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Natural History of the Lutz’s Frog Cycloramphus lutzorum Heyer, 1983
(Anura: Cycloramphidae) in the Brazilian Atlantic Forest: Description of
the Advertisement Call, Tadpole, and Karyotype
ANDRE
´M. X. LIMA,
1,2
MICHEL V. GAREY,
3
RAFAEL B. NOLETO,
4
AND VANESSA K. VERDADE
5
1
Programa de Po
´s-graduac¸a
˜o em Ecologia e Conservac¸a
˜o, Universidade Federal do Parana
´, Curitiba, Parana
´, Brazil
3
Departamento de Zoologia e Bota
ˆnica, Universidade Estadual Paulista, Sa
˜o Jose
´do Rio Preto, Sa
˜o Paulo, Brazil
4
Departamento de Gene
´tica, Universidade Federal do Parana
´, Curitiba, Parana
´, Brazil
5
Departamento de Zoologia, Universidade de Sa
˜o Paulo, Sa
˜o Paulo, Brazil
ABSTRACT.—We describe the advertisement call, tadpole, karyotype, and additional information on the
natural history of Cycloramphus lutzorum from southern Brazil. Sonograms were generated from digitally
recorded calls. Tadpoles were collected in the field for description in the lab, and an adult was collected for
karyotyping. Data on seasonal activity were gathered monthly from November 2005 to November 2007. All
tadpoles (N=21), juveniles (N=18), and adults (N=52) were found exclusively in streams. Reproduction, as
identified by calling frogs, occurred from July through November. Frogs call all day long, but mostly at dusk,
from rock crevices inside the stream edges near the splash zone. The call is short and loud, with 11 pulsed
notes, of 491–641 ms, with a dominant frequency of 0.98–1.39 kHz. We describe the exotrophic and
semiterrestrial tadpoles, always found in constantly humid vertical rock walls in the stream. Tadpoles of C.
lutzorum are recognized by differences in labial tooth row formula, eye diameter, body shape, position of
nares, and development of tail. Like congeneric species, the karyotype of C. lutzorum comprises 26
metacentric and submetacentric chromosomes. Cycloramphus lutzorum is restricted to and adapted for living
in fast flowing streams, many of which are threatened by deforestation, pollution, and habitat loss.
Therefore, we recommend the status of C. lutzorum be changed from its current ‘‘Data Deficient’’ to ‘‘Near
Threatened (NT)’’ in the IUCN species red list.
The genus Cycloramphus is endemic to the
Atlantic Forest and comprises 26 species (Ver-
dade and Rodrigues, 2008; Frost, 2009; Socie-
dade Brasileira de Herpetologia, 2009) that
inhabit leaf litter and fast flowing streams of
mountainous forests in eastern Brazil (Heyer,
1983a,b, 1988; Verdade and Rodrigues, 2003).
Although some information on taxonomy,
biogeography, and speciation are available
(Heyer and Maxon, 1983; Verdade, 2005), most
species are virtually unknown (Bokermann,
1951; Heyer, 1983a; Verdade, 2005; Lingnau et
al., 2008). Two ecomorphological species groups
are recognized in the genus in which one
inhabits forest litter and the other inhabits
streams (Verdade, 2005). The forest litter species
deposit their eggs in humid habitats, with
endotrophic tadpoles that complete their devel-
opment in terrestrial environments (Heyer and
Crombie, 1979; V. K. Verdade, J. Cassimiro, L.
Duarte, and M. T. Rodrigues, unpubl. data). The
stream species deposit their eggs on rocks and
logs at the splash zone, and tadpoles are
exotrophic, completing their development feed-
ing on humid rocks, out of water (Lutz, 1929;
Heyer, 1983a; Giaretta and Cardoso, 1995;
Giaretta and Facure, 2003). Five taxonomic
groups have been recognized for Cycloramphus
(Heyer, 1983a): the bolitoglossus and eleuthero-
dactylus species groups are forest litter species,
whereas the ohausi,granulosus, and fuliginosus
groups are stream species. Cycloramphus lut-
zorum belongs to the fuliginosus group. These
groups were defined based on overall similarity
and, except for ohausi, were considered non-
monophyletic based on morphology (Verdade,
2005).
Cycloramphus lutzorum was found in fast
flowing streams in areas of sharp relief in the
states of Sa
˜o Paulo and Parana
´, Brazil, with a
single dubious record for the state of Rio de
Janeiro (Heyer, 1983a). The species is known
from few places in Parana
´State, and no other
report was made since the species was de-
scribed (Heyer, 1983a; Segalla and Langone,
2004). Neither the advertisement call nor the
tadpole of C. lutzorum are known, and the lack
of natural-history data rendered the classifica-
tion of the species as Data Deficient (DD) in
worldwide (IUCN, 2009) and regional (Segalla
and Langone, 2004) lists of threatened species.
Additionally, populations of some species of
Cycloramphus have crashed, similar to global
2
Corresponding Author. E-mail: andremxlima@
uol.com.br
Journal of Herpetology, Vol. 44, No. 3, pp. 360–371, 2010
Copyright 2010 Society for the Study of Amphibians and Reptiles
declines in many other species (Eterovick et al.,
2005; Verdade et al., 2009). Thus, data on the
natural history of C. lutzorum are even more
urgent to understand both its ecology and its
conservation needs.
Here, we describe data collected near Mor-
retes, in the southern Brazilian state of Parana
´,
where we studied C. lutzorum and gathered
information on reproduction, male vocaliza-
tions, and tadpoles. Additionally, we describe
the karyotype structure for the species.
MATERIALS AND METHODS
Study Area.—After the first record in Septem-
ber 2005, we searched for individuals between
100 and 550 m a.s.l. in the Brejamirim Stream
(25u35926.570S, 48u48954.090W), a tributary of
Sagrado River, municipality of Morretes,
Parana
´, southern Brazil. Specimens were found
only between 200 and 300 m a.s.l. The area is
approximately 150 km south of the species’ type
locality (Iporanga municipality, state of Sa
˜o
Paulo; Fig. 1). The entire region is within
mountainous area of the Atlantic Forest Domain
(Ab’Saber, 1970). The Brejamirim Stream is 3–
10 m wide with 20–25uincline under a closed
canopy, with occasional waterfalls and rapids.
Data Collection.—In a 100-m stretch of the
stream, we systematically searched for frogs
from November 2005 throughout November
2007 every 2–3 days each month. We actively
searched for individuals under rocks and in
crevices (inside the stream edges; total of 550
person h
21
), as well as on the dry ground and in
the vegetation near the stream (outside the
stream edges; total of 400 person h
21
). Searches
were conducted by one or two people from
0800–1200 h and 1400–2300 h. For each speci-
men found, we identified males by their calls or
inguinal glands and females by observing eggs
through the body or lack of inguinal glands
FIG. 1. Map showing the location of the study area and of the type locality for Cycloramphus lutzorum.
BIOLOGY, CALL, TADPOLE, AND KARYOTYPE OF CYCLORAMPHUS LUTZORUM 361
(Heyer, 1983a). At each encounter, we described
the location in which the individual was found,
such as what the site was made of (e.g., sand,
rock, litter) and how exposed it was (frogs were
uncovered, partially hidden or totally hidden in
rock crevices). We avoided multiple counting of
the same individual by marking the location of
each site each day. Voucher specimens were
fixed in 10%formalin and preserved in 70%
alcohol and deposited in the herpetological
collections of Museu de Zoologia da Universi-
dade de Sa
˜o Paulo (MZUSP 135281–135282) and
Museu de Histo
´ria Natural Capa
˜o da Imbuia in
Curitiba (MHNCI 6588).
We check for variation in the daily vocal
activity of the males through the breeding
season (daily calling rate). We recorded vocal
activity at 10 points evenly spaced along the
100-m transect. These points were visited twice
each month from August through November
2007, 1400–2300 h. During each count, we
remained at each point for 5 min and noted
the time of each vocalization heard during that
interval. Then, we walked to the next point and
within 5 min initiated the count at that point.
Advertisement Call.—Advertisement calls
(sensu Wells, 1977) were recorded with a Sony
DSH2 digital recorder and an external micro-
phone Sennheiser MKE 300 positioned 40 cm
from the calling male. We recorded air temper-
ature with a digital thermometer to the nearest
0.1uC for each call. Advertisement calls were
analyzed using Raven Lite 1.0, with a 22 kHz
sampling frequency, FFT and frame length of
256 samples, 75%contrast, and 75%brightness.
Acoustic parameters include call type, call
length (ms), interval between calls (sec), and
number of notes per call, fundamental and
dominant frequencies (kHz), peak sound level
(dB), frequency modulation, and call structure
following Abrunhosa et al. (2005).
Tadpole Description.—Tadpoles were collected
by hand on humid rocks in the stream and
identified as Cycloramphus if they displayed the
following characteristics: semiterrestrial, ab-
dominal flap restricted to the posterior region
(Bokermann, 1965; Heyer, 1983a). The only
species found at the stream in the genus was
C. lutzorum, and the color patterns of tadpoles at
late stages of development and of metamorphs
matched those of adults. Tadpole description
was based on specimen MZUSP 139310, where-
as variation was examined in a series of seven
tadpoles and three metamorphs (MZUSP
139309 series) preserved in 10%formalin. Stages
followed Gosner (1960), and morphological
terminology followed Altig and McDiarmid
(1999) and Altig (2007), except for the interor-
bital diameter, which we measured as the
distance between the eyes (Nascimento and
Skuk, 2006).
Fourteen variables were measured: total
length (TL); body length (BL); greatest body
width (GBW, measured behind the eyes in
dorsal view); greatest body height (GBH,
measured at half BL); tail length (TAL); tail
musculature height (TMH); tail musculature
width (TMW); dorsal and ventral fin height
(DFH and VFH, measured at 6 mm from the
body terminus); internarial distance (IND);
interorbital distance (IOD); eye diameter (ED);
and length of the upper (UJS) and lower (LJS)
jaw sheaths. We also described the labial tooth
row formula (LTRF). Measurements using
digital calipers are in millimeters with 0.01 mm
precision for TL and BL. Other variables were
measured under stereoscopic microscopy with a
metric ocular. Illustrations were drawn using a
camera lucida. Larvae were compared with
those of other Cycloramphus when available in
literature (Heyer 1983a,b; Heyer et al., 1990) and
direct observation (see Appendix 1).
Karyotype.—Cytogenetic analyses were car-
ried out on one adult male. Mitotic metaphases
were obtained from bone marrow and liver,
after pretreatment in vivo with 0.01%colchicine
solution for at least 6 h, at 0.1 mL 10 g
21
animal
weight (Baldissera et al., 1993). Standard stain-
ing was performed with 5%Giemsa solution
diluted in phosphate buffered saline (pH 56.8).
About 35 metaphases were available for analy-
sis, and the chromosomes were measured and
arranged following Levan et al. (1964).
RESULTS
Natural History.—Cycloramphus lutzorum was
the only species in the genus found at the study
site. Other frogs found along the stream
included Vitreorana uranoscopa (Centrolenidae)
and Hylodes heyeri (Hylodidae). A total of 52
adults (39 males, 2 females, and 11 of unknown
sex) and 18 juveniles of C. lutzorum was
observed. Adults and juveniles were always
found along the stream, on rocks (N520) or in
rock crevices (N539). Juveniles were also
found among foliage between rocks (N511) in
the stream. No individuals were found outside
the stream edges. Tadpoles were always found
near to seven call sites in constantly humid
vertical rock walls in the stream (N521).
Breeding Biology.—The earliest record for a
gravid female was 16 July 2007 (1 August 2006).
Males vocalized from late July (23 July 2006 and
18 July 2007) through November (15 November
2006 and 21 November 2007). Tadpoles were
found from October to January and juveniles
from November through March (Table 1). We
362 A. M. X. LIMA ET AL.
found frogs at any time of day or night. Daily
calling rate remained constant throughout the
breeding season (F
7,225
50.72, P.0.05), but
vocalizations were most common at dusk (1800–
1900 h; Fig. 2).
Advertisement Call.—All calls were of a single
type, which sounded like a short and loud bark
of a dog (Fig. 3). The interval between calls is
approximately six seconds but usually is spo-
radic. The call comprises 11 pulsed notes,
lasting 491–641 ms, with a decrease in intensity
modulation, and the first four notes are of
higher frequencies (Fig. 3A, B). The fundamen-
tal frequency ranges between 0.50 and 0.65 kHz,
dominant frequency between 0.98 and 1.39 kHz,
and the peak sound level is 145.4 dB (Table 2).
The minimum and maximum frequencies are
0.50 and 2.00 kHz. The low frequency of the call
is similar to that of the noise made by running
water. However, harmonics are found at very
high frequencies (14–19 kHz; Fig. 3C).
Frogs call from the stream near the splash
zone in rock crevices, (N539), exposed near
the entrance of their refuge (N55), or
completely hidden (N534). We found frogs
calling in 14 places along the 100 m, of which
eight were always occupied by frogs at each
count. Most of the sites (N512) were near to
the areas regularly splashed but not submerged
by the stream water (the ‘‘splash zone’’).
Tadpole Description.—Tadpole bodies are de-
pressed (GBH/GBW 582%), elliptical in dorsal
and lateral views with greatest body width at
half body length. The snout is rounded in dorsal
and lateral views and eyes are dorsolateral, with
a very conspicuous superior meniscus on the
FIG. 2. Temporal variation in vocalization frequency from August through November 2007 in Morretes, state
of Parana
´, southern Brazil.
TABLE 1. Monthly distribution of breeding activities (indicated by an X) of Cycloramphus lutzorum in Morretes,
state of Parana
´, Brazil, between November 2005 and November 2007.
Activity Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar
Female with eggs X X X
Calling males X X X X X
Tadpoles X X X X
Juveniles X X X X X
BIOLOGY, CALL, TADPOLE, AND KARYOTYPE OF CYCLORAMPHUS LUTZORUM 363
iris (seen at Stage 29 in our series), dorsolateral
nares half way between the anterior border of
the eyes and snout tip, with round apertures.
No spiracular tube with a single and inconspic-
uous spiracular aperture. The abdominal flap
extends posteriorly along the body, with a
medial vent, difficult to see under the abdom-
inal flap. Long, rounded, muscular tail (TAL/
TL 50.75), with symmetrical tail myomeres and
tail fin lower than body height (DFH +VFH/
FIG. 3. Oscillogram (A) and audiospectrogram (B) of the advertisement call of Cycloramphus lutzorum
(MHNCI 6588, SVL 543.1 mm, air temperature: 17uC), Morretes, state of Parana
´, Brazil. (C) Audiospectogram of
the advertisement call of C. lutzorum (MHNCI 6588, SVL 543.1 mm, air temperature: 17uC) and of the constant
noise from the stream, analyzed with 0%contrast, 50%brightness, in southern Brazil. Note that the frequency of
the call are within the range of water noise (0–10 kHz), but a harmonic structure appears at high frequencies
rates (15–19 kHz).
364 A. M. X. LIMA ET AL.
MTH 50.4), parallel to tail musculature and
restricted to distal half of tail. The origin of the
dorsal fin is slightly posterior to that of the
ventral. The oral disc is transversally elliptical,
about 65%of GBW, ventral, with lateral emargi-
nation and marginal papillae in a uniserial row.
The anterior labium has six papillae approxi-
mately 0.09 mm in diameter, separated by a wide
dorsal gap. The posterior labium has small and
conical marginal papillae approximately 0.03 mm
in diameter and uniformly distributed with no
gap. LTRF is 2(2)/3. There is a symmetrical
interruption of the teeth line at the second row
but does not constitute a gap (Fig. 4D). Similar
interruption of the teeth line was found in two
other tadpoles of our series, one at Stage 30 and
other at Stage 37, and in the remainder, there is
no interruption. Each labial ridge has a single
row of labial teeth and the jaw sheath has a
strongly keratinized central area, chisel-like,
with serrations on superior and inferior borders.
In life, tadpoles are uniformly brown, with a
very conspicuous light middorsal ocellus, later-
ally the body is mottled with shades of brown;
the venter is unpigmented, and the tail has a
TABLE 2. Main acoustic parameters of the
advertisement call of Cycloramphus lutzorum in
Morretes, state of Parana
´, southern Brazil.
Behavior Mean 6SD
Amplitude
range
Calls
male
21
Call length (ms) 557 632.2 491–641 29/16
Number of notes
per call 11.1 60.3 10–12 29/16
Call interval (sec) 6.21 60.56 4.95–7.31 12/12
Fundamental
frequency (kHz) 0.58 60.05 0.51–0.65 29/16
Dominant frequency
(kHz) 1.14 60.19 0.98–1.39 29/16
Peak sound level
(dB) 145.4 69.1 134.3–155.8 29/16
FIG. 4. Lateral (A), dorsal (B), and ventral (C) views and oral disc (D) of the tadpole of Cycloramphus lutzorum
(MZUSP 139310, Morretes, state of Parana
´) by V. K. Verdade. Gosner Stage 36; Total length (TL) 526.23 mm.
BIOLOGY, CALL, TADPOLE, AND KARYOTYPE OF CYCLORAMPHUS LUTZORUM 365
series of light dorsal ocelli. In preservation, the
general pattern is the same, but the middorsal
ocellus is less evident. Snout–vent length (SVL)
of metamorphs are no longer than 140 mm (SVL
108 626 mm, N53). In preservation, the
dorsum, hands, thighs, and shanks are yellow-
brownish with dark brown spots. The middor-
sal ocellus on tadpoles turns into a light yellow-
brown spot in juveniles and is also present in
adults. The general color pattern observed in
juveniles is very similar to that of adults, except
for more contrasting colors and absence of
white spots on belly (present in adults). Mea-
surements of larvae are summarized in Table 3.
Karyotype.—The karyotype of C. lutzorum is
2n 526 with all chromosomes biarmed and the
fundamental number (FN) 552. Pairs 1 and 5–
13 are metacentric and pairs 2–4 are submeta-
centric. The first five pairs are large; pair 6 is
somewhat smaller, and the remaining seven
pairs are all small (Fig. 5).
DISCUSSION
Cycloramphus lutzorum is clearly associated
with fast flowing streams, as is the case of
species in the Cycloramphus fuliginosus group
(Heyer, 1983a; Heyer and Maxon, 1983), but C.
lutzorum might be restricted to the fast flowing
sections of small and shadowy streams. Cyclo-
ramphus lutzorum was the only species in the
genus found throughout this study and proba-
bly the only species in this stream. Sympatry
has been found among Cycloramphus species but
not syntopy (Heyer et al., 1990). Cycloramphus
boraceiensis and Cycloramphus semipalmatus have
both been found at the Boraceia Biological
Station, but C. boraceiensis is found amid large
wet rock exposures, whereas C. semipalmatus is
found along small streams in the forest and only
in Sa
˜o Paulo State (Heyer et al., 1990).
Breeding Biology.—The breeding biology of C.
lutzorum is associated with the stream habitat.
We classify C. lutzorum as reproductive mode 19
(Haddad and Prado, 2005). The reproductive
season is long (sensu Wells, 1977) and begins
earlier than that of most anuran species of the
region (Abrunhosa and Wogel, 2004; Kokubum
and Giaretta, 2005; Toledo and Haddad, 2005;
Conte and Rossa-Feres, 2007). Cycloramphus
lutzorum begins breeding in the southern cool
and dry winter. Stream species of Cycloramphus
TABLE 3. Body measurements (mm) taken from Cycloramphus lutzorum tadpoles Gosner Stage 29–44. Gosner
Stage 30 (N53) mean and SD are presented. For abbreviations, see Materials and Methods. If blank, the
structure was not comparable to other stages.
Tadpole: MZUSP 139310 MZUSP 139309 (series)
Stage: 36 29 30 37 38 43 44
TL 26.23 22.52 24.67 60.20 29.66 30.26 26.87 25.75
BL 6.59 5.46 5.62 60.03 6.85 6.85 7.62 8.10
GBW 4.06 3.17 3.06 60.04 4.12 4.56
GBH 3.36 2.14 2.08 60.09 2.58 2.86
TAL 19.64 17.06 19.05 60.23 22.82 23.41 19.25 17.66
TMH 2.19 1.75 1.84 60.05 2.03 2.25 2.12 1.59
TMW 1.90 1.68 1.68 60.02 2.25 2.32 1.98 2.25
DFH 0.54 0.10 0.19 60.05 0.44
VFH 0.41 0.06 0.35 60.04 0.60
IND 1.17 0.98 1.08 60.03 1.14 1.11 1.05 1.05
IOD 2.95 2.29 2.29 60.03 3.02 3.08 3.52 3.37
ED 1.17 0.95 0.98 60.02 1.27 1.37 1.21 1.21
UJS 0.32 0.22 0.32 60.02 0.38 0.41
LJS 0.48 0.32 0.35 60.01 0.41 0.38
FIG. 5. Conventional Giemsa-stained karyotype of a male Cycloramphus lutzorum (MHNCI 6588). Scale bar 5
10 mm.
366 A. M. X. LIMA ET AL.
have long breeding seasons, but they may vary
among species. For example, C. boraceiensis and
C. semipalmatus breed from October to March
(Heyer et al., 1990), whereas Cycloramphus
dubius breed throughout the year (Giaretta and
Cardoso, 1995). Perhaps the stream environ-
ment is less variable in temperature and
humidity and, therefore, is more favorable for
reproduction throughout the year (Afonso and
Eterovick, 2007). An important limiting factor
for reproduction may be the heavy rains in the
summer, which inundate the streams. Here,
breeding ended in November, and heavier rains
usually begin in December and last until March.
Calling Activity and Calling Sites.—Cycloram-
phus lutzorum can be active throughout the day
and night, whereas most species of the genus
are usually nocturnal (Heyer, 1983a). Both C.
dubius (Giaretta and Cardoso, 1995) and C.
boraceiensis (Hartmann et al., 2003) were report-
edly active during the day as well. Perhaps
activity patterns are less fixed than previously
thought and the reported patterns are caused by
observer bias.
Frogs seem to choose specific places to call
perhaps because of protection and humidity for
safe reproduction. The call site might be a
locally and regionally limiting factor and
optimal sites seem to be relatively uncommon
in the study area and may be restricted to a
certain slope angle and water flow (Heyer,
1983a). Frogs seem to be territorial in that they
often return to, or remain at, specific locations
and aggressive behaviors (biting and grasping)
have been observed. However, marking indi-
viduals is necessary to examine territoriality. In
a brief census, the greatest number of males
calling simultaneously was 10 (maximum den-
sity of 0.08 60.02 male m
22
). Limited avail-
ability of sites may explain territorial and
aggressive behavior in the species. Additionally,
territories may be used for more than one
reproductive event at a time (Giaretta and
Cardoso, 1995; Giaretta and Facure, 2003). These
patterns, and the low density of males, would
suggest territoriality.
Advertisement Call.—The advertisement call of
C. lutzorum shares some traits with other stream
species of Cycloramphus, such as the pulses and
low frequency (Heyer and Mello, 1979; Heyer,
1983a; Haddad and Sazima, 1989; Giaretta and
Cardoso, 1995). Despite similarities, the adver-
tisement call of C. lutzorum is easily distin-
guished from that of C. boraceiensis,Cycloram-
phus brasiliensis,Cycloramphus izecksohni,
Cycloramphus rhyakonastes, and C. semipalmatus
by the call type (Heyer, 1983a); and from these
and Cycloramphus bolitoglossus,C. dubius,Cyclo-
ramphus eleutherodactylus,Cycloramphus faustoi,
Cycloramphus juimirim,Cycloramphus ohausi, and
Cycloramphus valae by the call length, call
modulation, and dominant frequency (Table 4).
The low frequency calls as C. lutzorum are in the
same range of running water, but the harmonics
at higher frequencies may be important as an
acoustic adaptation for living in noisy environ-
ments, similar to the high frequency trills of
stream species in the genus Hylodes (Vielliard
and Cardoso, 1996; Lingnau and Bastos, 2007)
and other stream frog species (Dubois and
Martens, 1984). Continued study of sound
dynamics in noisy environments is necessary
to understand the evolution of vocal communi-
cation in species of frogs associated with fast-
flowing streams.
Tadpole.—The tadpole of C. lutzorum is semi-
terrestrial (following Altig and Johnston, 1989).
Semiterrestrial tadpoles are known today only
for species in the genera Cycloramphus,Thoropa
(Cycloramphidae), and Petropedetes (Ranidae)
(McDiarmid and Altig, 1999). The semiterrestri-
al tadpoles of C. lutzorum are easily recognized
and separated from terrestrial endotrophic
larvae, in similar stages, of the leaf litter species
of Cycloramphus (Heyer, 1983a; V. K. Verdade,
unpubl. data) by larger total body length; longer
tail; tail fins conspicuous at posterior half of tail
(restricted to a dermal ridge in leaf litter
dwellers Cycloramphus, e.g., Cycloramphus stejne-
geri), no yolk at Stage 36 (large amount
remaining in forest litter species), body de-
pressed in lateral view (elliptical in forest litter
dweller tadpoles), eyes located and oriented
dorsolaterally (oriented laterally in leaf litter
species), posterior abdominal flap (restricted to
medial lobes in leaf litter species), and well-
developed oral disc (reduced in leaf litter
species).
Tadpoles of only five species of stream
Cycloramphus have been described (C. boraceien-
sis,C. brasiliensis,C. fuliginosus,C. izecksohni—
under C. duseni, and C. valae; Heyer, 1983a,b),
and the larvae are morphologically very similar
and difficult to diagnose. Additionally, larvae of
different stages have been described making
comparisons difficult. We found differences in
labial tooth row formula (LTRF), eye diameter,
body shape, position of nares, and development
of ventral tail fin among the tadpoles of C.
lutzorum and those from other species of
Cycloramphus (Table 5).
We found inconsistencies regarding LTRF
reported for some species (C. boraceiensis; see
Table 5). We suggest that these inconsistencies
are caused by the interpretation of a gap
(present or absent) at the second tooth row on
the upper lip. We noted a gap that is very
narrow and visible only under stereomicro-
scope. All reports on the absence of a gap on the
second tooth row of the upper lip Cycloramphus
BIOLOGY, CALL, TADPOLE, AND KARYOTYPE OF CYCLORAMPHUS LUTZORUM 367
TABLE 5. Comparative morphology of the tadpoles of stream Cycloramphus species. Characters were summarized from literature (1 5Heyer, 1983a; 2 5Heyer et al.,
1990; and 3 5Heyer, 1983b) and direct observation of tadpoles in this study (Appendix 1). Question marks indicate character not mentioned in literature; asterisks
indicate detailed discussion in the text. BS 5body shape; DES 5distance between eyes and snout; DO 5direct observation; LTRF 5labial tooth row formula. For other
abbreviations, see Materials and Methods. The dashes (–) indicate the information was not available.
Species Source Stage
TL
(mm)
BL
(%of TL)
Dorsal
BS
Lateral
BS
ED
(%of BL)
Position
of nares Abdominal flap Spiracle Vent tube Ventral tail fin LTRF
lutzorum DO 36 26.2 23 both
elliptical
both
depressed
15 both at half
DES
shallowly bilobed
or not
both small both
median
both at the
distal half
2(2)/3
DO 43 26.9 31 20
boraceiensis 1, 2 42 27.2 23 – – 18 half DES – not visible absent – 2(2)/3,
2/3(1)
DO 37 30.7* 23 elliptical depressed 22 half DES bilobed small not visible distal third 2/3*, 2(2)/
3(1)
brasiliensis 1 41 37.5 25 – depressed 17 half DES bilobed very small not visible distal half 2/3(1)
fuliginosus 1 41 43.5 19 – depressed 12 – – small median distal half 2/3
izecksohni 1, 3 41 32.0 23–28 – – 13–18 – shallowly bilobed
or not
very small median distal half 2/3
DO 34–42 22.0–28.9 26–29 elliptical very
depressed
12–16 closer to eyes distal fourth 2(2)/3(1)
valae 3 36 29.3 24–29 – – 16–19 half DES shallowly bilobed not visible – distal half 2(2)/3(1)
DO 35 26.4 25 oval depressed 16 half DES small median distal third 2(2)/3(1)
TABLE 4. Comparison of some of the parameters of the advertisement call for 13 species of Cycloramphus. Call type (Heyer 1983a): A 5single pulse; B 5several pulses;
C5pulses organized into three notes. If blank, information was not available.
Species Taxonomic group Ecomorph group Call type Call length (sec)
Dominant frequency (Hz)
ReferencesRange Peak
lutzorum fuliginosus Stream B 0.05–0.06 980–1,390 1,140 This study
bolitoglossus bolitoglossus Litter B 3.95–4.48 1,320–2,440 Lingnau et al., 2008
boraceiensis fuliginosus Stream A 0.03–0.06 500–3,500 2,300 Heyer, 1983a; Heyer et al., 1990
brasiliensis fuliginosus Stream C 1.0 1,600–1,800 1,700 Heyer, 1983a
dubius fuliginosus Stream B 0.2 1,200–3,100 Giaretta and Cardoso, 1995
eleutherodactylus eleutherodactylus Litter B 4.04–4.34 800–2,200 Brasileiro et al., 2007
faustoi eleutherodactylus Litter B 2.53–4.17 900–2,200 Brasileiro et al., 2007
izecksohni fuliginosus Stream A 0.02 1,400–3,000 Heyer, 1983a
juimirim fuliginosus Stream B 0.4–0.7 1,200–1,700 Haddad and Sazima, 1989
ohausi ohausi Stream B 1.76 750–1,100 910 Heyer, 1983a
rhyakonastes fuliginosus Stream A 0.04 1,300–2,200 1,850 Heyer, 1983a
semipalmatus fuliginosus Stream A 0.02–0.04 200–5,000 800–1,500 Heyer, 1983a; Heyer et al., 1990
valae granulosus Stream B 1.3–1.9 1,250–2,250 Heyer, 1983b
368 A. M. X. LIMA ET AL.
should be considered with caution. However,
the gap, or lack thereof, at the first tooth row on
lower lip of tadpoles of Cycloramphus is real, and
the variation may be intraspecific. Based on our
observations and the study of illustrations
available in literature (Lutz, 1929; Bokermann,
1951; Heyer, 1983a; Heyer et al., 1990), we
believe that the LTRF of stream dweller species
of Cycloramphus is conservative and typically
2(2)/3 or 2(2)/3(1).
Karyotype.—The diploid chromosome number
(2n 526) in C. lutzorum is in agreement with
that previously found for all other Cycloramphus
species (Silva et al., 2001, and references
therein), and it is shared by other species in
the family Cycloramphidae (for review see
King, 1990; Kuramoto, 1990). An interesting
finding is related to the variation of chromo-
some fundamental number (FN) among species.
Cycloramphus boraceiensis,C. dubius, and C.
eleutherodactylus all have FN 550, whereas
Cycloramphus acangatan,Cycloramphus asper,C.
lutzorum, and C. fuliginosus have FN 552 (Silva
et al., 2001; Amaro-Ghilardi, 2005). It is not yet
clear how the FN is related to the Cycloramphus
taxonomic groups (Heyer, 1983a). Rearrange-
ments, such as pericentric inversions, seem
implicated in the chromosomal evolution of this
group, but translocations are also a possibility
(Amaro-Ghilardi, 2005).
Conservation.—The close association of C.
lutzorum with fast-flowing streams probably
reduces the recovery capability of the species
when anthropogenic habitat modifications occur.
The elevation range of the species (200–300 m
a.s.l.) is in a region of actual and potential intense
human occupation. At the study site and sur-
roundings, the main threats for the species are
habitat degradation from clear cutting of stream
margin vegetation, water contamination, and
removal of rocks to build recreational pools in
the stream (AMXL, pers. obs.). The last might be a
common threat in the steep relief of the Atlantic
Forest, where natural pools in the streams are
enlarged by removing and relocating the rocks.
The major effect of this interference is habitat
degradation resulting from changes in the struc-
ture and number of suitable reproduction sites
and altering water flow. When we removed rocks
from a couple of calling sites, they were promptly
abandoned. Also, we suggest that suitable habitat
includes shade, which is almost always found
where the frogs occur. Also, anthropogenic
activities usually open up the canopy reducing
the shade, thereby changing microclimate.
We suggest that the limited habitat require-
ments, the low population density, the biology
of this species, and the status of decreasing
population (Heyer and Pimenta, 2004) warrant
it being classified as Near Threatened (NT). We
recommend further study, especially of repro-
ductive success, territoriality, dispersal ecology,
and call dynamics in noisy streams to better
understand conservation needs of this species.
Acknowledgments.—We acknowledge the Bra-
zilian National Institute of Natural Resources
(IBAMA), for research permit (license 10075-1).
We thank M. G. de Mello Leita
˜o Filho and C. H.
de Mello Leita
˜o for permission to work in their
area, to F. H. de Mello Leita
˜o for helping in the
fieldwork, to C. Castro-Mello and H. Zaher
from MZUSP and J. C. de Moura Leite from
MHNCI for loaning specimens under their care,
to M. T. Rodrigues for logistics at IBUSP and for
reading a earlier version of the manuscript, to R.
C. Amaro for sharing unpublished data, and to
F. F. Curcio who also read a first version of the
manuscript. We thank J. Stoike for the first
English revision, to the anonymous reviewers
that greatly improved the manuscript, and to J.
J. Roper, who critically reviewed the English
and offered suggestions for the improvement of
this manuscript. All specimens were treated
according to the scientific and ethical guide-
lines, proposed by the Brazilian National
Council of Veterinary and adopted by IBAMA.
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APPENDIX 1
Additional Specimens Examined
Cycloramphus boraceiensis, Brazil, Sa
˜o Paulo, Sa
˜o
Sebastia
˜o: MZUSP 128256 (tadpoles).
Cycloramphus izecksohni, BR 280, 17 km from
Pirabeiraba: MZUSP 57773 (tadpoles).
Cycloramphus lutzorum, Brazil, Sa
˜o Paulo, 11 km
from Iporanga: MZUSP 57805 (holotype), MZUSP
57806–57808 (paratopotypes).
Cycloramphus mirandaribeiroi, Brazil, Parana
´,9km
from Sa
˜o Joa
˜o da Graciosa on PR 410: MZUSP 57809
(holotype), MZUSP 57810–57814 (paratypes).
Cycloramphus rhyakonastes, Brazil, Parana
´,15km
from Sa
˜o Joa
˜o da Graciosa on PR 410: MZUSP 57827
(holotype), MZUSP 57828–57859 (paratypes).
Cycloramphus stejnegeri, Brazil, Rio de Janeiro,
Tereso
´polis: MZUSP 58582 (tadpoles).
Cycloramphus valae, Brazil, Sa
˜o Paulo, 10 km Itaim-
bezinho a Praia Grande: MZUSP 59282 (tadpole).
BIOLOGY, CALL, TADPOLE, AND KARYOTYPE OF CYCLORAMPHUS LUTZORUM 371
