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Notes on vocalizations in three species of Atelopus from Central and South America

Authors:
Stefan Lötters at Trier University
Stefan Lötters
Frank Glaw at Zoologische Staatssammlung München
Frank Glaw
EBERHARD MEYER
EBERHARD MEYER
EBERHARD MEYER
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Abstract

We report on short calls in three species of Atelopus. In two (A. peruensis GRAY & CANNATELLA, 1985, A. tricolor BOULENGER, 1902) vocalizations were previously unknown; in the third (A. chiriquiensis SHREVE, 1936) they resemble short call descriptions from elsewhere within its distribution range. Short calls in these taxa are compa- rable to those known from other species of the genus. Concerning/I. tricolor, we also report on a distinctly longer call. In overall structure it corresponds to the pulsed call type known in Atelopus species, although it is considerably shorter than in other species.
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HERPETOZOA 12 (1/2): 79 - 83 KURZE MITTEILUNG / SHORT NOTE
Wien, 30. Juli 1999
Notes on vocalizations in three species of Atelopus
from Central and South America
(Anura: Bufonidae)
Bernerkungen zu Lautiiufierungen dreier Atelopus-Aiten aus Mittel- und Sudamerika
(Anura: Bufonidae)
STEFAN
LOTTERS & FRANK GLAW & STEFFENREICHLE
& JORNKOHLER & EBERHARD MEYER
KURZFASSUNG
Ober den kurzen Ruftyp bei drei Atelopus-Aiien wird berichtet. Von zwei Arten (A. peruensis GRAY & CAN-
NATELLA, 1985, A. tricolor BOULENGER, 1902) waren bisher keine LautauBerungen bekannt; bei der dritten Art (A.
chiriquiensis SHREVE, 1936) stimmt der Ruf mit Beschreibungen des kurzen Ruftyps von anderer Stelle innerhalb
ihres Verbreitungsgebietes weitgehend Oberein. Die Rufe der behandelten Taxa sind vergleichbar mit dem kurzen Ruf-
typ bei anderen Atelopus-Aiten. Von A. tricolor konnte zudem ein deutlich langerer Ruf aufgenommen werden. Er
gleicht in der Struktur dem gepulsten Ruftyp, der fur diverse Atelopus-Aiten beschrieben wurde, ist jedoch kurzer als
bei anderen Arten.
ABSTRACT
We report on short calls in three species of Atelopus. In two (A. peruensis GRAY & CANNATELLA, 1985, A.
tricolor BOULENGER, 1902) vocalizations were previously unknown; in the third (A. chiriquiensis SHREVE, 1936)
they resemble short call descriptions from elsewhere within its distribution range. Short calls in these taxa are compa-
rable to those known from other species of the genus. Concerning/I. tricolor, we also report on a distinctly longer call.
In overall structure it corresponds to the pulsed call type known in Atelopus species, although it is considerably shorter
than in other species.
KEY WORDS
Amphibia, Anura, Bufonidae, Atelopus chiriquiensis, A. peruensis, A. tricolor, vocalizations, Neotropics
Contrary to anurans in general, in COCROFT& al. (1990) noted three different
Neotropical bufonids of the genus Atelopus call types among eight Atelopus species
acoustic communication has been sug- analyzed: pulsed calls having a duration of
gested to be of minor importance; indi- 227-1240 ms, pure tone calls lasting 180-
viduals communicate primarily by visual 297 ms, and short calls with a duration of
cues (COCROFT & al. 1990; LINDQUIST & 22-100 ms. However, their functional
HETHERINGTON 1996; LOTTERS 1996). Ac- significance in the intraspecific ethological
cording to McDlARMlD (1971), this is sup- context is only poorly understood (Coc-
ported by two circumstances. First, most ROFT & al. 1990). At least, short calls are
species of Atelopus occur along fast moving produced by males when they are crowded
or cascading noisy streams which may con- (e.g., in a collecting bag), physically con-
siderably disturb acoustic communication, tacted, or clasped by other males (JASLOW
Second, as known thus far, members of the 1979; COCROFT & al. 1990; LINDQUIST &
genus except for some Amazonian species HETHERINGTON 1996), and thus may have
(e.g., A. spumarius
COPE,
1871) usually release function.
lack a middle ear. Nevertheless, yet in males Calls with possible release function in
of 13 species or subspecies of Atelopus vo- male Atelopus can be provoked easily by
calizations have been recognized (summary handling or touching their backs. Using
in LOITERS 1996: 79). Moreover, recently this method, we recorded calls in one male
JASLOW & LOMBARD (1996) demonstrated each of A. chiriquiensis (from a trail to
that at least the earless A. chiriquiensis Cerro Chirripo, about 2150 m a.s.l., Pro-
SHREVE, 1936 is capable of detecting aerial vincia San Jose, Costa Rica — recorded by
sound with frequencies higher than 1 kHz. E.M.), A. peruensis GRAY & CANNATELLA,
80
S. LOTTERS & F. GLAW & S. REICHLE & J. KOHLER & E. MEYER
A Frequency (kHz)
r\
1Q
_
100 ms
100 ms
D Frequency (kHz)
D
10
100 ms
100 ms
Vocalizations in three Atelopus species
81
C
Frequency (kHz)
10
100 ms
100 ms
Fig. 1 (opposite page and above):
Spectrograms and oscillograms of short calls of (h) Atelopus chiriquiensis
SHREVE,
1936,
(B) A. peruensis GRAY & CANNATELLA, 1985, and (C) A. tricolor BOULENOER, 1902.
Abb.
1 (gegenuberliegende Seite und oben):
Spektrogramme und Oszillogramme vom kurzen Ruftyp von (A) Atelopus chiriquiensis SHREVE, 1936,
(B) A peruensis GRAY & CANNATELLA, 1985 und (C) A tricolor BOULENGER, 1902.
1985 (in captivity; specimen from the De-
partamento Cajamarca, Peru — recorded
by S.L.), and A. tricolor
BOULENGER,
1902
(from Rio Neces, Departamento La Paz,
Bolivia — recorded by S.R.). In addition,
in another male A. tricolor (from the road
from Paracti to Cochabamba, about 1300 m
a.s.l., Departamento Cochabamba, Bolivia)
a relatively long call of unknown function
was recorded in captivity by S.L. This type
of call was repeatedly emitted by the male
when seeing one of the two females which
were in the same tank. The studied speci-
men of A. tricolor from Rio Neces is de-
posited at Coleccion Boliviana de Fauna,
La Paz (CBF 2502; the other A. tricolor
male was not preserved), that of A. peru-
ensis at Zoologisches Forschungsinstitut
und Museum Alexander Koenig, Bonn
(ZFMK 64569). The male A. chiriquiensis
recorded is in the private collection of E.M.
(129.1993). Various calls in the latter spe-
cies were already described by JASLOW
(1979) who studied a Panamanian popula-
tion, however. No data are available on vo-
calizations in A. peruensis or A. tricolor.
For A. peruensis and A. tricolor we used
recording equipment as mentioned by
LOT-
TERS & WIDMER (1997), and for A. chiri-
quiensis that described by MEYER (1996).
Analyses of call parameters (table 1) were
done by means of a Medav® MOSIP 3000
sound spectrograph with integrated soft-
ware (Spektro 3.2.). Frequency information
was obtained using fast Fourier transfor-
mation (FFT width 512).
Spectrograms and oscillograms are
shown in fig. 1. Data of call parameters are
listed in table 1. The calls in A. chiriqui-
ensis, A. peruensis, and the shorter one in
A.
tricolor can be identified as short calls
sensu COCROFT & al. (1990). According to
S. LOTTERS & F. GLAW & S. REICHLE & J. KOHLER & E. MEYER
Table 1: Parameters of vocalizations recorded in three species of Atelopus. SVL = Snout-vent length. Termi-
nology of call types follows COCROFT & al. (1990). Data on "Call duration" and "Number of pulses per call" include
arithmetic mean ± one standard deviation, and range.
Tabelle 1: Parameter der aufgenommenen LautauBerungen dreier/itefcpw.s-Arten. SVL = Kopf-Rumpf-LSnge.
Terminology der Ruftypen nach COCROFT & al. (1990). Die Angaben zu "Rufdauer" und "Anzahl Pulse je Ruf be-
inhalten das arithmetische Mittel ± eine Standardabweichung sowie die Spannweite.
Species / Art
SVL [mm]
Call type /
Ruftyp
Number of calls analyzed /
Anzahl untersuchter Rufe
Temperature [°C] / Temperatur [°C]
Call duration [ms] /
Rufdauer [ms]
Number of pulses per call /
Anzahl Pulse je Ruf
Frequency range [kHz] /
Frequenzbereich [kHz]
Dominant frequency range [kHz] /
Bereich der Dominanzfrequenz [kHz]
A.
chiriquiensis
28.3
short call /
kurzer Ruf
13
25.5
24.61 ± 12.25
12-52
unpulsed call /
ungepulster Ruf
1.70-2.35
1.90-2.15
(n = 13)
A.
peruensis
37.0
short call /
kurzer Ruf
12
15.0
73.83 ±22.53
44-114
unpulsed call /
ungepulster Ruf
1.50-2.15
1.50-1.75
(n= 11)
1.80-2.10
(n= 1)
A.
tricolor
21.9
short call /
kurzer Ruf
10
17.5
23.50 ±21.23
7-77
unpulsed call /
ungepulster Ruf
2.10-2.90
2.10-2.85 (n=l)
2.15-2.70 (n = 5)
2.45-2.85 (n = 4)
A.
tricolor
(pulsed call) /
(gepulster Ruf)
15
26.2
103.13 ±4.45
92-108
17.80 ±1.08
16-19
2.25-7.0
2.97-3.45 (n= 15)
Frequency (kHz)
300 ms
300 ms
Fig. 2: Spectrogram and oscillogram ofa pulsed call of Atelopus tricolor BOULENGER, 1902.
Abb.
2: Spektrogramni und Oszillogramm eines gepulsten Rufes von Atelopus tricolor BOULENGER, 1902.
Vocalizations
in
three Atelopus species 83
these authors, short calls
in
most Atelopus
ate pulsed, while only
in A.
zeteki DUNN,
1933 they
are not.
Short calls
of
those taxa
studied
in
this paper also lack pulsed
structure
(fig. 1).
Moreover, they
do not
show distinct frequency modulations.
Fre-
quency ranges
are
similar
in A.
chiriqui-
ensis
and A.
peruensis, whereas
the fre-
quency range
of the
smaller
A.
tricolor
is
somewhat wider (table
1). The
call dura-
tions
are
extremely variable
and
overlap
con-
siderably between
the
three species
ana-
lyzed here
or
those studied
by
previous
authors (e.g., COCROFT
& al.
1990). This
includes
the two
populations
of
A. chiriqui-
ensis from Costa Rica (studied here)
and
Panama (studied
by
JASLOW
1979)
where
no significant differences were found.
COCROFT
& al.
(1990) found intra-
individual variation
in the
dominant
fre-
quency
of
short calls among seven Atelopus
species.
We
report this
for A.
peruensis
and
A.
tricolor (table
1).
The longer call recorded
in A. tri-
color does
not
only differ from
the
short
call
in
duration
but
also
in
showing
a dis-
tinct amplitude modulation
and in
being
pulsed (figs.
1C and 2).
Hence,
we are con-
vinced that
our two
recordings
of
this
spe-
cies correspond
to
completely different call
types.
However, pulsed
or
pure tone calls
as
reported from eight
and
three species
of
Atelopus, respectively (COCROFT
& al.
1990),
are usually longer than
our
second call
re-
ceived from
A.
tricolor. Nevertheless,
in
overall structure (pulses, amplitude modu-
lation, frequency modulation)
it
resembles
the pulsed call type sensu COCROFT
& al.
(1990).
The
relatively short duration
of
this
call might possibly
be due to the
somewhat
unusual high temperature during recording
(A.
tricolor
is a
montane forest inhabiting
species). However,
it
cannot
be
excluded
that
the
call recorded
by us
refers
to an un-
known type. Also from
the
(artificial)
be-
havioral context mentioned above,
the
longer call recognized
in A.
tricolor
may
best
be
interpreted
as an
advertisement call,
as suggested
for
pulsed calls
in
Atelopus
species studied
by
COCROFT
& al.
(1990).
Intraspeculc variation
and
interspecific
overlap suggest that
the
evolution
of at
least
short calls
has
been conservative
in
Atelopus.
Two observations
fit
well
to
this assumption:
(1) Sympatry
of two or
more species
of Ate-
lopus
is
rare (LOTTERS
1996: 96). (2)
Intras-
pecific acoustic communication
in
general
plays
a
less important role. Since many
spe-
cies
of
Atelopus (occasionally only
the
males)
have brightly colored throats
(e. g.,
LOTTERS
1996) signaling
at
least towards nearby males
may also
be
effected by inflated vocal sacs.
REFERENCES
COCROFT,
R. B. &
MCDIARMID,
R. W. & JAS-
LOW,
A. P.&
RuiZ-CARRANZA,
P. M.
(1990): Vocal-
izations
of
eight species
of
Atelopus (Anura: Bufonidae)
with comments
on
communication
in the
genus.- Copeia;
1990:631-643.
JASLOW,
A. P.
(1979): Vocalization
and
aggres-
sion
in
Atelopus chiriquiensis (Amphibia, Anura, Bufo-
nidae).-J. Herpetol.;
13:
141-145.
JASLOW,
A. P. &
LOMBARD,
R. E. (1996): Hear-
ing
in the
Neotropical frog, Atelopus chiriquiensis.-
Copeia; 1996: 428-432.
UNDQUIST,
E. D. &
HETHERINGTON,
T. E.
(1996):
Field studies
on
visual
and
acoustic signaling
in
the "earless" Panamanian golden frog, Atelopus zeteki.-
J. Herpetol.;
30:
347-354.
LOTTERS,
S.
(1996):
The
Neotropical toad genus
Atelopus. Checklist
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Biology
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&
Glaw).
LOTTERS,
S. &
WlDMER,
A.
(1997): Bioacoustic
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Dendrobates
lehmanni from northwestern South America (Amphibia:
Dendrobatidae),
pp.
237-245.
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B0HME,
W. &
BlSCHOFF,
W. &
ZlEGLER,
T.
(eds.): Herpetologia
bon-
nensis; Bonn (SEH).
MCDIARMID,
R. W.
(1971): Comparative
mor-
phology
and
evolution
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frogs
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Oreophrynella.- Bull.
Los
Angeles County.
Mus. Nat.
Hist;
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MEYER,
E.
(1996): Okologie
und
Biogeographie
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Den-
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tat
Ulm.
DATE
OF
SUBMISSION: September
1st, 1998
Corresponding editor: Heinz Grillitsch
AUTHORS: STEFAN LOTTERS, STEFFEN REICHLE, JORN KOHLER, Zoologisches Forschungsinstitut
und Mu-
seum Alexander Koenig, Adenauerallee
160, 53113
Bonn, Germany [e-mail: uzs5r6@uni-bonn.de]; FRANK GLAW,
Zoologische Staatssammlung, MunchhausenstraBe
21,
81247 Munchen, Germany, EBERHARD MEYER, Abteilung
Okologie
und
Morphologie
der
Tiere, Universitat Ulm, Albert-Einstein-Allee 11, 89069 Ulm, Germany.
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Full-text available
  • Sep 1996
Field studies were conducted on the visual and acoustic behavior of the Panamanian golden frog, Atelopus zeteki, a species lacking a tympanic middle ear. Males displayed three stereotyped behaviors in response to playbacks of male pulsed vocalizations: foot signaling, vocalization, and repositioning orientation. Frequencies of foot signaling and orientation responses were significantly increased by presentation of playback vocalizations. Vocal responses also increased (non-significantly) during the playback period and continued to increase during post-playback silence. These results provide the first experimental evidence that an "earless" anuran species displays behavioral responses to sound, and that vocalization may play an important role in communication. The forefoot waving, and possibly hindfoot raising observed in this species appear to represent visual signals used intraspecifically in male agonistic behavior. male frogs appear to rely preferentially on visual signaling (foot signaling) as compared to acoustic signaling (vocalizing). The existence and preferential use of visual signaling in this species may be correlated with their noisy, montane stream habitat. Orientation by the frogs toward the playback speaker suggests that this "earless" species of anuran is capable of localizing a sound source.
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Vocalizations of Eight Species of Atelopus (Anura: Bufonidae) With Comments on Communication in the Genus
Article
Full-text available
  • Sep 1990
  • COPEIA
Vocalizations of frogs of the genus Atelopus include three discrete types of signals: pulsed calls, pure tone calls, and short calls. Repertoire composition is conservative across species. Repertoires of most species whose calls have been recorded contain two or three of these identifiable call types. Within a call type, details of call structure are very similar across species. This apparent lack of divergence in calls may be related to the rarity of sympatry among species of Atelopus and to the relative importance of visual communication in their social interactions.
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Hearing in the Neotropical Frog, Atelopus chiriquiensis
Article
  • May 1996
  • COPEIA
Few studies have measured the hearing of frequencies above 1 kHz in anurans lacking middle ear structures. Auditory frequency threshold curves were determined under similar laboratory conditions for Atelopus chiriquiensis, which lacks a tympanum, middle ear cavity, and stapes, and Hyla regilla, a similarly sized species which has these middle ear structures characteristic of most frogs. Both species were found to have similar hearing capabilities, with bimodal threshold curves and peak sensitivities at about 0.2 kHz and 2-3 kHz. This record of hearing sensitivity in a frog lacking a tympanic ear corroborates a similar observation made by Loftus-Hills in 1973 for Pseudophryne semimarmorata, which also lacks most middle ear structures and is in a different family.
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Vocalization and Aggression in Atelopus chiriquiensis (Amphibia, Anura, Bufonidae)
Article
  • Apr 1979
Atelopus chiriquiensis were observed during May and June, in 1976 in Chiriqui Province, Panama. Three distinct male vocalizations were recorded and analyzed and their contexts are described. Calling males oriented toward calling neighbors and occasionally wrestled to defend calling sites. Wrestling included an apparent submissive posture and the flipping of opponents.
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Comparative morphology and evolution of frogs of the Neotropical genera Atelopus, Dendrophryniscus, Melanophryniscus, and Oreophrynella
Article
  • Jan 1971
Thesis (Ph. D.)--University of Southern California, 1969. "Literature cited": leaves 264-282.
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  • Jan 1996
  • 428-432
  • A P Jaslow
  • R E Lombard
JASLOW, A. P. & LOMBARD, R. E. (1996): Hearing in the Neotropical frog, Atelopus chiriquiensis.-Copeia; 1996: 428-432.
  • Jan 1996
  • S Lotters
LOTTERS, S. (1996): The Neotropical toad genus Atelopus. Checklist -Biology -Distribution;
Bioacoustic comparisons of the advertisement calls of the poison-dart frogs Dendrobates histrionicus and Dendrobates lehmanni from northwestern South America (Amphibia: Dendrobatidae)
  • Jan 1997
  • Herpetologia bon- nensis
  • S Lotters
  • A Wldmer
LOTTERS, S. & WlDMER, A. (1997): Bioacoustic comparisons of the advertisement calls of the poison-dart frogs Dendrobates histrionicus and Dendrobates lehmanni from northwestern South America (Amphibia: Dendrobatidae), pp. 237-245. In: B0HME, W. & BlSCHOFF, W. & ZlEGLER, T. (eds.): Herpetologia bonnensis;