Advertisement Call of A Population of The Nurse Frog Leucostethus Fraterdanieli (Anura: Dendrobatidae), With Notes On Its Natural History
Advertisement Call of A Population of The Nurse Frog Leucostethus Fraterdanieli (Anura: Dendrobatidae), With Notes On Its Natural History
Advertisement Call of A Population of The Nurse Frog Leucostethus Fraterdanieli (Anura: Dendrobatidae), With Notes On Its Natural History
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Abstract
We describe the advertisement call of seven males and observations on the natural history related to the paren-
tal attention by males, of a population of nurse frogs attributed to the Leucostethus fraterdanieli complex from the
Central Cordillera in the Department of Caldas, Colombia. The advertisement call consists of a long sequence
of repeated (x̅ = 143 notes.min-1) pulsed notes, which have an average duration of 79 ± 17 ms (range 63-122 ms),
separated by time intervals between 187-413 ms (289 ± 67 ms). The dominant frequency values are in the range
between 3209-3520 Hz. Our results suggest differences in temporal and spectral parameters between the popula-
tion studied and other populations assigned to L. fraterdanieli, L. brachistriatus, and the recently described L. jota.
Key words. Amphibia. Andes. Bioacoustics. Caldas. Colombian Central Cordillera. Male brooding behavior.
Phytotelmata.
Resumen
Describimos el canto de advertencia de una población atribuida a Leucostethus fraternadieli de los Andes centrales
de Colombia, basados en el análisis temporal y espectral del canto de siete machos, y aportamos observaciones
de historia natural asociadas al cuidado parental de los machos. El canto de advertencia consiste en una larga
secuencia de notas pulsadas repetidas (x̅ = 143 notes.min-1), las cuales tienen una duración promedio de 79 ∓ 17
ms (rango 63-122 ms), separadas por intervalos de tiempo de entre 187-413 ms (289 ∓ 67 ms). Los valores de fre-
cuencia dominante registrados están en el rango entre 3209-3520 Hz. Nuestros resultados sugieren diferencias en
parámetros temporales y espectrales entre la población estudiada y otras poblaciones asignadas a L. fraterdanieli,
L. brachistriatus, y la especie recientemente descrita L. jota.
Palabras clave. Amphibia. Andes. Atención de nidadas. Bioacústica. Caldas. Cordillera Central de Colombia.
Fitotelmata.
Urticaceae), dulomoco (Saurauia cuatrecasana, Actini- call of L. fraterdanieli complex consisted of one note emit-
daceae), drago (Croton magdalenensis, Euphorbiaceae), ted in fast succession, with a mean call rate of 143 notes.
nigüito (Miconia poecilantha, M. theaezans, Melastoma- min-1 (range 93-168; Table 1; Figure 1), each sounding
taceae), wax palm (Ceroxylon quindiuense, Arecaceae), like a ‘peep’ to the human ear. The notes had an average
among many others (Vargas, 2002). duration of 79 ∓ 17 ms (63-122 ms) and were separa-
ted by inter-note intervals of 289 ∓ 67 ms (187-413 ms).
Call analysis. The advertisement call of seven indivi- The dominant frequency of the call was 3338.75 ∓ 99.99
duals of the L. fraterdanieli complex is described based Hz (3209-3520 Hz); the minimum frequency 2812.5 ∓
on recordings made by the first author on 12 May 2012 74.34 Hz (2692-2899 Hz) and the maximum frequency
between 14:33-17:32 h. For the description, 84 calls in to- 3881.91 ∓ 69.91 Hz (3830-4037 Hz). All recorded males
tal (12 calls for each male), randomly selected from one presented harmonic bands in their calls, but there were
minute of recording for each individual were analyzed. differences in the number of bands registered for each
Males were recorded at 50-70 cm average distance with male (see Table 1). Harmonic 1 ranged from 4850 to
a Sennheiser© ME64 cardioid unidirectional micropho- 5487 Hz, harmonic 2 from 6315 to 7350 Hz, harmonic 3
ne, adapted to a Marantz© PMD620 digital recorder. from 7971 to 9317 Hz, harmonic 4 from 9736 to 10 973
Temperature (Table 1) was registered at the time of each Hz, harmonic 5 from 11 387 to 11 932 Hz. The harmo-
recording, with an Extech© EA25 infrared thermometer, nic 6 (13 173-13 459 Hz), harmonic 7 (14 795-15 114 Hz),
and male’s snout-to-vent length (SVL) was measured and harmonic 8 (18 327-18 614 Hz) were present only
with a 0.01 mm Mitutoyo© MI-500-171-30B precision’s in male 01. Notes were typically pulsed (2-11 pulses.
caliper (Table 1). Because the individuals of L. fraterdanie- note; Figure 2), although a small fraction of the notes
li complex have shown an aggregate local distribution, did not have pulses. Pulses have a duration of 4 ∓ 0.5
the recordings were taken at least 5-20 m apart for each ms (2-7 ms). Table 1 summarizes the acoustic attributes
male, to avoid pseudoreplication. No voucher specimens of the analyzed individuals.
were collected in this study; however, 13 vouchers from
this locality are housed at the herpetological collection Natural history observations. At the study site
of the Museo de Historia Natural, Universidad de Cal- (Figure 3A), Leucostethus fraterdanieli complex is the
das (MHN-UCa 416-418, 447-452, 831-834). We followed most abundant diurnal amphibian species in the local
Wells (2007), Toledo et al. (2015) and Köhler et al. (2017) assemblage. In a small area of 25 m2 in which two of the
for the description of the temporal and spectral parame- sound tracks were recorded, twelve individuals were
ters of the calls. Recordings were digitized and analyzed counted calling hidden under the leaf litter of white
with the software RAVEN © Pro 1.4 (Bioacoustics Re- yarumo trees (Cecropia telealba) and bamboos (Guadua
search Program 2011) at a resolution of 16 bits and 44.1 angustifolia) (Figure 3B). In this site, on February 9, 2012,
kHz sampling rate. Oscillograms and spectrograms were a male attending a clutch was found placed on a dry
analyzed with a FFT (Fast Fourier Transformation) of bromeliad leaf (Aechmea sp.) at 1.25 m above the ground,
512 points and Hann algorithm. Description of the call and approximately 40 m away from the nearest water
parameters are presented as mean ∓ standard deviation body (Figure 4A). The male (SVL 23.7 mm) was in clo-
(range). During the course of other research (2010-2012), se contact with the egg mass performing a ‘brooding
the first author gathered additional information on mi- behavior’ sensu Vockenhuber et al. (2008) (Figure 4B).
crohabitat and specific observations on the behavior The sex of the individual was determined based in the
and activity of wild individuals in areas close to that black spots in the throat and the swollen third finger,
of this study (municipalities of Neira and Villamaría, which are characteristics in adult males (Grant & Cas-
Department of Caldas). tro 1998). The egg-clutch contained 17 eggs in develo-
pmental stage 17 sensu Gosner (1960) (Figure 4C). Both
the male and the egg-clutch were monitored between
Results 07:00-18:00 h, time during which the male remained
Advertisement call. Males of the L. fraterdanieli complex attending eggs while staying on top of them. For other
recorded in the study area called synchronically, over- forested sites sampled near the cities of Manizales, Vi-
lapping during this activity. When a male began to emit llamaría, and Neira, Department of Caldas, we observed
advertisement calls, almost immediately neighbouring that adults of the L. fraterdanieli complex were usually
individuals also started to vocalize, forming a chorus located at a distance (> 50 m) from water bodies du-
audible at great distance (> 30 m). The advertisement ring the day, with a calling activity from early morning
Number of male
Parameter 01 02 03 04 05 06 07
Snouth vent-length (mm) 23.37 22.7 21.8 22.2 22.95 21.5 22.25
Temperature (°C) 27 27 28 28 26 21 21
DOI: 10.21068/c2021.v22n01a08
Note duration (ms) 66 ± 27 (58-106) 79 ± 17 (63-122) 105 ± 18 (48-134) 71 ± 19 (23-97) 71 ± 19 (66-87) 67 ± 18 (59-93) 69 ± 15 (43-92)
Number of pulses/note 7.33 ± 3.214 (5-11) 8 ± 5.932 (2-15) 6.905 ± 2.165 (2-10) 5.25 ± 2.121 (2-9) 6.703 ± 3.114 (2-12) 6.956 ± 3.117 (2-14) 6.202 ± 3.117 (2-9)
Pulse duration (ms) 5 ± 3 (2-7) 4 ± 1 (4-7) 4 ± 2 (4-6) 4 ± 2 (4-6) 5 ± 1 (4-6) 5 ± 2 (3-6) 4 ± 2 (3-5)
0.633 ± 0.072 0.289 ± 0.067 0.425 ± 0.097 0 . 4 2 4 ± 0 . 0 7 0.476 ± 0.085 0.421 ± 0.068 0.423 ± 0.068
Inter-note intervals (s) (0.466-0.765) (0.187-0.413) (0.274-0.613) (0.35-0.572) (0.28-0.586) (0.367-0.585) (0.327-0.497)
2530.58 ± 86.84 2648.66 ± 184.37 2736.5 ± 148.59 2 8 1 2 . 5 ± 7 4 . 3 4 2 6 5 2 . 5 ± 9 1 . 2 2 2850.6 ± 85.413 2 7 6 8 ± 7 5 . 3 5
Fundamental frecuency (Hz) (2386-2673) (2381-2899) (2482-2959) (2692-2899) (2390-2906) (2460-2880) (2560-2760)
3135.41 ± 59.516 3355.75 ± 12047 3 3 2 0 ± 4 5 . 8 5 7 3338.75 ± 99.991 3 3 5 5 ± 5 4 . 2 3 3 2 0 ± 4 3 . 3 1 3 3 2 0 ± 4 5 . 6 7 1
Dominant frecuency (Hz) (3055-3245) (3209-3623) (3245-3375) (3209-3520) (3209-3623) (3200-3495) (3220-3530)
3684.25 ± 66.566 4080.41 ± 142.79 3961.5 ± 95.545 3881.91 ± 61.914 3 9 5 5 ± 6 5 . 6 3 3 9 3 0 ± 6 1 . 3 2 1 3 8 7 0 ± 9 5 . 2 3
Maximum frecuency (Hz) (3627-3830) (3934-4348) (3818-4105) (3830-4037) (3818-4037) (3846-4055) (3810-3970)
4924.08 ± 86.593 5262.75 ± 164.14 5003.58 ± 75.675 4 9 1 7 ± 7 0 . 1 1 6 4 9 7 5 ± 8 6 . 5 8 5 0 2 5 ± 7 3 . 2 1 4 9 1 0 ± 6 8 . 2 3
Harmonic 1 (Hz) (4865-5155) (5073-5487) (4868-5155) (4865-5073) (4860-5120) (4920-5145) (4850-5140)
6640.58 ± 98.74 7099.58 ± 251.43 6 6 5 0 ± 7 4 . 3 8 5 6513.16 ± 93.113 6 5 5 5 ± 7 2 . 3 8 6 5 6 0 ± 9 5 . 3 5 4 6 5 7 0 ± 7 8 . 1 3 4
2 (6522-6873) (6729-7350) (6491-6777) (6315-6625) (6507-6642) (6495-6615) (6315-6615)
8300.75 ± 107.933 8807.83 ± 375.79 8320.5 ± 156.71 8178.16 ± 108.102 8 3 4 3 ± 1 2 3 . 6 4 8 2 9 0 ± 1 0 3 . 2 2 8307 ± 106.432
3 (8209-8495) (8385-9317) (8018-8591) (7971-8385) (8260-8535) (8135-8350) (8270-8345)
10 010.66 ± 136.71 10 593 ± 313.01 (10 9998.91 ± 116.06 9851.91 ± 115.5 9 9 6 0 ± 1 1 6 . 0 1 10 050 ± 132.05 9 9 5 0 ± 1 2 5 . 3 4
4 (9736-10 214) 145-10 973) (9832-10 214) (9627-10 042) (9832-10 060) (9809-10 150) (9854-10 050)
11 654 ± 101.842 11 508.08 ± 59.651
5 (11 550-11 932) (11 387-11 594)
13 281.75 ± 68.038
6 (13 173-13 459)
14 967 ± 78.165 (14
7 795-15 114)
18 422.75 ± 107.899
8 (18 327-18 614)
Rojas-Morales et al.
Rojas-Morales et al. Advertisement call of a population of the nurse frog
Figure 1. Oscillogram, spectrogram, and power spectrum of the advertisement call of Leucostethus fraterdanieli (male 02 in
Table 1, SVL 22.7 mm), from Manizales, Caldas, Colombia. Visualization of five seconds of recording; temperature 27 °C.
Figure 2. Oscillogram, spectrogram, and power spectrum of a pulsed note of an adult individual (male 06 in Table 1, SVL
21.5 mm) of the Leucostethus fraterdanieli complex from Manizales, Caldas, Colombia. Temperature, 21 °C.
(06:30-07:00 h) to the late afternoon (18:00-18:30 h). In 4000 Hz. In general terms, this call seems to be similar
contrast, we observed at night that parental males fre- to that ‘chirp call’ type defined by Lötters et al. (2003).
quented leaf litter or rocks at the edge of small streams, The call here described is similar in general patterns to
carrying up to 15 larvae on their backs (N = 4, range that described by Grant & Castro (1998) as the adver-
12-15 larvae; Figure 3C). Tadpoles aggregated at the ed- tisement call of L. brachistriatus (as C. fraterdanieli), ba-
ges of small streams and creeks (0.4-3.5 m width), with sed on two males collected within a cloud forest in the
abundant sand and rocky soil (Figure 3D). western slopes of the Cordillera Occidental, Department
of Valle del Cauca. The call was described like a single
note repeated up to 300 times, with frequencies between
Discussion 3156-3250 Hz and harmonics occurring at 4800-6400 Hz
Since anuran acoustic signals are species-specific and (Individual 1), and 3593-3656 Hz and harmonics in the
play a critical role in species recognition and mate choi- bands of 5500-7400 Hz (Individual 2; Grant & Castro,
ce (Wells, 2007), advertisement call analysis is a power- 1998). However, there is a difference in the note dura-
ful tool to recognize distinct species. The advertisement tion. For the population of the Western Cordillera, notes
call of the population of the L. fraterdanieli complex des- ranged between 38-49 ms (Grant & Castro, 1998), while
cribed here can be characterized as a long train of re- for the population that we analyzed in the Central An-
peated ‘peep’ notes, with a maximum frequency up to des, note duration was between 63-122 ms.
Figure 3. A, habitat of Leucostethus fraterdanieli complex at the Botanical Garden of the Universidad de Caldas, Manizales,
Colombia, 2150 m a.s.l.; B, calling male concealed in a caulinar fallen leaf of bamboo (Guadua angustifolia) at this site; C, male
carrying tadpoles on dorsum, before depositing them in a body of water, from the Chisperos creek, located near Manizales;
D, tadpole at a margin of the Chisperos creek. Photographs by J. A. Rojas-Morales.
Recently, Marín et al. (2018) presented a bioacoustic within Colostethus) from the Upper Cauca river valley
comparison between L. fraterdanieli and L. jota from the and the Central Cordillera (Grant & Castro, 1998; Marín
Central Cordillera, in Antioquia. The call described for et al., 2018). However, individuals from Manizales are
L. fraterdanieli includes values between 3100-3500 Hz, a morphologically indistinguishable from L. fraterdanieli
rate of 98 ∓ 12.5 calls.min-1, with a call duration of 0.09 sensu stricto (fide Grant et al., 2017). An integrative
± 0.03 s and intervals between calls 0.55 ± 0.16 s. These approach, including a molecular analysis and a study
results are quite different in temporal traits from those of larval morphology, is badly needed to assess the ta-
of L. fraterdanieli complex from Manizales (call rate 98 xonomic status of this and other populations under the
vs 143 calls.min-1). Compared to L. jota, the advertise- name of L. fraterdanieli in the Colombian Andes.
ment call of the population of L. fraterdanieli complex
presented here shows major differences in temporal Life history data for Colostethinae frogs are limited
parameters. A higher call duration (0.14 vs. 0.079 s), (Wells, 1980; Coloma, 1995; Duellman 2004). Ovipo-
lower call rate (21.8 vs. 143 calls.min-1), and higher call sition sites recorded in these frogs include shadow lo-
interval (2.55 vs. 0.289 s) differentiates L. jota from L. cations in mosses and under stones (Coloma, 1995).
fraterdanieli complex from Manizales. Guevara-Molina Parental care of the embryos and eggs are carried out
et al. (2017) presented information on the biology of L. by males; however, in species such as Colostethus pa-
fraterdanieli (L. brachistriatus sensu Grant et al., 2017), in- namensis, C. pratti and C. argyrogaster, the female is in
cluding an oscillogram and spectrogram of a call from charge of this function (Wells, 1980; Duellman, 2004).
the Department of Quindío, in the central Andes, but Despite this, microhabitat for oviposition is unknown
no additional details were provided. for a large proportion of Colostethus and Leucostethus
species. For L. fraterdanieli complex from Manizales,
Our results show that the advertisement call of the po- we observed one oviposition site located on a dead leaf
pulation of L. fraterdanieli complex from Manizales is of a terrestrial bromeliad (Figure 4A). To our knowle-
quite different from other known Leucostethus (formerly dge, this is the first reference for an oviposition site in
Figure 4. Oviposition site of individual of the Leucostethus fraterdanieli complex in the Botanical Garden of the Universidad
de Caldas, Manizales, Colombia, 2150 m a.s.l. A, terrestrial bromeliad (Aechmea sp.) used as oviposition site; B, detail of the
leaf where a male (SVL 23.7 mm) is attending a clutch in ventral brooding-behavior; C, egg-clutch with 17 embryos. Photo-
graphs by J. A. Rojas-Morales.
Leucostethus. We also observed males performing pa- cies complex with description of two new species
rental care –i. e., egg-brooding– of an egg-clutch, and from Central Peru (Anura: Dendrobatidae). Zoota-
transporting larvae to the water, which show the role of xa, 1823, 1-24.
males in the parental care of embryos until they conti- https://doi.org/10.11646/zootaxa.1823.1.1
nue their aquatic phase. However, reproductive activity Brown, J. L., Morales, V. & Summers, K. (2008b). Diver-
and behavior patterns may vary from one population gence in parental care, habitat selection and larval
to another and from year to year (Wells, 1980); for that life history between two species of Peruvian poison
reason, is important to monitor this population over frogs: an experimental analysis. Journal of Evolutio-
several years, in order to obtain data on territorial be- nary Biology, 21, 1534-1543.
havior, courtship, amplexus, and parental care of the https://doi.org/10.1111/j.1420-9101.2008.01609.x
eggs and embryos. The distinctive call, its preference for Brown, J. L., Twomey, E., Morales, V. & Summers, K.
forested habitats and its abundance predicted through (2008c). Phytotelm size in relation to parental care
the calls, make this species a good model for bioacoustic and mating strategies in two species of Peruvian
monitoring to detect population trends in these Andean poison frogs. Behaviour, 145, 1139-1165.
highly transformed ecosystems. https://doi.org/10.1163/156853908785387647
Brown, J. L., Twomey, E., Amézquita, A., De Souza,
M., Caldwell, J. P., Lötters, S., Von May, R., Me-
Acknowledgments lo-Sampaio, P. R., Mejía-Vargas, D., Pérez-Peña, P.,
JAR is deeply grateful to Paul D. Gutiérrez for the loan Pepper, M., Poelman, E. H., Sánchez-Rodríguez, M.
of the recording equipment, and to José Humberto Ga- & Summers, K. (2011). A taxonomic revision of the
llego for the permit access at the Botanical Garden of Neotropical poison frog genus Ranitomeya (Amphi-
the Universidad de Caldas. We are grateful to Moisés bia: Dendrobatidae). Zootaxa, 3083, 1-120.
Escalona, Estefany Cano and two anonymous reviewers https://doi.org/10.11646/zootaxa.3083.1.1
for their helpful comments on the manuscript. Cárdenas-Ortega, S. & Herrera-Lopera, M. (2016). Co-
lostethus fraterdanieli (Santa Rita Rocket frog, Rana
Cohete). Anurophagy. Herpetological Review, 47(3),
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https://doi.org/10.1007/s10211-014-0194-4 001.0001
Julián A. Rojas-Morales
Corporación Universitaria Santa Rosa de Cabal (UNISARC),
Santa Rosa de Cabal – Risaralda Colombia
[email protected] Advertisement call of a population of the nurse frog
https://orcid.org/0000-0002-3312-8022
Leucostethus fraterdanieli (Anura: Dendrobatidae),
with notes on its natural history
Enrique La Marca
Universidad de Los Andes, Mérida, Venezuela Citación del artículo: Rojas-Morales, J.A., La Marca, E. &
[email protected] Ramírez-Chaves, H.E. (2021). Advertisement call of a po-
https://orcid.org/0000-0002-6508-3375 pulation of the nurse frog Leucostethus fraterdanieli (Anura:
Dendrobatidae), with notes on its natural history. Biota
Colombiana, 22(1), 123-133. https://doi.org/10.21068/
Héctor E. Ramírez-Chaves
c2021.v22n01a08
Museo de Historia Natural, Universidad de Caldas,
Manizales, Colombia
[email protected]
Received: May 8, 2020
https://orcid.org/0000-0002-2454-9482
Accepted: November 9, 2020