Call Structure and Activity Period of Pristimantis festae, a High-Elevation Anuran in Ecuador

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———, s. d. Marshall, J. boundy, and a. a. WilliaMs. 2006. Status and
geographic expansion of the Mediterranean gecko, Hemidactylus
turcicus, in Louisiana: implications for the southeastern United
States. Herpetol. Conserv. Biol. 1:45–50.
Mitchell, J. c. 1982. Geographic distribution: Anolis sagrei. Herpetol.
Rev. 13:80.
Myers, s. 1977. Geographic distribution: Osteopilus septentrionalis.
Herpetol. Rev. 8:12.
Plotkin, M., and r. atkinson. 1979. Geographic distribution: Eleu-
therodactylus planirostris. Herpetol. Rev. 10:59.
riCHArdson, d. M., P. Pyšek, M. reJMÁnek, M. g. bArbour, F. d. PAneTTA,
and c. J. West. 2000. Naturalization and invasion of alien plants:
concepts and definitions. Divers. Distrib. 6:93–107.
schWartz, a. 1952. Hyla septentrionalis Duméril and Bibron on the
Florida mainland. Copeia 1952:117–118.
seebens, h., t. M. blackburn, e. e. dyer, P. genovesi, P. e. hulMe, J. M.
Jeschke, s. Pagad, P. Pyšek, M. van kleunen, M. Winter, and M. ansong.
2018. Global rise in emerging alien species results from increased
accessibility of new source pools. Proc. Nat. Acad. Sci. 115:E2264–
E2273.
servoss, J. M., s. sFerra, t. r. Jones, M. J. sredl, and P. c. rosen. 2013.
Geographic distribution: Ramphotyphlops braminus. Herpetol.
Rev. 44:477.
skelton, c. n., and d. ParMley. 2005. Geographic distribution: Anolis
sagrei. Herpetol. Rev. 36:467.
slevin, J. r. 1930. A note on the discovery of the genus Typhlops in the
Hawaiian Islands. Copeia 1930:158
ssar (society For the study oF aMPhibians and rePtiles). 2018. Herpetolog-
ical Review Geographic Distribution Notes Formatting Guidelines.
https://ssarherps.org/wp-content/uploads/2018/07/GeoDist-
Notes_FormattingGuidelines-Jul2018.pdf, Accessed 18 June 2019.
steJneger, l. 1922. Two geckos new to the fauna of the United States.
Copeia 108:56.
Wilson, l. d. and l. Porras. 1983. The Ecological Impact of Man on the
South Florida Herpetofauna. Univ. Kansas Mus. Nat. Hist. Spec.
Publ. No. 9, Lawrence, Kansas. 83 pp.
Herpetological Review, 2019, 50(3), 479–483.
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Call Structure and Activity Period of Pristimantis festae,
a High-Elevation Anuran in Ecuador
Perhaps the most well-studied aspect of anuran communica-
tion, vocalizations play an integral role in mate attraction (Lit-
tlejohn 1977; Gerhardt 1991; Tobias et al. 1998), demarcation of
territory (Wagner 1989; Byrne 2009), and myriad other social in-
teractions (Wells 1977; Wells and Schwartz 2007). Environmental
factors such as temperature and humidity, as well as individual
intrinsic factors such as size, are known to cause variations in
call frequency and duration (Lingnau and Bastos 2007; De To-
ledo et al. 2009; Costa and Toledo 2013). However, the majority of
variation is caused by changes in behavioral context.
The genus Pristimantis (Craugastoridae) has undergone ex-
tensive taxonomic revision and contains ca. 530 currently rec-
ognized species (Hedges et al. 2008; Frost 2019). As with most
members of this group, species of Pristimantis are highly cryp-
tic, reclusive, and almost exclusively nocturnal (Lynch and Du-
ellman 1997). For this reason, species data on calls and behavior
are sparse (Duellman and Lehr 2009).
Included within the Pristimantis myersi group (Hedges et al.
2008; Padial et al. 2014), Pristimantis (Eleutherodactylus) festae
(Fig. 1) has received physical, distribution, and phylogenetic re-
lationship descriptions (Lynch and Duellman 1980; Heinicke et
al. 2007; Padial et al. 2014); however, vocalizations and period of
activity have not been well documented. Pristimantis festae is
a small, high-elevation anuran distributed in páramo and sub-
páramo Andean habitats, and primary and secondary forests
in the Napo, Imbabura, and Tungurahua provinces of northern
Ecuador at elevations between 2360 and 3650 m (Lynch and Du-
ellman 1980; Yánez-Muñoz et al. 2014). Although listed by the
IUCN as Endangered (Coloma et al. 2004), AmphibiaWebEcua-
dor Red List has it marked as Least Concern with major threats
being habitat destruction and degradation (Ron et al. 2011).
With 9.865 million hectares of total forested area in 2010 (Ba-
hamondez et al. 2010), Ecuador has experienced a 60% reduc-
tion of forest habitat since the early 20th century (Cabarle et al.
1989; Mosandl et al. 2008; Bahamondez et al. 2010). Because P.
festae is endemic to Ecuador and unlikely to occur in heavily dis-
turbed habitats (Yánez-Muñoz et al. 2014), deforestation along
with climate abnormalities and the spread of infectious disease
CHACE HOLZHEUSER*
Galo Plaza Lasso Foundation, Conservation Department,
Hacienda Zuleta, Zuleta, Ecuador
ANDRES MERINOVITERI
Museo de Zoología, Escuela de Ciencias Biológicas,
Ponticia Universidad Católica del Ecuador,
Avenida 12 de Octubre y Roca, Apartado17-01-2184, Quito, Ecuador
*Corresponding author; e-mail: c.holzheuser@gmail.com Fig. 1. Pristimantis festae found in Ecuador.
PHOTO BY SANTIAGO RON

Herpetological Review 50(3), 2019
480 ARTICLES
(Bustamante et al. 2005; Pounds et al. 2006; Lips et al. 2008) may
have led to population fragmentation as it has in other species of
the Ecuadorian highlands. Although chytrid fungus has not been
directly linked to this species, most likely because of a lack of
testing, it has been detected in other species of Pristimantis and
is a likely factor in their declines (Lips et al. 2008; Cusi et al. 2015;
Narvaez 2015). Therefore, it is imperative to document the call
behavior of P. festae so biologists may easily identify and docu-
ment populations in the field, thereby facilitating future popula-
tion assessments and conservation efforts.
Materials and Methods
Study Site.—San Pedro de la Rinconada, within the Haci-
enda Zuleta property, Zuleta Valley, Imbabura Province, Ecuador
(00.19223°N, 78.05978°W; NAD 27) is a high-elevation Andean
habitat at 2900 m. Although no official measurements have been
taken of this valley, Zuleta falls within the equatorial subpáramo
and páramo habitats (Buytaert et al. 2006) and is characterized
by seasonal stability with large, yet consistent, daily temperature
fluctuations (Hedberg 1964; Sarmiento 1986).
Call Structure.—We collected call samples from July to
August 2015 using a digital Olympus LS-10 linear PCM recorder
with a Sennheiser K6 microphone attachment. Calls were
analyzed using Raven 1.3 software (www.birds.cornell.edu/
raven) at a sampling frequency of 44.1 kHz and a frequency
resolution of 10.8 Hz. All calls were recorded within 2 m of the
subject. Measured call variables are defined using the definitions
found in Kok and Kalamandeen (2008). All acoustic parameters
are presented as mean ± standard deviation. The call recordings
have been deposited at the Museo de Zoología (QCAZ) of
the Pontificia Universidad Católica del Ecuador and are available
through their web platform Bioweb Ecuador (https://bioweb.
bio).
Because variability exists between acoustic intensities, lower
intensity harmonics were not always visible in the spectrogram for
every note. To describe these instances, we used the terminology
outlined in Costa and Toledo (2013) of “visible harmonics” to
identify the harmonics with sufficient intensity to visibly register
in the spectrogram, and “nonvisible harmonics” for those with too
low of an intensity to appear in the spectrogram (Fig. 2). We used
only harmonics visibly differentiated by spectral analysis in the
description of acoustic parameters.
Statistical Analyses.—We recorded temperatures using a
HOBO Pendant© Temperature Data Logger (UA-001-64) at a
sampling rate of 15 minutes located 1.5 m above ground in the
table 1. Average amplitude, frequencies, and duration measurements ± one standard deviation.
Parameter Average
Amplitude (u), simple call 178993.890 ± 568780.748
Amplitude (u), compound call note-1 7864.804 ± 3597.313
Amplitude (u), compound call note-2 8563.568 ± 4475.707
Fundamental and dominant frequency (Hz), simple call 2230.416 ± 195.179
Fundamental and dominant frequency (Hz), compound call note-1 2232.159 ± 109.583
Fundamental and dominant frequency (Hz), compound call note-2 2235.495 ± 106.602
Call duration (s) simple note 0.181 ± 0.038
Call duration (s) compound call 1.025 ± 0.101
Note duration (s) simple call 0.181 ± 0.038
Note duration (s) compound call, note-1 0.202 ± 0.033
Note duration (s) compound call, note-2 0.173 ± 0.030
Inter-call interval (s) 9.090 ± 2.990
Inter-note interval (s) compound call 0.651 ± 0.082
Call rate (call/min) 8.147 ± 1.498
Fig. 2. Spectrogram of a typical Pristimantis festae call illustrating visual harmonics, the dominant and fundamental frequency, and the range
of nonvisual harmonics. With P. festae, the dominant frequency is always the same as the fundamental frequency (Kok and Kalamandeen
2008; Costa and Toledo 2013).

Herpetological Review 50(3), 2019
ARTICLES 481
recording site. Analyses were conducted using R software (R Core
Team 2015). We used linear regression to calculate the possible
relationships between temperatures and call characteristics.
results
We recorded both simple and compound advertisement
vocalizations for P. festae. All calling individuals were recorded
during the day between 1114 h and 1626 h in primary forest un-
der fallen logs, leaf piles, and collections of general detritus in
shaded to well-lit primary forest, and within 20 m of a flowing
stream. Of the 20 individuals recorded, we analyzed 11 resulting
in a total of 186 notes. The values of each individual’s call were
averaged together then averaged with the values of the other 10
individuals. The nine individuals not analyzed were omitted due
to call-overs from other individuals or ambient distortions lead-
ing to poor-quality recordings. Only advertisement calls were
registered. Surveys were also conducted after sunset (1830 h)
however no calls were heard.
Calls may be composed of one to several notes, with the note
being the smallest contained unit of the call. The vocalizations
are considered simple when formed by a single note, and com-
pound when formed by two or more distinct notes (Kok and Ka-
lamandeen 2008). Of the 11 individuals analyzed, five performed
compound calls consisting of two notes, all of which vocalized at
least one simple call at some point during the recording session,
while the remaining six performed exclusively simple calls. The
simple advertisement call is a single high-pitched whistle with
a mean call and note duration of 0.181 ± 0.038 s and comprised
66.2% of the total calls recorded. While the compound call con-
sists of two high-pitched whistles with a mean call duration of
1.025 ± 0.101 s, and a mean inter-note interval of 0.651 ± 0.082
s. The first note of the compound call has a mean duration of
0.202 ± .033 s, and the second note has a mean duration of 0.173
± 0.030 s. Compound calls comprised 33.8% of all recorded calls.
The simple and compound calls have a mean inter-call interval
of 9.090 ± 2.990 s, and a mean call rate of 8.147 ± 1.498 calls per
minute (Table 1).
Although the majority of calls were uniform, we encoun-
tered one individual that vocalized a unique call. In addition to
the standard whistle, one to two short auxiliary notes were often
added immediately after the main note (Fig. 3). These auxiliary
notes had a mean duration of 0.008 s, and a mean inter-note in-
terval of 0.004 s with no difference in frequency from the main
note. This individual was collected and then stored in the Mu-
seum of Zoology (QCAZ) at Pontificia Universidad Católica del
Ecuador, reference number QCAZ-A 62034.
During the analysis we identified eight distinct harmonics,
however none of the 186 notes contained all eight visual har-
monics at once (Fig. 2). The most common pattern was three
to four visual harmonics at 66.14%, while 24.87% had five to
six harmonics, and 8.99% had two. In every note, the first har-
monic had both the lowest frequency and the highest intensity
and therefore forms the fundamental and dominant frequency.
table 2. Note duration (s) and frequency harmonics (Hz) followed by one standard deviation of the simple call, and notes 1 and
2 of the compound call.
Simple call Compound call, note 1 Compound call, note 2
Note duration (s) 0.181 ± 0.038 0.202 ± 0.033 0.173 ± 0.030
Harmonic (Hz) - 1 2230.416 ± 195.416 2232.159 ± 109.583 2235.495 ± 106.602
2 4300.932 ± 230.250 4405.335 ± 220.525 4437.537 ± 220.724
3 6148.740 ± 343.842 6370.324 ± 226.512 6433.227 ± 181.588
4 6977.910 ± 73.612 6976.358 ± 40.711 7008.166 ± 66.536
5 8189.713 ± 279.887 8221.0714 ± 0.000 8674.814 ± 0.000
6 10151.914 ± 594.674 10099.100 ± 0.000 9873.000 ± 0.000
7 13055.870 ± 776.393 12031.650 ± 0.000 11784.057 ± 0.000
8 15027.475 ± 0.000 14899.167 ± 0.000 14747.157 ± 0.000
Fig. 3. Oscillogram (top) and spectrogram (bottom) of the standard
compound call (A), simple call (B), and simple call with auxiliary
trailing note (C). The auxiliary note only occurred in one individual
(QCAZ-A 62034).

Herpetological Review 50(3), 2019
482 ARTICLES
The average fundamental and dominant frequency (harmonic 1)
of the simple call was 2230.416 ± 195.416 Hz, and harmonic 1
of the first and second notes of the compound call had a mean
frequency of 2232.159 ± 109.583 Hz and 2235.495 ± 106.602 Hz,
respectively (Table 2).
When vocalization recordings were taken, the lowest temper-
ature registered was 11.53°C and the highest was 15.09°C with
an average of 13.23 ± 1.24°C. Call rate (calls/minute) showed a
significant positive correlation with air temperature (P = 0.02).
Other call characteristics such as call duration (P = 0.22), inter-
call interval (P = 0.25), dominant/fundamental frequency of the
single call, and compound call note 1 and note 2 (P = 0.76, 0.76,
and 0.75, respectively) showed no significant correlation with air
temperature.
discussion
The call frequencies and durations of P. festae are fairly uni-
form and predictable between individuals. However, certain ex-
ceptions occur. The majority of calls consisted of a single note,
but a double note call was not uncommon, as it comprised ap-
proximately 1/3 of all calls. With respect to duration, the single
call was most similar to the second note of the compound call,
however the mean harmonic 1 frequencies for all three types of
notes fell within 5.079 Hz of each other. Harmonics 2–8 of the
simple and compound notes demonstrate frequency similarities
as well, with harmonic 7 showing the largest variation between
notes.
It is possible the simple, compound, and auxiliary note calls
have a behavioral context that was not observed in this study.
Wagner (1989) demonstrated that the duration and number of
pulses per call of Acris crepitans changed significantly in relation
to the proximity and intensity of the nearest calling neighbor,
while Gerhardt (1991) showed dramatic alteration of a male’s
call as a female approached. This last behavior has also been ob-
served in Pristimantis unistrigatus, another Ecuadorian Andean
species, in the presence of other males (Merino-Viteri, unpubl.
data). Temperature, humidity, and other environmental factors
have also been shown to cause alterations in call structure and
duration (Costa and Toledo 2013). We recommend that future
studies be conducted to discern the behavioral and environ-
mental influence on call structure for this species.
Temperature effects on note duration have been well
documented in other species (Lingnau and Bastos 2007);
however, only call rate showed significant correlation during
this study. This is to be expected, as there was only a difference
of 3.6°C between the warmest and coolest recording period.
More observations should be conducted with a larger sample
size and a wider range of temperatures to better determine any
significant correlations.
All calls of P. festae were recorded during the day in both shad-
ed and well-lit areas. Call observations were also documented,
but not recorded, from individuals calling in the páramo from
clump grass during the day, and never at night. It is possible that
significant shade and humidity might mimic conditions required
for nocturnal activity and prompt diurnal calling, but as the
Páramo lies above the tree line, recordings were taken at lower
elevations in well-lit areas, and recordings were attempted from
1830 to 2200 h with no success, this does not appear to be the
case for P. festae. Therefore, P. festae is most likely a diurnal spe-
cies. Although diurnal species of Pristimantis are not unheard of,
the majority of species of this genus are nocturnal (Lynch and
Duellman 1997; Arroyo et al. 2008). Additional attempts to record
calls should be conducted after sunset throughout the lunar cy-
cle to verify this observation.
There are three close relatives to P. festae: P. ocreatus, P. phyr-
romerus, and P. leoni (Pinto-Sánchez et al. 2012; Padial et al. 2014;
Yánez-Muñoz et al. 2014). Pristimantis leoni was described in
Lynch and Duellman (1997) as having a distinct “tink” call; how-
ever, only the call of P. phyrromerus has been spectrographically
analyzed (Guayasamin 2000). Pristimantis phyrromerus has a dis-
tinctly different call from P. festae; the average call duration lasts
0.207 ± 0.129 s and contains 1–8 notes, each with a mean duration
of 0.032 ± 0.007 s and a mean inter-note interval of 0.035 ± 0.031
s. The dominant and fundamental frequencies of P. phyrromerus
are also separate with the mean fundamental frequency register-
ing 82.5 ± 28.831 Hz, and the dominant at a much higher 2830 ±
117.501 Hz. It is interesting to note that P. phyrromerus was fre-
quently recorded during the day. This may indicate further diurnal
tendencies in other closely related members of this group. Addi-
tional testing and observation is recommended.
The single high-pitched whistle of the simple call of P. festae
sounds similar to the call of Hyloxalus jacobuspetersi (Dendrobati-
dae), a sympatric species. However, H. jacobuspetersi has a slightly
longer duration at 0.23–0.31 s, with a lower fundamental frequen-
cy between 1300 and 1500 Hz, and higher dominant frequency
between 2900 and 3400 Hz (Coloma 1995). These measurements
were taken from two individuals in Pichincha and Bolívar Prov-
inces.
Acknowledgments.—We thank the Galo Plaza Lasso Foundation,
the Hacienda Zuleta, T. Luxner, Y. Potaufeu, X. Pazmiño, and S. Ron for
their assistance and advice with this project. Santiago Ron provided
advice on call structure analyses. Specimens were collected under
permit 009-2015-FAU-DPAP-MA issued by Ministerio del Ambiente
del Ecuador.
literature cited
arroyo, s. b., v. h. serrano-cardozo, and M. P. rAMírez-PiniLLA. 2008. Diet,
microhabitat and time of activity in a Pristimantis (Anura, Strabo-
mantidae) assemblage. Phyllomedusa: J. Herpetol. 7:109–119.
bahaMondez, c. c., t. csoka, P. drichi, P. FiliPchuk, a. de Jong, and b. h. J.
o. ÁLvArez. 2010. Global forest resources assessment 2010 main re-
port. Food Agr. Org. United Nations.
bustaMante, M. r., s. r. ron., and l. a. coloMa. 2005. Cambios en la di-
versidad en diete comunidades de anuros en los Andes de Ecuador.
Biotropica 37:180–189.
buytaert, W., r. célleri, b. de bièvre, F. cisneros, g. Wyseure, J. deckers,
and r. hoFstede. 2006. Human impact on the hydrology of the An-
dean páramos. Earth-Sci. Rev. 79:53–72.
byrne, P. g. 2009. Strategic male calling behavior in an Australian ter-
restrial toadlet (Pseudophryne bibronii). Copeia 2009:57–63.
cabarle, b., M. cresPi, c. dodson, c. luzuriaga, d. rose, and J. shores.
1989. An assessment of biological diversity and tropical forests for
Ecuador. Draft report for USAID/Quito. World Resources Institute,
Washington, DC.
coloMa, l. a. 1995. Ecuadorian frogs of the genus Colostethus (An-
ura: Dendrobatidae). Univ. Kansas Nat. Hist. Mus. Misc. Publ. No.
87:1–72.
———, s. r. ron, d. ALMeidA, And M. yÁnez-Muñoz. 2004. Pristimantis
festae. The IUCN Red List of Threatened Species. Version 2015.2.
<www.iucnredlist.org>. Downloaded on 23 August 2015.
costa, t. r., and l. F. toledo. 2013. Physalaemus spiniger (Anura: Lei-
uperinae): a frog with an extensive vocal repertoire. J. Herpetol.
47:530–538.

Herpetological Review 50(3), 2019
ARTICLES 483
cusi, J. c., a. c. barboza, v. vredenburg, and r. von May. 2015. A new
locality, range extension and record of Batrachochytrium dendro-
batidis in the endangered terrestrial breeding frog Pristimantis ka-
toptroides Flores, 1988 (Anura: Craugastoridae) in Peru. Check List
11:1608.
duellMan, W. e., and e. lehr. 2009. Terrestrial-breeding frogs (Strabo-
mantidae) in Peru. Natur und Tier Verlag, Münster, Germany. 384
pp.
Frost, d. r. 2019. Amphibian Species of the World: An Online Refer-
ence. Version 6.0, accessed 13 March 2019. Electronic database
accessible at http://research.amnh.org/herpetology/amphibia/in-
dex.html. American Museum of Natural History, New York.
gerhardt, h. c. 1991. Female mate choice in treefrogs: static and dy-
namic acoustic criteria. Anim. Behav. 42:615–635.
guAyAsAMín-ernsT, J. M. 2000. Partición acústica en una comunidad de
ranas del género Eleutherodactylus (Anura: Leptodactylidae) en un
bosque nublado del occidente del Ecuador. Licenciatura disserta-
tion. Pontificia Universidad Católica Del Ecuador.
hedberg, o., 1964. Features of Afroalpine plant ecology. Acta Phyto-
geographica Suecica 49:1–144.
hedges, s. b., W. e. duellMan, and M. P. heinicke. 2008. New World direct-
developing frogs (Anura: Terrarana): molecular phylogeny, classifi-
cation, biogeography, and conservation. Zootaxa 1737:1–182.
heinicke, M. P., W. e. duellMan, and s. b. hedges. 2007. Major Caribbean
and Central American frog faunas originated by oceanic dispersal.
Proc. Natl. Acad. Sci. 104:10092–10097.
kok, P. J., and M. kalaMandeen. 2008. Introduction to the taxonomy of
the amphibians of Kaieteur National Park, Guyana. Belgian Devel-
opment Cooperation.
lingnau, r., and r. P. bastos. 2007. Vocalizations of the Brazilian tor-
rent frog Hylodes heyeri (Anura: Hylodidae): repertoire and influ-
ence of air temperature on advertisement call variation. J. Nat Hist.
41:1227–1235.
liPs, k. r., J. diFFendorFer, J. r. Mendelson, and M. W. sears. 2008. Rid-
ing the wave: reconciling the roles of disease and climate change in
amphibian declines. PLoS Biol. 6(3): e72.
littleJohn, M. J. 1977. Long-range acoustic communication in an-
urans: an integrated and evolutionary approach. In D. H. Taylor and
S. I. Guttman (eds.), The Reproductive Biology of Amphibians, pp.
263–294. Springer Science, New York.
lynch, J. d., and W. e. duellMan. 1980. The Eleutherodactylus of the Am-
azonian slopes of the Ecuadorian Andes (Anura: Leptodactylidae).
Univ. Kansas Mus. Nat. Hist. Misc. Publ. No. 69:1–86.
———, and W. e. duellMan. 1997. Frogs of the genus Eleutherodacty-
lus (Leptodactylidae) in western Ecuador: systematics, ecology and
biogeography. Univ. Kansas Mus. Nat. Hist. Spec.l Publ. No. 23.
Mosandl, r., s. günter, b. stiMM, an d M. Weber. 2008. Ecuador suf-
fers the highest deforestation rate in South America. In E. Beck,
J. Bendix, I. Kottke, F. Makeschin, and R. Mosandl (eds.), Gradi-
ents in a Tropical Mountain Ecosystem of Ecuador, pp. 37–40.
Springer, Germany.
narvaez, d. 2015. Determinación de la infección de Batrachochytrium
dendrobatidis en el Cutín de Quito (Pristimantis unistrigatus) y su
relación con la infección de renacuajos de la Rana Marsupial de
Quito (Gastrotheca riobambae) en el Parque Metropolitano Guan-
guiltagua de Quito. Licenciatura dissertation, Pontificia Universi-
dad Católica Del Ecuador.
Padial, J. M., t. grant, and d. r. Frost. 2014. Molecular systematics of
terraranas (Anura: Brachycephaloidea) with an assessment of the
effects of alignment and optimality criteria. Zootaxa 3825:1–132.
PinTo-sÁnCHez, n. r., r. ibAñez, s. MAdriñAn, o. i. sAnJur, e. berMinghaM,
and a. J. craWFord. 2012. The great American biotic interchange in
frogs: multiple and early colonization of Central America by the
South American genus Pristimantis (Anura: Craugastoridae). Mol.
Phylogenet. Evol. 62:954–972.
Pounds, J. a., M. r. bustaMante, l. a. coloMa, J. a. consuegra, M. P.
Fogden, P. n. Foster, e. la Marca, k. l. Masters, a. Merino-viteri, r.
PuschendorF, and s. r. ron. 2006. Widespread amphibian extinc-
tions from epidemic disease driven by global warming. Nature
439:161–167.
ron, s. r., J. guayasaMin, and P. Menéndez-guerrero. 2011. Biodiversity
and conservation status of Ecuadorian amphibians. In H. Heat-
wole, C. L. Barrio-Amoros, and H. W. Wilkinson (eds.), Amphibian
Biology, pp. 129–170, Volume 9, Part 2. Surrey Beatty & Soons PTY
Limited, Australia.
sarMiento, g. 1986. Ecologically crucial features of climate in high
tropical mountains. In F. Vuilleumier and M. Monasterio (eds.),
High Altitude Tropical Biogeography, pp. 11–45. Oxford University
Press, Oxford.
tobias, M. l., s. s. visWanathan, and d. b. kelley. 1998. Rapping, a fe-
male receptive call, initiates male–female duets in the South Afri-
can clawed frog. Proc. Natl. Acad. Sci. 95:1870–1875.
de toledo, l. F., c. Fernando, and b. haddad. 2009. Defensive vocaliza-
tions of Neotropical anurans. South Am. J. Herpetol. 4:25–42.
Wagner, W. e. 1989. Social correlates of variation in male calling
behavior in Blanchard’s cricket frog, Acris crepitans blanchardi.
Ethology 82:27–45.
Wells, k. d. 1977. The social behaviour of anuran amphibians. Anim.
Behav. 25:666–693.
———, and J. J. schWartz. 2006. The behavioral ecology of anuran
communication. In P. Narins, A. S. Feng, and R. R. Fay (eds.), Hear-
ing and Sound Communication in Amphibians, pp. 44–86. Spring-
er, New York.
yÁnez-Muñoz, M. H., C. FrenkeL, J. M. guAyAsAMín, A. vAreLA-JArAMiLLo,
and s. r. ron. 2014. Pristimantis festae. In S. R. Ron, J. M. Guayasa-
min, M. H. Yanez-Muñoz, A. Merino-Viteri, D. A. Ortiz, and D. A.
Nicolalde. 2016. AmphibiaWebEcuador. Version 2016.0. Museo de
Zoología, Pontificia Universidad Católica del Ecuador. <http://
zoologia.puce.edu.ec/vertebrados/anfibios/FichaEspecie.
aspx?Id=3419>, accessed 31 January 2016.