost half the mean size of
adults. The hands of metamorphs present
supranumerary tubercles, one at the base of
finger II, one at the base of finger III, and one at
the base of finger IV. Dorsal color pattern of
hands, thighs, and shanks are already visible
but not as contrasting as verified in adults.
Although faded it is possible to see a more
intense pigmentation laterally on the body from
the tip of snout to the inguinal region. The
tympanum is not visible.
Measurements of the Larvae Described (mm).—
TL 23.3; BL 7.8; GBW 4.5; GBH 3.5; TAL 16.2;
TMH 2.1; TMW 2.4; MTH 3.2; DFH 0.8; VFH 0.7;
IND 1.7; IOD 2.1; ED 0.8; DNS 4.3; LUJ 0.8; LLJ
0.4.
TAXONOMIC REVIEW OF ALLOBATES FROM THE ATLANTIC FOREST
577
FIG. 10. Tadpole of Allobates olfersioides (MNRJ 23729, Tijuca, Rio de Janeiro, state of Rio de Janeiro): (A)
lateral and (B) dorsal views, and (C) detail of oral disc, ventral view.
Natural History.—Allobates olfersioides is diurnal and lives on the forest floor. When
disturbed, it immediately jumps and dives into
the forest litter (Izecksohn and Carvalho-e-Silva,
2001). The tadpoles hatch in humid terrestrial
nests and are carried by their parents to puddles
of small rivulets on the forest floor where they
feed until metamorphosis (Lutz, 1954; Bokermann, 1967; Izecksohn and Carvalho-e-Silva,
2001). Two nursing frogs captured at Una
(MZUSP 132191, 132202) and two from Ilhéus
(MZUSP 93872–73), Bahia were examined and
found to be male. They carried tadpoles at
Gosner stage 25 agreeing with reports for other
dendrobatids (Coloma, 1995; Juncá, 1998; Caldwell et al., 2002b). Unfortunately, we have
information on the number of tadpoles carried
for only one of the specimens from Una (12).
The frogs from Ilhéus were in a bottle with 22
tadpoles. Previous reports on Allobates found
eight to 48 tadpoles being carried by the parent
(Caldwell et al., 2002b). We found 14 of the 20
females dissected from Tijuca, municipality of
Rio de Janeiro, state of Rio de Janeiro with
mature eggs in the ovaries. The females had
a maximum of 11 mature eggs (about 1.5 mm
each) and mean of 8 6 1.4. Based on these data,
we suggest that the tadpoles from Ilhéus
belonged to two individuals. The presence of
mature eggs and developing follicles together
indicate that females reproduce more than once
in the reproductive period, as observed for
other species of Aromobatidae (Juncá, 1998).
Gravid females were observed in samples from
Ilhéus (MZUSP 93874–913) in August; from
Tijuca (MZUSP 93914–94021) in February, August, and September; and from Represa Rio
Grande, State of Rio de Janeiro (MZUSP 93664–
665) in April, suggesting reproduction throughout the year.
Distribution.—Allobates olfersioides occurs in
coastal forests of the Atlantic Domain from sea
level to about 1000 m a.s.l. The species can be
found from the north of the state of Alagoas to
the south of the state of Rio de Janeiro (between
08u549S and 23u009S latitudinal degrees), with
a probable occurrence in Parque Estadual do
Rio Doce, State of Minas Gerais.
DISCUSSION
The lack of information on the natural history
and molecular phylogeography of Allobates from
the Atlantic Forest populations are important
578
V. K. VERDADE AND M. T. RODRIGUES
barriers to obtaining a better picture of its
differentiation. Data on vocalization are anecdotal, and reported declines in the states of Espı́rito
Santo and Rio de Janeiro (Weygoldt, 1989;
Izecksohn and Carvalho-e-Silva, 2001) render it
difficult to obtain vocalizations and tissue samples, delaying further discussions on possible
geographical call and molecular variation.
As far as we know, the distribution of
Allobates olfersioides seems to be unrelated to
any hydrographic basin, and no river in the
coastal region of Brazil appears to be a geographic barrier. The presence of continuous
character gradients suggests uninterrupted
gene flow between adjacent populations, at
least until recently. Other amphibian populations widely distributed in the coastal area of
Brazil seem to present similar patterns of
geographic variation. Pombal and Haddad
(1992); studying populations of Phyllomedusa
burmeisteri baihana and P. b. burmeisteri from the
states of Rio de Janeiro, Espı́rito Santo, and
Bahia; found a continuum in the color pattern of
the posterior surface of the thigh of the
individuals, with more complex character frequency changes at the state of Espı́rito Santo
(Silva-Filho and Juncá [2006] recently attributed
species status to these subspecies, but without
considering variation in the state of Espı́rito
Santo). A similar pattern was observed by
Jackson (1978) while studying the pattern of
character variation of lizards of the genus
Enyalius (Leiosauridae). Again, the populations
from the state of Espı́rito Santo were those
presenting the largest amount of variation
(Jackson, 1978) compared to that along a northsouth transect.
These congruent geographical patterns may
be a hint of historical events that occurred from
the southern state of Bahia to the northern state
of Rio de Janeiro. It may be caused by the
continuity of forest habitats along the coast
before deforestation or by a residual effect of
a complex introgression caused by the flooding
of the habitats along the coast prior to the last
marine transgression (Suguio and Nogueira,
1999). Molecular phylogeographic studies
might provide much needed evidence for the
discussion of these hypotheses.
Acknowledgments.—We are indebted to the
following colleagues for the loan of specimens:
E. Freire, E. M. Gonçalves, F. Juncá, F. M. Souza,
H. Zaher, J. Jim, J. Pombal, M. Soares, O. L.
Peixoto, S. P. Carvalho-e-Silva, U. Caramaschi,
and W. R. Heyer. We thank Hussam Zaher and
C. Castro-Mello for allowing the access and
logistics at the MZUSP; P. E. Vanzolini for
providing important data from specimens from
W. C. A. Bokermann collection; V. R. Morales for
providing literature, S. P. Carvalho-e-Silva and E.
Izecksohn, for sharing their knowledge on
Allobates populations at the state of Rio de
Janeiro, G. Skuk for the picture of the live
specimen. We also thank the Brazilian environmental organization IBAMA, for collection permits. P. Narvaes, D. Pavan, and T. Grant read and
criticized the manuscript. This paper is a result
from the project ‘‘Revisão sistemática das espécies de Colostethus da Mata Atlântica’’ supported
by FAPESP-Fundação de Amparo à Pesquisa do
Estado de São Paulo process (97/13503–6) as
fulfillment to the requirement of the master’s
degree in zoology by the Instituto de Biociências,
Universidade de São Paulo, São Paulo, Brazil.
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Accepted: 9 May 2007.
APPENDIX 1
Specimens Examined
Allobates brunneus: Brazil, Mato Grosso, Chapada
dos Guimarães: MZUSP 121875–82. Allobates goianus:
Brazil, Goiás, Chapada dos Veadeiros: MZUSP 76652
(holotype), 73706, 76651 (paratypes). Allobates marchesianus: Brazil, Amazonas, Reservas INPA–WWF:
MZUSP 67823–25. Allobates masniger: Brazil, Pará,
Parque Nacional da Amazônia: MZUSP 69166–67
(paratypes); SW of Itaituba, Rio Tapajós: MZUSP
69168–71 (paratypes). Allobates olfersioides: BRAZIL,
Alagoas, Maceió: MUFAL 98735–36, 98739–40; Mangabeiras: MZUSP 73823–30 (A. alagoanus, paratypes),
73707 (A. alagoanus holotype), 78191–78197; Manimbu:
MZUSP 11994, 11997–33; Murici: MZUSP 76432; Novo
Dino: MNRJ 9910; Rio Largo: MUFAL 930809–810;
Bahia, Cumuruxatiba: MZUSP 59433; Elı́sio Medrado:
UEFS 81; Ilhéus: MNRJ 23767–70, 23728, MZUSP
81133, 93874–913, 93872–73; Porto Seguro: MZUSP
63195–97, 126361–65, UFPB 866150, 866153–54, 866193,
866196–97, 866212–13; São José: MZUSP 63495; Una:
MZUSP 63719–21, 125848, 132188–206; Uruçuca:
MZUSP 26916–18, 132187; Espı́rito Santo, Baixo
Guandu: MZUSP 35674; Linhares: MZUSP 93871;
Refúgio Sooretama: MZUSP 76628–76629 (A. capixaba,
paratype), 73752 (A. capixaba, holotype); Santa Teresa:
MZUSP 53559–60; USNM 208141, 208147, 200452–53;
Rio de Janeiro, Angra dos Reis: MNRJ 5094; Araruama:
MNRJ 4115, 15398–406, 4143, 15431–39; Imbiara: MNRJ
23716–19; Itaguaı́: EI 4321–56, JJ 7787, 7792–96, ZUEC
2741–42, MNRJ 23724–27; Represa Rio Grande: MZUSP
73714 (A. carioca, paratype), 73753 (A. carioca, paratype),
76653 (A. carioca, holotype), 93651–65, 93671; Sacra
Famı́lia do Tinguá: EI 8598–600, JJ 7788–91, ZUEC
10824; Serra da Piedade: MNRJ 23730–34; MZUSP
9801–9803; Teresópolis: MNRJ 23721–23, MZUSP
580
V. K. VERDADE AND M. T. RODRIGUES
53448–51, USNM 208396–208401; Tijuca: JJ 224–231,
MZUSP 76418, 76728–29, 93624–49, 93666–767, 93914–
94377; Tinguá: EI 4290, 4306; Sergipe, Areia Branca:
MZUSP 88954. Allobates sumtuosus: Brazil, Pará, Reserva Biológica Rio Trombetas: MZUSP 69157–60
(paratypes). Anomaloglossus beebei: French Guian, Saut
Mais: MZUSP 58230. Anomaloglossus degranvillei:
French Guian, Saül: MZUSP 58231. Anomaloglossus
stepheni: Brazil, Amazonas, Manaus: MZUSP 64569
(holotype), 64570 (paratype).
APPENDIX 2
Gazetteer (State, code number used at Fig. 1, specific
locality, approximate coordinate).—Alagoas, 4, Maceió:
09u409S, 35u419W; 6, Mangabeiras: 09u569S, 36u059W; 5,
Manimbu: 09u529S, 36u099W; 2, Murici: 09u189S,
35u569W; 1, Novo Dino: 08u549S, 35u389W; 3, Rio
Largo: 09u299S, 35u509W; Bahia, 15, Cumuruxatiba:
17u069S, 39u119W; 8, Elı́sio Medrado: 12u569S, 39u319W;
10, Ilhéus:14u489S, 39u039W; 14, Porto Seguro: 16u269S,
39u059W; 11, São José: 15u099S, 39u189W; 12, Jussari,
Serra do Teimoso: 15u099S, 39u319W; 13, Una: 15u179S,
39u059W; 9, Uruçuca: 14u339S; 39u189W; Espı́rito Santo,
18, Baixo Guandu: 19u319S, 41u029W; 17, Linhares:
19u239S, 40u049W; 16, Refúgio Sooretama: 19u009S,
40u009W; 19, Santa Teresa: 19u569S, 40u379W; Rio de
Janeiro, 29, Angra dos Reis: 23u009S, 44u199W; 20,
Araruama: 22u529S, 42u209W; 22, Imbiara: 22u429S,
42u379W; 26, Itaguaı́: 22u489S, 43u419W; Rio de Janeiro,
24, Represa Rio Grande: 22u559S, 43u259W; 28, Sacra
Famı́lia do Tinguá: 22u309S, 43u379W; Rio de Janeiro,
27, Serra da Piedade: 23u009S, 43u399W; 21, Teresópolis: 22u269S, 42u299W; Rio de Janeiro, 25, Tijuca:
22u489S, 43u329W; 23, Tinguá: 22u339S, 43u269W;
Sergipe, 7, Areia Branca: 10u469S, 37u199W.