Vocalizations of two anuran species from Costa Rica

ANARTIA

Publicación del Museo de Biología de la Universidad del Zulia

ISSN 1315-642X (impresa) / ISSN 2665-0347 (digital)

Anartia, 32 (junio 2021): 67-70

Description of two previously unknown anuran vocalizations

from the Caribbean rainforests of Costa Rica

Descripción de dos vocalizaciones de anuros previamente desconocidas

del bosque húmedo caribeño de Costa Rica

Stanley Salazar1, Andrés Camilo Montes-Correa2 & César L. Barrio-Amorós3

1DOSEL SA, Rain Forest Adventures, La Esperanza, Horquetas, Sarapiquí, Heredia, Costa Rica.

2Grupo de Investigación en Manejo y Conservación de Fauna, Flora y Ecosistemas Estratégicos Neotropicales (MIKU),

Universidad del Magdalena, Santa Marta, Colombia.

3CRWild / Doc Frog Expeditions, Uvita, Puntarenas, Costa Rica.

Correspondence: César L. Barrio-Amorós: cbarrioamoros@crwild.com

(Received: 05-05-2021 / Accepted: 28-06-2021 / Online: 15-10-2021)

e small Central American country of Costa Rica is

known to have one of the highest diversities of amphibians

per surface area on the planet, with 215 species in 51.100

km2 (Savage 2002, Leenders 2016). Despite being one of

the best-studied countries in Latin America for its amphib-

ians fauna, with a long tradition of foreign and national

herpetologists regularly publishing about them (summa-

rized in Savage 2002, Leenders 2016), many aspects regard-

ing the taxonomy and natural history of most amphibians

remain poorly understood or completely unknown.

Two species of anurans from the Caribbean versant

of Costa Rica, the hylid Ecnomiohyla sukia Savage and

Kubicki, 2010 (Fig 1A) and the craugastorid Craugastor

megacephalus (Cope 1876, Fig 2A), are the subjects of this

work. While the male advertisement call (AC) of E. sukia

has been previously described (Savage & Kubicki 2010),

herein we document for the rst time the female call (FC)

of this species. With the FC described herein, E. sukia is

now known to be one of the few hylids to have female call-

ing behavior. e advertisement call of C. megacephalus is

also documented here for the rst time. We classify our

recorded calls of E. sukia and C. megacephalus according

to the functional categories proposed by Wells (2007) for

the acoustic repertory of anurans. To describe the FC of E.

sukia and AC of C. megacephalus, recorded vocalizations

were extracted from the original sound les that were gen-

erated in the eld (using a cell phone Wavepad app of An-

droid in wav format), and analyzed with PRAAT 6.0.13

for Windows (Boersma & Weenink 2007). For the FC

of E. sukia the following parameters were measured, note

duration (in seconds –s–), inter-note interval (s), rate of

notes per second (notes/s), and dominant frequency (Hz)

were measured. Means (x) and standard deviations (SD)

were calculated for each call trait. For the AC of C. mega-

cephalus, the following characters were measured: call du-

ration in seconds (s), inter-call interval (s), call repetition

rate per minute (calls/m), dominant frequency (Hz), and

visible harmonics. Our terminology follows that proposed

and revised by Köhler et al. (2017) for call traits. Oscillo-

grams and spectrograms were obtained with the Seewave

package (Sueur et al. 2008) for the R platform.

e fringe-limbed treefrogs of the genus Ecnomiohyla

are some of the most mysterious and elusive anurans in the

Neotropics (Kubicki & Salazar 2015). Ecnomiohyla sukia

was described in 2010 (Savage & Kubicki 2010) from the

Atlantic versant of Costa Rica based on a few specimens

from Guayacán de Siquirres and Fila Asunción, both lo-

calities in Limón Province. e known advertisement call

consists of 13 to 20 staccato barks repeated aer a time gap

of up to or more than an hour. e AC of E. sukia was de-

scribed from a single male in captivity; it consisted of 15-

16 separate notes with a dominant frequency of 1.15kHz

DOI: https://doi.org/10.5281/zenodo.5571329

S. Salazar, A. C. Montes-Correa & C. L. Barrio-Amorós

(Savage & Kubicki 2010). Vocalizations used for the de-

scription of the AC for this taxon were taken at 22.15h

and 22.52h (Savage & Kubicki 2010). Until now, a female

vocalization has never been described for any species of

the genus Ecnomiohyla (Duellman, 2001, Mendelson et al.

2015, Wells 2007). Our description of the FC of E. sukia

(Fig. 1B) is based on a single vocalization emitted by an

individual located approximately 17m above the ground

in the forest canopy (thus the low quality of the recording)

at Finca la Guacamaya, near Santa Clara (N 10.219, W

83.949). Due to the distance of the female individual from

the cellphone microphone at the time she emitted the re-

corded vocalization analyzed herein, the overall quality

is less then optimal, but of sucient enough intensity to

perform our analysis. is call consists of a series of seven

tonal short notes (call duration = 6.643 s; note duration =

0.222–0.295 s, X = 0.257 s, SD = 0-031 s) emitted in an

inter-note of 0.710–1.145s (X = 0.9808, SD = 0.167) and

a note repetition rate of 1.054 notes/s. Bandwidth ranges

between 822–1749 Hz, with a dominant frequency of

1274.97–1337.14 Hz (X = 1305.18, SD = 20.01), and an

apparent ascendant modulation frequency. is vocaliza-

tion does not have detectable harmonics. e FC of E.

sukia is like that of a bird, diering from the dog-like AC

reported by Savage & Kubicki (2010). e AC of E. sukia

described by Savage & Kubicki (2010) is very similar to the

FC; in general terms, the FC and AC of E. sukia share the

same structure of a series of short tonal short notes. Even

though the AC and FC have notes of similar duration (AC

= 0.220–0.252s, FC = 0.222– 0.295), the AC has twice as

many notes (AC= 15–16 notes, FC = 7 notes) in shorter

intervals (AC = 0.287–0.302 s, FC = 0.710–1.145s), so

the rate of repetition of the notes is higher (AC = 1.93–

1.94 notes/s, FC = 1.054 notes/s). Additionally, the dom-

inant frequency of the AC is slightly lower than that of the

FC (AC=1150 Hz, FC= 1274.97–1337.14 Hz). Female

E. sukia call more oen than males, and therefore, they are

easier to nd in the high vegetation. Females of E. sukia

have been observed vocalizing from the bark of the trunk

and branches of trees, in addition to the surrounding veg-

etation in the canopy, while males have only been seen call-

ing from in and around reproductive tree holes (pers. obs.

SS). e peak of activity is during dusk and early hours of

the night (17-19 h). When the weather is drier and there

is a fair amount of moonlight, females of E. sukia can be

heard calling even until midnight. As many as 20 dier-

ent females have been heard calling from the margins of a

single forest clearing (pers. obs. SS), but none seemed to

be specically calling in a reciprocal fashion to male vocal-

izations, which are much more sporadic. A single female

individual was recorded while vocalizing and subsequently

collected on 04 June 2015 at Finca la Guacamaya in Sara-

piquí, Heredia province. It was calling from a site in the

canopy located 17 m above the ground. e sex of this in-

dividual of E. sukia was conrmed aer its collection by

the examination of its internal organs by Brian Kubicki.

Few female anurans are known to produce vocalizations

(Wells 2007). Several functions of female calling have been

proposed, including easing males to locate them by stimu-

lating an increase of calling from close males, identication

Figure 1. Calling female of Ecnomiohyla sukia (A) and the courtship call (B).

Vocalizations of two anuran species from Costa Rica

of territorial and satellite males, and identication of other

females as competitors (Emerson & Boyd 1999). e case

reported herein is the rst FC described from the genus

Ecnomiohyla, although, we are aware of at least one other

species producing it (Víctor Jiménez-Arcos, pers. comm.).

Currently, we are not sure about the function of the female

vocalization in this species.

Some species of the genus Craugastor are very secretive

or have suered extensive declines (Savage 2002, Leenders

2016). eir elusive habits are not well-known, and most

act as sit and wait predators. An intermittent and untrace-

able call was heard a multitude of times in the forest by

SS at Finca la Guacamaya, near Santa Clara (N 10.219,

W83.949), but we were unable to locate the source of

the vocalization, until a single recording was made at a

horizontal distance of about seven meters; the individual

responsible for this call was located under the leaf-litter,

it was a male C. megacephalus. Male C. megacephalus are

typically dicult to locate, compared to juveniles (which

are the most common) and females (common in certain

areas), and are always hidden under leaf litter or rotten

logs. e hours of calling activity are restrained to dusk.

Craugastor megacephalus males appear to be actively call-

ing during the drier months (March through May) of the

Caribbean versant of Costa Rica. e description of the

AC of C. megacephalus is based in a series of nine calls. e

AC of C. megacephalus consists of a single tonal short note

(call duration = 0.038–0.052s, X = 0.042 s, SD=0.004 s,

Fig. 2B) emitted at irregular intervals. Notes can be emit-

ted with pauses between them of less than a half second or

as infrequent as having pauses lasting more than ten sec-

onds (inter-call interval = 0.492–13.755 s, X = 8.640s,

SD = 5.282 s). e call series last 69.5 s, with a repetition

rate of 7.7 calls/minute. e prevalent bandwidth rang-

es between 286–2870 Hz, with a dominant frequency

of 1050.11–1205.23 Hz (X=1154.82 Hz, SD = 52.45

Hz). In addition, the AC of C. megacephalus exhibits

two visible harmonics, the rst at 1550.59–1844.45 Hz

(X=1730.50 Hz, SD=87.51 Hz), and the second at

2088.81–2436.32 Hz (X = 2311.94 Hz, SD =110.32

Hz).

According to Savage and Myers (2002), no advertise-

ment calls of any member of the Craugastor gulosus species

group (sensu Hedges et al. 2008) is known. Padial et al.

(2014) situated C. megacephalus in a more comprehensive

Craugastor punctariolus species group. One of the char-

acteristics of the former is the absence of vocal slits and a

vocal sac. Nevertheless, the absence of these organs does

not necessarily represent the inability to vocalize (which

has also been evidenced for other groups such as the for-

mer Craugastor laticeps species group; Ibáñez et al. 2012,

Salazar-Zúñiga & García-Rodríguez 2014). e descrip-

tion of the AC of C. megacephalus included herein opens

new perspectives for future bioacoustic studies, as well as

questions about the evolution of acoustic communication

of craugastorid frogs.

ACKNOWLEDGEMENTS

SS wants to thank Brian Kubicki for his help in deter-

mining the sex of the female specimen of Ecnomiohyla

sukia mentioned in the publication. He also was a mindful

referee, which along with another anonymous one helped

to improve this work.

Figure 2. Calling male of Craugastor megacephalus (A) and the advertisement call (B).

S. Salazar, A. C. Montes-Correa & C. L. Barrio-Amorós

REFERENCES

Boersma, P. & D. Weenink. 2013. Praat, a system for doing pho-

netics by computer. Glot International 5: 341–345.

Cope, E. D. 1876. On the Batrachia and Reptilia of Costa Rica.

Journal of the Academy of Natural Sciences of Philadelphia 8:

93–154.

Duellman, W. E. 2001. Hylid ogs of Middle America. 2 vols.

[2nd ed.]. [St. Louis, Mo]: Society for the Study of Amphib-

ians and Reptiles, Contributions to Herpetology, xv + x +

1159 pp., 92 pls.

Emerson, S. B. & S. K. Boyd. 1999. Mating vocalizations of fe-

male frogs: control and evolutionary mechanisms. Brain Be-

havior Evolution 53: 187–97.

Hedges, S. B., W. E. Duellman & M. P. Heinicke. 2008. New

World direct-developing frogs (Anura: Terrarana): molecu-

lar phylogeny, classication, biogeography, and conservation.

Zootaxa 1737: 1–182.

Ibáñez, R., C. A. Jaramillo & F. A. Solís. 2012. Description of the

advertisement call of a species without vocal sac: Craugastor

gollmeri (Amphibia: Craugastoridae). Zootaxa 3184: 67–68.

Köhler, J., M. Jansen, A Rodríguez, P. J. R. Kok, L. F. Toledo,

M. Emmrich, F. Glaw, C. F. B. Haddad, M. O. Rödel & M.

Vences. 2017. e use of bioacoustics in anuran taxonomy:

theory, terminology, methods, and recommendations for

best practice. Zootaxa 4251: 1–124.

Kubicki, B. & S. Salazar. 2015. Discovery of the Golden-eyed

Fringe-limbed Treefrog, Ecnomiohyla bailarina (Anura: Hy-

lidae), in the Caribbean foothills of southeastern Costa Rica.

Mesoamerican Herpetology 2: 76–86.

Mendelson, J. R., III, A. Eichenbaum & J. A. Campbell. 2015.

Taxonomic review of the populations of the Fringe-limbed

Treefrogs (Hylidae: Ecnomiohyla) in Mexico and nuclear

Central America. South American Journal of Herpetology 10:

187–194.

Padial, J. M., T. Grant & D. R. Frost. 2014. Molecular system-

atics of terraranas (Anura: Brachycephaloidea) with an as-

sessment of the eects of alignment and optimality criteria.

Zootaxa 3825: 1–132.

Salazar-Zúñiga, J. A. & A. García-Rodríguez. 2014. Advertise-

ment call of Craugastor noblei: another calling species of the

Craugastor gollmeri group (Anura: Craugastoridae). Phyllo-

medusa 13: 67–70.

Savage, J. M. 2002. e Amphibians and Reptiles of Costa Rica:

a herpetofauna between two continents, between two seas. Chi-

cago: University of Chicago Press, 934 pp.

Savage, J M. & C. W. Myers. 2012. Frogs of the Eleutherodac-

tylus biporcatus group (Leptodactylidae) of Central America

and northern South America, including rediscovered, res-

urrected, and new taxa. American Museum Novitates 3357:

1–21.

Savage, J. M. & B. Kubicki. 2010. A new species of fringe-limb

frog, genus Ecnomiohyla (Anura: Hylidae), from the Atlan-

tic slope of Costa Rica, Central America. Zootaxa 2719:

21–34.

Sueur, J., T. Aubin & C. Simonis. 2008. Seewave: a free modular

tool for sound analysis and synthesis. Bioacoustics 18: 213–

226.

Wells, K. D. 2007. e ecology and behavior of amphibians. Chi-

cago: e University of Chicago Press, 1148 pp.