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Introduction
The Amazonian lowlands of Loreto region in northern
Peru represent one of the most biodiverse areas on
the planet along with neighbouring regions in eastern
Ecuador and southern Colombia (Bass et al., 2010;
Jenkins et al., 2013). Pitman et al. (2013) reported
218 species of amphibians throughout Loreto, and
this number has increased with the addition of newly
described taxa and new geographic records (e.g.,
Ortega-Andrade et al., 2015; Ron et al., 2016).
Allpahuayo-Mishana National Reserve is one of
the smallest protected areas (58,069.9 ha) in Loreto
(SERNANP, 2017). Yet, 83 amphibian and 120 reptile
species are reported in the area (Rivera and Soini, 2002;
Rivera-Gonzáles et al., 2003). Some amphibian and
bird species seem to be restricted to white-sand forests,
a rare Amazonian phytophysiognomy that exists within
the reserve (Álvarez et al., 2013; Rojas et al., 2015).
Allpahuayo-Mishana is the only protected area around
the growing city of Iquitos (the urban area of the city
is only 25 km distant), and plays an important role in
preventing urban and agricultural expansion, as well
in preserving and raising awareness about the local
biodiversity.
Previous herpetological research conducted in
Allpahuayo-Mishana resulted in notable records of
rare species such as Rhinella ceratophrys, Nyctimantis
rugiceps and Hemiphractus scutatus (Rivera and Soini,
2002; Rivera-Gonzáles et al., 2006). Here, we report
for the first time the presence of Gastrotheca longipes
(Boulenger, 1882), Cochranella resplendens (Lynch
and Duellman, 1973) and Teratohyla midas (Lynch
and Duellman, 1973) in the reserve. Additionally,
we provide natural history information based on new
observations and from the literature, and we update the
distribution ranges of these three Amazonian species.
Materials and Methods
We conducted visual encounter surveys (Crump,
1994) in the Allpahuayo-Mishana National Reserve
Herpetology Notes, volume 12: 461-472 (2019) (published online on 13 May 2019)
First records of Gastrotheca longipes (Boulenger, 1882),
Cochranella resplendens (Lynch and Duellman, 1973) and
Teratohyla midas (Lynch and Duellman, 1973) for the
Allpahuayo-Mishana National Reserve, Peru, with comments
on their distribution in the Amazon basin
Omar Rojas-Padilla1,2,3,*, Ehiko J. Rios-Alva1,4, and Giussepe Gagliardi-Urrutia1,3
1 Programa de Investigación en Biodiversidad Amazónica,
Instituto de Investigaciones de la Amazonía Peruana, Av.
Quiñones km 2.5, Iquitos, Loreto, Peru.
2 Tropical Herpetology Laboratory, Departamento de Ciências
Biológicas, Universidade Estadual de Santa Cruz, Rodovia
Jorge Amado, km 16, Ilhéus, Bahia 45662-900, Brazil.
3 Laboratório de Sistemática de Vertebrados, Pontifícia
Universidade Católica do Rio Grande do Sul, Av. Ipiranga,
6681, Porto Alegre, Rio Grande do Sul 90619-900, Brazil.
4 Instituto de Biologia, Universidade Federal da Bahia, Campus
de Ondina, Salvador, Bahia 40170-290, Brazil.
* Corresponding author. E-mail: projasomar@gmail.com
Abstract. We report the first records of Gastrotheca longipes, Cochranella resplendens and Teratohyla midas in the
Allpahuayo-Mishana National Reserve, Loreto region, Peru. We update the distribution maps of these three species within the
Amazon basin, provide information about their natural history, and describe puffing-up body and mouth gapping behaviours
in Gastrotheca longipes.
Keywords. Anura, Centrolenidae, distribution, Hemiphractidae, Iquitos, Peruvian Amazon
Omar Rojas-Padilla et al.
462
(Fig. 1) between 2013 to 2018. Voucher specimens
were collected using approved protocols under
permit (RJN°002-2018-SERNANP-RNAM-JEF)
and deposited in the Coleção de Anfíbios do Museu
de Ciências e Tecnologia da Pontifícia Universidade
Católica do Rio Grande do Sul (MCP), Brazil, and in
the Colección Referencial de Biodiversidad del Instituto
de Investigaciones de la Amazonía (CRBIIAP), Peru.
We photographed and measured snout-vent length
(SVL) of captured frogs when possible. We geolocated
capture points with a GPS Garmin 64s. We reviewed
records published in peer reviewed journals and books,
and projected their geographical coordinates on a map
to confirm their location. We estimated elevations
with Google Earth Pro™ 7.3.0.3832 (Google Inc.).
We generated the updated distribution map in QGIS
Desktop 2.18.9 (QGIS Development Team 2017).
Species identities were confirmed by comparison with
the original descriptions and other pertinent literature,
and with the aid of specialists in Centrolenids and
Hemiphractids (see Acknowledgments).
Results
Gastrotheca longipes (Fig. 2, Table 1).—Specimens
captured in Allpahuayo-Mishana match diagnostic
characteristics noted by Boulenger (1882), Almendáriz
and Cisneros-Heredia (2005), and Duellman (2015):
skin of skull smooth not ossified, tympanic ring
granular, dorsal skin green and that of venter cream,
throat and chest yellow, upper lip white, lower lip green,
white spot present under the eye and posteriorly to jaw,
iris white with brown halftones, bones green, outer edge
of heel brown to the tip of the outer toe. One juvenile
individual had white spots on dorsum and flanks (where
they were more numerous), cream yellow upper lips,
white dermal folds on arms and legs, a brown stripe
with white dots on dorsal surface of fingers, a single
white dot on ventral surface of fingers, throat and chest
yellow cream, belly green with creamy yellow spots;
discs on fingers green; toes IV – V brown. We observed
closed dorsal pouches in a female individual.
We captured three males and one female near forest
streams heavily influenced by seasonal rains (i.e.,
where stream depth exceeded 1.5 meters during the
peak of the rainy season). We found the first male
Figure 1. Geographic distribution of Cochranella resplendens (blue circles), Teratohyla midas (yellow circles) and Gastrotheca
longipes (green circles). The star represents the new records of these species in Allpahuayo-Mishana National Reserve, in Loreto,
Peru. Inset: Location of records within the reserve, most of them between “Paujil” and “Allpahuayo” creeks.
(unvouchered, SVL: 77.3 mm) on 4 May 2013 at 17:35
h. At the time of capture, this male appeared to assume
a defence position (appearing “swollen”) and issued a
distress call which we did not record. While we were
taking photographs, the individual opened and closed
his mouth constantly (Fig. 2A–B). We found a second
male (SVL: 76.1 mm, not photographed) on 25 August
2014 at 18:30 h. We found a juvenile (CRBIIAP 1982,
First records of frog species for the Allpahuayo-Mishana National Reserve, Peru 463
Figure 2. Gastrotheca longipes found at Allpahuayo-Mishana National Reserve. (A–B) an unvouchered adult male (SVL: 77.3
mm). (C–D) juvenile (CRBIIAP 1982, SVL: 32.88 mm). (E–F) a female bearing eggs on dorsal pouch (MCP 13954). Photos by
G. Gagliardi-Urrutia.
SVL: 32.88 mm; Fig. 2C–D) perched on a leaf at 0.40 m
height at the margin of the same stream on 4 June 2018.
Finally, on 10 June 2018, we found a female with four
eggs inside the pouch (MCP 13954, Fig. 2E–F) perched
on a branch at 0.80 m near a stream.
Cochranella resplendens (Fig. 3, Table 2).—
Specimens captured and photographed match the
diagnostic characteristics provided by Lynch and
Duellman (1973): snout round in dorsal view and
sloping in lateral view, dorsal colouration dark green
with scattered white spots, dermal folds present on the
outer edge of hand, arm, foot, tarsus and around the heel,
anal fold u-shaped, parietal and visceral peritoneum
white, humeral spine absent, heart not visible through
skin in life.
We captured three individuals, two of which were
found along a forest stream and a third near a small
temporary pond fed by stream water. We found an adult
male (unvouchered, SVL: 27.7 mm; Fig. 3A–B) on 16
March 2015 at 14:15 h perched on a branch 1.4 m above
the ground. The vegetation of the area was composed
of large trees (canopy reaching 15–25 meters), lianas
and shrub vegetation on white sandy-clay soil. We
found another male (MCP 13953, SVL: 23.48 mm; Fig.
3C–D) and a female with eggs (CRBIIAP 1969, SVL:
25.89 mm) perched on a leaf 0.5 m from the ground on
13 March 2018 at 23:00 h.
Omar Rojas-Padilla et al.
464
Table 1. Records of Gastrotheca longipes in the Amazon basin. Geographical coordinates Datum
WGS84.
Locality Country Latitude Longitude Altitude Source
Rutuno River, Pastaza Province Ecuador -1.916 -77.250 446 Goin (1964)
Sunkuyacu River, Orellana Province Ecuador -0.694 -76.670 315
Almendáriz and
Cisneros-Heredia
(2005)
Tiputini Biological Station, Orellana
Province Ecuador -0.791 -77.527 838
Almendáriz and
Cisneros-Heredia
(2005)
Canelos, Pastaza Province Ecuador -1.587 -77.734 453
Almendáriz and
Cisneros-Heredia
(2005)
Chigkan Entse, Cenepa River,
Amazonas region Peru -4.466 -78.166 662
Almendáriz and
Cisneros-Heredia
(2005)
near Caterpiza, Caterpiza River,
Amazonas region Peru -3.916 -77.716 188
Almendáriz and
Cisneros-Heredia
(2005)
Chichirota, Pastaza Province Ecuador -1.166 -77.216 422 Duellman et al.
(2006)
Pongo Chimin, Datem del Marañón
Province, Loreto region Peru -3.112 -77.776 384 Catenazzi and
Venegas (2011)
Barranca, upper Marañón River,
Loreto region Peru -4.832 -76.697 129 Duellman (2015)
"José Álvarez Alonso" Biological
Station, Allpahuayo-Mishana National
Reserve, Loreto
Peru -3.952 -73.432 130 This report
"José Álvarez Alonso" Biological
Station, Allpahuayo-Mishana National
Reserve, Loreto
Peru -3.954 -73.417 140 This report
"José Álvarez Alonso" Biological
Station, Allpahuayo-Mishana National
Reserve, Loreto
Peru -3.952 -73.431 125 This report
Table 1. Records of Gastrotheca longipes in the Amazon basin. Geographical coordinates Datum WGS84.
Teratohyla midas (Fig. 4, Table 3).—Diagnostics
characteristics of captured specimens matched the
description provided by Lynch and Duellman (1973):
snout truncate in dorsal and lateral view, iris silvery
bronze with black reticulations, chest white, skin on
venter coarsely areolate, dorsal skin shagreened without
warts or spicules, dorsal colouration green with yellow
spots, parietal peritoneum white, visceral peritoneum
white, heart not visible through skin, arms and legs
lacking dermal folds, hands and feet dull greenish
yellow, humeral spine absent in males, bones green.
We found about 10 individuals during surveys. On
4 May 2013, we found an adult (unvouchered, Fig.
4A–B) on a branch 0.5 m above the ground. On 4 June
2017, we heard two males calling, and captured one
(CRBIIAP 2099, SVL: 17.9 mm; Fig. 4C–D) on a leaf
at 1.80 m above the stream. We also photographed an
adult male in calling activity (Fig. 4E) and an egg clutch
(Fig. 4F) with 13 tadpoles at developmental stage 17–19
(Gosner, 1960) on the same day. On 02 February 2018,
we captured three adults (MCP 13950, SVL: 17.4 m;
MCP 13951, SVL: 16.9, CRBIIAP 2101, SVL: 20.3
mm).
Discussion
Gastrotheca longipes was previously known to occur
from 250 to 1,020 m a.s.l. in Amazonian Ecuador
and Peru (Almendáriz and Cisneros-Heredia, 2005;
Duellman et al., 2006; Catenazzi and Venegas, 2012;
Duellman, 2015). Our records in Allpahuayo-Mishana
National Reserve extend the lower boundary of the
species’ elevational range to 125 m a.s.l. Our records
also stretch the species’ geographical range 508 km
eastward, and adds a third known locality for the
species in Loreto. Gastrotheca longipes might be
First records of frog species for the Allpahuayo-Mishana National Reserve, Peru 465
Figure 3. Cochranella resplendens found in Allpahuayo-Mishana National Reserve. (A–B) an unvouchered adult specimen
(SVL: 27.7 mm). (C–D) an adult male (MCP 13953, SVL: 23.48 mm). Note intraspecific variation on dermal folds on legs and
arms, and in colouration of hands and feet. Photos by G. Gagliardi-Urrutia.
distributed throughout the Amazon basin (Blackburn
and Duellman, 2013), but records are very rare because
this marsupial frog inhabits the forest canopy and is
rarely observed in the forest understory (Almendáriz
and Cisneros-Heredia, 2005; Guayasamin et al., 2006).
The distress behaviour of the male we captured and
photographed has been termed “puffing-up body” and
“mouth gapping” (Toledo et al., 2011), and has been
observed in others Hemiphractids species (Lourenço-
de-Moraes et al., 2016). Our observation constitutes the
first report of such behaviours in G. longipes.
Cochranella resplendens was known from 11
localities in the Andean and lowland Amazon forests of
Peru, Ecuador and Colombia, with an elevational range
from 190 to 1,699 m a.s.l. (Lynch and Duellman, 1973;
Cisneros-Heredia and McDiarmid, 2005; Cisneros-
Heredia and Meza-Ramos, 2007; Torres-Gastello et al.,
2007; Terán-Valdez et al., 2009; Malambo et al., 2013;
Twomey et al., 2014; Chávez and Mueses-Cisneros,
2016; Molina-Zuluaga et al., 2017). Our record extends
the species’ known distribution 345 km southwest and
represents the third geographic record of the species
for Peru, the second for the Loreto region and the first
inside a protected area. Previous records have been
made in areas close to streams within primary forests
and mature secondary forest (Chávez and Mueses-
Cisneros, 2016), which are similar in structure to those
where we found our individuals. One of the specimens
found during surveys, had small and scattered spots,
small dermal folds on legs and arms, and yellow hands
Omar Rojas-Padilla et al.
466
Table 2. Records of Cochranella resplendens in the Amazon basin. Geographical coordinates Datum
WGS84.
Locality Country Latitude Longitude Altitude Source
Santa Cecilia, Sucumbios Province Ecuador -0.080 -76.990 339 Lynch and Duellman
(1973)
Pozo Garza, Oryx, Pastaza Province Ecuador -1.433 -77.05 312 Cisneros-Heredia and
McDiarmid (2005)
Tiputini Biological Station, Orellana
Province Ecuador -0.616 -76.166 257 Cisneros-Heredia and
McDiarmid (2005)
Viejo de Sumaco, Orellana Province Ecuador -0.533 -77.416 948 Cisneros-Heredia and
Meza-Ramos (2007)
Tiputini Biological Station, Orellana
Province Ecuador -0.791 -77.527 300 Cisneros-Heredia and
Meza-Ramos (2007)
Napinaza River, Morona Santiago
Province Ecuador -2.926 -78.406 1100 Terán-Valdez et al. (2009)
Microcuenca La Resaca, Municipality of
Belén de Los Andaquíes, Caquetá
departament
Colombia 1.439 -75.890 482 Malambo et al. (2013)
Stream near the village of San Jose in the
Cainarachi valley near Tarapoto, San
Martín region
Peru -0.642 -76.291 518 Twomey et al. (2014)
Quebrada Bufeo, Putumayo Province,
Loreto region Peru -2.330 -71.607 124 Chávez and Mueses-
Cisneros (2016)
Finca El Chaquiral, vereda El Retiro,
Municipality de Anorí, Antioquia region Colombia 6.988 -75.130 1699 Molina-Zuluaga et al.
(2017)
El Eden, vereda San Antonio,
Municipality de Alejandría, Antioquia
region
Colombia 6.367 -75.027 1309 Molina-Zuluaga et al.
(2017)
"José Álvarez Alonso" Biological Station,
Allpahuayo-Mishana National Reserve,
Loreto
Peru -3.966 -73.418 129 This report
"José Álvarez Alonso" Biological Station,
Allpahuayo-Mishana National Reserve,
Loreto
Peru -3.965 -73.431 131 This report
Table 2. Records of Cochranella resplendens in the Amazon basin. Geographical coordinates Datum WGS84.
and feet. Based on available publications, this pattern is
within the range of intraspecific colour variation of the
species. Malambo et al. (2013) reported one individual
with green hands and feet, and with small and scattered
spots on dorsum. Molina-Zuluaga et al. (2017) reported
one individual with green legs and two individuals with
yellow colouration on the hands and feet, in addition
to variation in the length and width of dermal folds
on arms and legs. Combined, these reports suggest C.
resplendens to be polychromatic, and future studies
Figure 4. Teratohyla midas found in Allpahuayo-Mishana National Reserve, in Loreto, Peru. (A–B) an unvouchered adult
specimen. (C–D) male (CRBIIAP 2099, SVL: 17.9 mm). (E) an unvouchered adult male in calling activity. (F) egg clutch
containing 13 embryos at developmental stages 17-19 (Gosner, 1960). Photos A–B by E.J. Rios-Alva; C–F by G. Gagliardi-
Urrutia.
First records of frog species for the Allpahuayo-Mishana National Reserve, Peru 467
Table 3. Records of Teratohyla midas in the Amazon basin. Geographical coordinates Datum WGS84.
Locality Country Latitude Longitude Altitude Source
Santa Cecilia, Napo Province Ecuador -0.05 -76.983 339 Lynch and
Duellman (1973)
Panguana, Huánuco region Peru -9.583 -74.8 405 Toft and Duellman
(1979)
Pakitza, Madre de Dios region Peru -11.9 -71.366 345 Morales and
McDiarmid (1996)
Tiputini Biodiversity Station, Orellana
Province Ecuador -0.616 -76.166 190
Cisneros-Heredia
and McDiarmid
(2005)
Yasuní Scientific Station, Orellana
Province Ecuador -0.666 -76.400 230
Cisneros-Heredia
and McDiarmid
(2005)
Puerto Misahualli, Napo Province Ecuador -1.033 -77.666 400
Cisneros-Heredia
and McDiarmid
(2005)
Oglán River, Pastaza Province Ecuador -1.333 -77.583 600
Cisneros-Heredia
and McDiarmid
(2005)
Alto Mazan, Loreto region Peru -2.586 -74.492 134 Catenazzi and
Bustamante (2007)
Alto Nanay, Loreto region Peru -2.806 -74.825 153 Catenazzi and
Bustamante (2007)
Pisorié Setsa’cco, between Aguarico
and Pisorié rivers, Dureno Ecuador -0.001 -76.671 278 Yánez-Muñoz and
Chimbo (2007)
Totoa Nai’qui, Dureno Ecuador -0.0513 -76.796 298 Yánez-Muñoz and
Chimbo (2007)
Güeppicillo, Sucumbíos Ecuador -0.177 -75.675 225 Yánez-Muñoz and
Venegas (2008)
Crique Grand Leblond, French
Guyana
Guyana
French 4.700 -53.183 76
Kok and
Castroviejo-Fisher
(2008)
Boca do Acre, Amazonas state Brazil -9.026 -67.236 151 França and
Venâncio (2010)
Regional Conservation Area
"Maijuna", Las Piedras river, Loreto
region
Peru -2.792 -72.917 163 von May and
Venegas (2010)
Choro, Yaguas National Park,
Putumayo Province, Loreto region Peru -2.610 -71.485 160
von May and
Mueses-Cisneros
(2011)
Pongo Chinim, Datem del Marañón
Province, Loreto region Peru -3.113 -77.776 385 Catenazzi and
Venegas (2012)
Quebrada Kampankis, Condorcanqui
Province, Amazonas region, Peru -4.043 -77.541 1336 Catenazzi and
Venegas (2012)
Municipality of Solita, Caquetá
departament Colombia 0.883 -75.616 219 Osorno et al.
(2011)
Mâncio Lima: Serra do Divisor
National Park: Igarapé Ramon Brazil -7.450 -73.766 276 Melo-Sampaio and
de Oliveira (2013)
Municipality of Sao Pedro da Água
Branca Brazil -5.085 -48.429 159 Pontes and Mattedi
(2013)
Municipality of Porto Velho, Vista
Alegre do Abuna, Rondônia state Brazil -9.576 -65.570 149 Melo-Sampaio and
de Oliveira (2013)
Locality
Country
Latitude
Longitude
Altitude
Source
Omar Rojas-Padilla et al.
468
Table 3. Continued.
Locality Country Latitude Longitude Altitude Source
Sucre, Municipality de Florencia Colombia 1.781 -75.651 950 Malambo et al.
(2013)
El corregimiento de Santo Domingo,
Municipality de Florencia Colombia 1.558 -75.668 295 Malambo et al.
(2013)
En la microcuenca La Resaca,
Municipality de Belén de los
Andaquíes
Colombia 1.439 -75.890 482 Malambo et al.
(2013)
San José, San Martín region Peru -6.420 -76.291 531 Twomey et al.
(2014)
Pongo de Rentema, Amazonas region Peru -5.295 -78.406 556 Twomey et al.
(2014)
Alto Cachiyacu, Loreto region Peru -5.516 -76.717 216 Venegas et al.
(2014)
"Sierra del Divisor" National Park,
Contamana Province, Loreto region Peru -7.204 -73.882 274 Melo-Sampaio and
de Souza (2015)
Quebrada Bufeo, Putumayo Province,
Loreto region Peru -2.330 -71.607 124
Chávez and
Mueses-Cisneros
(2016)
Puesto de Control y Vigilancia, La
Novia River, Ucayali region Peru -9.9882 -70.7081 260 Padial et al. (2016)
Sepahua River, Ucayali region Peru -11.05002 -72.45307 356 Padial et al. (2016)
3.8 km south of Puerto Breu, Ucayali
region Peru -9.566 -72.755 268 Padial et al. (2016)
Community Natural Reserve “El
Manantial”, Florencia, Caquetá
department
Colombia 1.847 -75.584 427-493 Rodríguez-Cardoso
et al. (2016)
"José Álvarez Alonso" Biological
Station, Allpahuayo-Mishana National
Reserve, Loreto
Peru -3.965 -73.431 133 This report
"José Álvarez Alonso" Biological
Station, Allpahuayo-Mishana National
Reserve, Loreto
Peru -3.937 -73.445 138 This report
"José Álvarez Alonso" Biological
Station, Allpahuayo-Mishana National
Reserve, Loreto
Peru -3.957 -73.420 123 This report
"José Álvarez Alonso" Biological
Station, Allpahuayo-Mishana National
Reserve, Loreto
Peru -3.952 -73.432 130 This report
"José Álvarez Alonso" Biological
Station, Allpahuayo-Mishana National
Reserve, Loreto
Peru -3.954 -73.433 125 This report
"José Álvarez Alonso" Biological
Station, Allpahuayo-Mishana National
Reserve, Loreto
Peru -3.951 -73.419 135 This report
"José Álvarez Alonso" Biological
Station, Allpahuayo-Mishana National
Reserve, Loreto
Peru -3.948 -73.434 131 This report
"José Álvarez Alonso" Biological
Station, Allpahuayo-Mishana National
Reserve, Loreto
Peru -3.964 -73.418 131 This report
"José Álvarez Alonso" Biological
Station, Allpahuayo-Mishana National
Reserve, Loreto
Peru -3.965 -73.4315 131 This report
First records of frog species for the Allpahuayo-Mishana National Reserve, Peru 469
should evaluated whether different colour morphotypes
are associated with particular geographic regions.
Teratohyla midas is regarded as a common species
with a broad distribution in northern South America,
altitudinally ranging from 76 to 1,336 m a.s.l. Most
geographic records were reported from Peru, Ecuador
and Colombia, with a few records in Brazil and French
Guiana (Table 3, Fig. 1). The species is likely to be
found in the Amazonian forests of Bolivia and other
localities in the Amazon basin where it has not yet been
detected. During our surveys we recorded individuals
calling and in amplexus on the riparian vegetation
along forest streams at different times of the year.
Reproductive activity increases considerably during
the rain. For example, in a survey on 04 June 2017,
we heard numerous and intense vocalizations along a
3 km-long stretch of a water stream, during and after a
rain storm. The activity continued, with lower intensity
along the following days. It seems that the species has
a gregarious behaviour during reproduction, because
many males can be found in nearby areas (Diaz-Ricarte
et al., 2016). Contrary to the report by Diaz-Ricarte et
al. (2016), we found egg clutches attached to the backs
of leaves, including palm leaves, always hanging above
water streams. We believe that the site and position of
egg clutches is not fixed reproductive trait in T. midas,
as it has been described for several other glassfrog
species (Vockenhuber et al., 2008; Delia et al., 2010;
Rojas-Morales and Escobar-Lasso, 2013).
With these three new records, the number of
amphibian species registered within the Allpahuayo-
Mishana National Reserve is increased to 86. This
protected area covers a diversity of ecosystems that
includes white-sand forests, forest growing over clay
forests and seasonally flooded forests, which have yet
to be thoroughly surveyed. Therefore, we expect further
work to reveal new records of amphibians and reptiles
in the area.
Acknowledgements. We are grateful to Andrés Costa-Galvis,
Fabrício H. Oda and anonymous reviewers for valuable
comments on the manuscript. H. Mauricio Ortega-Andrade for
the confirmation of the identifications, and Santiago Castroviejo-
Fisher for identification and comments about Cochranella
resplendens. To William E. Duellman for valuable information
about G. longipes. To José M. Padial, Pedro Ivo Simões, Pamela
Montero-Álvarez and Victor G.D. Orrico for the suggestions and
revisions on earlier versions of this manuscript. To the staff of the
“José Álvarez Alonso” Biological Station, especially to resident
investigator Freddy A. Arévalo Dávila. To Ramón Aguilar
M. for measuring specimens and for companionship during
surveys. O. Rojas-Padilla and E.J. Rios-Alva are supported by
MSc scholarships by Programa de Alianzas para la Educación
y la Capacitación de la Organización de Estados Americanos y
el Grupo Coimbra de Universidades Brasileras (PAEC OEA-
GCUB) and by Coordenação de Aperfeiçoamento de Pessoal de
Nível Superior (CAPES). G. Gagliardi-Urrutia is supported by
PhD scholarship from Conselho Nacional de Desenvolvimento
Científico e Tecnológico (CNPq) (process #140716/2016–5).
References
Almendáriz, A., Cisneros-Heredia, D.F. (2005): Nuevos datos
sobre la distribución e historia natural de Gastrotheca longipes
(Boulenger, 1882), una rana marsupial amazónica poco conocida
(Amphibia: Anura: Hylidae). Politécnica 26: 20–27.
Álvarez, J.A., Metz, M.R., Fine, P.V.A. (2013): Habitat
specialization by birds in western Amazonian White-sand
Forests. Biotropica 45: 365–372.
Bass, M., Finner, M., Jenkins, C.N., Kreft, H., Cisneros-Heredia,
D.F., McCracken, S.F., et al. (2010): Global conservation
significance of Ecuador’s Yasuní National Park. PLoS One 5:
e8767.
Blackburn, D.C., Duellman, W.E. (2013): Brazilian marsupial
frogs are diphyletic (Anura: Hemiphractidae: Gastrotheca).
Molecular Phylogenetics and Evolution 68: 709–714.
Boulenger, G.A. (1882): Catalogue of the Batrachia Salientas.
Ecaudata in the Collection of the British Museum, Second
Edition. London, United Kingdom, British Museum.
Catenazzi, A., Bustamante, M. (2007): Anfibios y Reptiles. In:
Perú: Nanay-Mazán-Arabela. Rapid Biological Inventories
Report 18, p. 62–67. Vriesendorp, C., Álvarez, J.A., Barbagelata,
N., Alverson, W.S., Moskovits, D.K., Eds., Chicago, USA, The
Field Museum.
Catenazzi, A., Venegas, P.J. (2012): Anfibios y Reptiles. In: Perú:
Cerros de Kampankis. Rapid Biological and Social Inventories
Report 24, p. 106–116. Pitman, N., Ruelas, E.I., Alvira, D.,
Vriesendorp, C., Moskovits, D.K., del Campo, Á., Wachter,
T., Stotz, D.F., Noningo, S.S., Tuesta, E.C., Smith, R.C., Eds.,
Chicago, USA, The Field Museum.
Chávez, G., Mueses-Cisneros, J.J. (2016): Amphibians and reptiles.
In: Perú: Medio Putumayo-Algodón. Rapid Biological and
Social Inventories Report 28, p. 131-199. Pitman, N., Bravo, A.,
Claramunt, S., Vriesendorp, C., Alvira Reyes, D., Ravikumar,
A., del Campo, Á., Stotz, D.F., Wachter, T., Heilpern, S.,
Rodríguez Grández, B., Sáenz Rodríguez, A.R., Smith, R.C.,
Eds., Chicago, USA, The Field Museum.
Cisneros-Heredia, D.F., McDiarmid, R.W. (2005): Amphibia,
Centrolenidae, Centrolene peristictum, Centrolene prosoblepon,
Cochranella cochranae, Cochranella midas, Cochranella
resplendens, Cochranella spinosa, Hyalinobatrachium
munozorum: Range extensions and new provincial records.
Check List 1: 18–22.
Cisneros-Heredia, D.F., Meza-Ramos, P. (2007): An enigmatic
new species of Glassfrog (Amphibia: Anura: Centrolenidae)
from the Amazonian Andean slopes of Ecuador. Zootaxa 1485:
33–41.
Crump, M.L., Scott, J.N. Jr. (1994): Visual encounter surveys.
In: Measuring and Monitoring Biological Diversity: Standard
Methods for Amphibians, p. 88–92. Heyer, W.R., Donnelly,
Omar Rojas-Padilla et al.
470
M.A., McDiarmid, R.W., Hayek, L.C., Foster, M.S., Eds.,
Washington DC, USA, Smithsonian Institution Press.
Delia, J., Cisneros-Heredia, D.F., Whitney J., Murrieta-Galindo,
R. (2010): Observations on the reproductive behavior of a
Neotropical glassfrog, Hyalinobatrachium fleischmanni (Anura:
Centrolenidae). South American Journal of Herpetology 5: 1–
12.
Diaz-Ricarte, J., Guevara-Molina, R., Díaz-Morales, R.D. (2016):
Natural history notes. Teratohyla midas (Santa Cecilia Cochran
Frog). Reproductive Behavior. Herpetological Review 47:
650–651.
Duellman, W.E., Trueb, L., Lehr, E. (2006): A new species
of marsupial frog (Anura: Hylidae: Gastrotheca) from the
Amazonian Slopes of the Cordillera Oriental in Peru. Copeia
4: 595–603.
Duellman, W.E. (2015): Marsupial Frogs Gastrotheca & Allied
Genera, First Edition. Baltimore, USA, Johns Hopkins
University Press.
França, F.G.R., Venâncio, N.M. (2010): Reptiles and amphibians
of a poorly known region in southwest Amazonia. Biotemas 23:
71–84.
Goin, C.J. (1964): Synonymy and distribution of the frog
Gastrotheca longipes (Boulenger). Quarterly Journal of the
Florida Academy of Sciences 26: 347–352.
Gosner, K.L. (1960): A simplified table for staging anuran embryos
and larvae with notes on identification. Herpetologica 16: 183–
190.
Guayasamin, J.M., Ron, S., Cisneros-Heredia, D.F., Lamar,
W., McCracken, S.F. (2006): A new species of frog of the
Eleutherodactylus lacrimosus assemblage (Leptodactylidae)
from the western amazon basin, with comments on the utility
of canopy surveys in lowland rainforest. Herpetologica 62:
191–202.
Jenkins, C., Pimm, S.L., Joppa, L.N. (2013): Global patterns of
terrestrial vertebrate diversity and conservation. Proceedings of
the National Academy of Sciences 110: E2602–E2610.
Kok, P.J.R., Castroviejo-Fisher, S. (2008): Glassfrogs (Anura:
Centrolenidae) of Kaieteur National Park, Guyana, with notes
of the distribution and taxonomy of some species of the family
in the Guiana Shield. Zootaxa 1680: 25–53.
Lourenço-de-Moraes, R., Ferreira, R.B., Mira-Mendes, C.V.,
Zocca, C.Z., Medeiros, T., Ruas, D.S., et al. (2016): Escalated
antipredator mechanisms of two neotropical marsupial treefrogs.
Herpetological Journal 26: 237–244.
Lynch, J.D., Duellman, W.E. (1973): A review of the Centrolenid
frogs of Ecuador, with descriptions of new species. Occasional
Papers University of Kansas Museum of Natural History 16:
1–66.
Malambo, C., Gonzáles-Ibarra, J.F., Gomez-Polania, Y.C. (2013):
Amphibia, Anura, Centrolenidae Teratohyla midas (Lynch
& Duellman, 1973) and Cochranella resplendens (Lynch &
Duellman, 1973): First and second record respectively for
Colombia. Check List 9: 894–896.
Melo-Sampaio, P.R., de Oliveira, M.B. (2013): Geographic
distribution. Teratohyla midas. Herpetological Review 44: 104.
Melo-Sampaio, P.R., de Souza, C.M.B. (2015): New and
noteworthy distributional records of treefrogs (Anura) from
southwestern Amazonia. Check List 11: 1681.
Molina-Zuluaga, C., Cano, E., Restrepo, A., Rada, M., Daza,
J.M. (2017): Out of Amazonia: the unexpected trans-Andean
distribution of Cochranella resplendens (Lynch and Duellman,
1978) (Anura: Centrolenidae). Zootaxa 4238: 268–274.
Morales, V.R., McDiarmid, R.W. (1996): Annotated checklist of
the amphibians and reptiles of Pakitza, Manu National Park
Reserve Zone, with comments on the herpetofauna of Madre de
Dios, Peru. In: Manu: The Biodiversity of Southeastern Peru,
p. 503–522. Wilson, E., Sandoval. A., Eds., Washington DC,
USA, Smithsonian Institution Press.
Ortega-Andrade, H.M., Rojas-Soto, O.R., Valencia, J.H., de los
Monteros, A.E., Morrone, J.J., Ron, S.R., Cannatella, D.C.
(2015): Insights from integrative systematics reveal cryptic
diversity in Pristimantis frogs (Anura: Craugastoridae) from the
Upper Amazon basin. PLoS ONE 10: e0143392.
Osorno, M.M., Gutiérrez-Lamus, D.L., Blanco, J.C. (2011):
Anfibios en un gradiente de intervención en el noroccidente de
la amazonia colombiana. Revista Colombia Amazónica 4: 143-
160.
Padial, J.M., Gagliardi-Urrutia, G., Chaparro, J.C., Gutérrez, R.C.,
Rojas-Padial, O., Castroviejo-Fisher, S. (2016): Diversidad de
anfibios y reptiles en el Parque Nacional Alto Purús, la Reserva
Comunal Purús, y sus áreas de influencia. In: Diversidad
Biológica del Sudeste de la Amazonía Peruana: Avances en
la Investigación, p. 105–121. Germaná, C., Mena Álvarez,
J.K., Eds., Lima, Perú, World Wildlife Fund, Cooperative
for Assistance and Relief Everywhere Perú, ProNaturaleza,
ProPurús, Sociedad Zoológica de Fráncfort, Organización
Regional AIDESEP Ucayali.
Pitman, N.C.A., Gagliardi-Urrutia, G., Jenkins, C.N. (2013): La
Biodiversidad de Loreto, Perú: El Conocimiento Actual de
Plantas y Vertebrados Terrestres, First Edition. Washington DC,
USA, Center for International Environmental Law.
Pontes, R., Mattedi, C. (2013): An unexpected record of Teratohyla
midas (Lynch and Duellman, 1973) for Brazil reveals the
presence of glassfrogs in the Brazilian northern lowlands
(Anura: Centrolenidae). Check List 9: 1590–1591.
QGIS Development Team (2017): QGIS Geographic Information
System. Open Source Geospatial Foundation. Available at:
http://qgis.osgeo.org. Accessed on 26 august 2018.
Rivera, C., Soini, P. (2002): Herpetofauna de Allpahuayo-Mishana.
La herpetofauna de la Zona Reservada Allpahuayo-Mishana,
Amazonía norperuana. Recursos Naturales 1: 143–151.
Rivera-Gonzáles, C., von May, R., Aguilar, C., Arista, I., Curo, A.,
Schulte, R. (2003): Una evaluación preliminar de la herpetofauna
en la Zona Reservada Allpahuayo-Mishana, Loreto, Perú. Folia
Amazónica 14: 139–148.
Rodríguez-Cardozo, N.R., Arriaga-Villegas, N.C., Diaz-Ricarte,
J.C. (2016): Anuran diversity in the El Manantial Community
Natural Reserve, Florencia, Caquetá, Colombia. Revista
Biodiversidad Neotropical 6: 212–220.
Rojas, R.R., Carvalho, V.T.D., Ávila, R.W., Farias, I.P., Gordo,
M., Hrbek, T. (2015): Two new species of Amazophrynella
(Amphibia: Anura: Bufonidae) from Loreto, Peru. Zootaxa
3946: 79–103.
Rojas-Morales, J.A., Escobar-Lasso, S. (2013): Notes on the natural
history of three glass frog species (Anura: Centrolenidae) from
the Andean Central Cordillera of Colombia. Boletín Científico
First records of frog species for the Allpahuayo-Mishana National Reserve, Peru 471
Museo de Historia Natural de la Universidad de Caldas 17:
127–140.
Ron, S.R., Venegas, P.J., Ortega-Andrade, H.M., Gagliardi-
Urrutia, G., Salerno, P.E. (2016): Systematics of Ecnomiohyla
tuberculosa with the description of a new species and comments
on the taxonomy of Trachycephalus typhonius (Anura, Hylidae).
ZooKeys 630: 115–154.
SERNANP (2017): Servicio Nacional de Áreas Naturales
Protegidas por el Estado: Allpahuayo Mishana. Available at:
http://www.sernanp.gob.pe/allpahuayo-mishana. Accessed on
22 august 2018.
Terán-Valdez, A., Guayasamin, J.M., Coloma, L.A. (2009):
Description of the tadpole of Cochranella resplendens and
redescription of the tadpole of Hyalinobatrachium aureoguttatum
(Anura, Centrolenidae). Phyllomedusa 8: 105–124.
Toft, C.A., Duellman, W.E. (1979): Anurans of the lower rio
Llullapichis, Amazonian Perú: A preliminary analysis of
community structure. Herpetologica 35: 71–77.
Toledo, L.F., Sazima, I., Haddad, C.F.B. (2011): Behavioural
defences of anurans: an overview. Ethology Ecology &
Evolution 23: 1–25.
Torres-Gastello, C.P., Suárez-Segovia, J., Cisneros-Heredia, D.F.
(2007): Cochranella erminea, a new species of Centrolenidae
(Amphibia: Anura: Athesphatanura) from Amazonian Peru.
Journal of the National Museum (Prague), Natural History
Series 176: 1–12.
Twomey, E., Delia, J., Castroviejo-Fisher, S. (2014): A review of
northern peruvian glassfrog (Centrolenidae) with the description
of four new remarkable species. Zootaxa 3851: 1–87.
Venegas, P.J., Gagliardi-Urrutia, G., Odicio, M. (2014): Anfibios y
reptiles. In: Perú: Cordillera Escalera-Loreto. Rapid Biological
and Social Inventories Report 26, p. 127–138. Pitman N.,
Vriesendorp C., Alvira D., Markel J.A., Johnston M., Ruelas
Inzunza E., Lancha Pizango A., Sarmiento Valenzuela G.,
Álvarez-Loayza P., Homan J., Wachter T., del Campo Á., Stotz
D.F., Heilpern S., Eds., Chicago, USA, The Field Museum.
Vockenhuber, E.A., Hödl, W., Karpefn, U. (2008): Reproductive
behaviour of the glass frog Hyalinobatrachium valerioi (Anura:
Centrolenidae) at the tropical stream Quebrada Negra (La
Gamba, Costa Rica). Stapfia 88: 335–348.
von May, R., Venegas, P.J. (2010): Anfibios y reptiles. In: Perú:
Maijuna. Rapid Biological and Social Inventories Report 22,
p. 74–81. Gilmore, M.P., Vriesendorp, C., Alverson, W.S., del
Campo, Á., von May, R., López Wong, C., Ríos Ochoa, S., Eds.
Chicago, USA, The Field Museum.
von May, R., Mueses-Cisneros, J.J. (2011): Anfibios y reptiles. In:
Perú: Yaguas-Cotuhé. Rapid Biological and Social Inventories
Report 23, p. 108–106. Pitman, N., Vriesendorp, C., Moskovits,
D.K., von May, R., Alvira, D., Wachter, T., Stotz, D.F., del
Campo, Á., Eds. Chicago, USA, The Field Museum.
Yánez-Muñoz, M.H., Chimbo, A. (2007): Anfibios y reptiles. In:
Ecuador: Territorio Cofan Dureno. Rapid Biological and Social
Inventories Report 19, p. 96–99. Borman, R., Vriesendorp, C.,
Alverson, W.S., Moskovits, D.K., Stotz, D.F., del Campo, Á.,
Eds. Chicago, USA, The Field Museum.
Yánez-Muñoz, M., Venegas, P.J. (2008): Anfibios y reptiles. In:
Ecuador-Perú: Cuyabeno-Güeppí. Rapid Biological and Social
Inventories Report 20, p. 90–96. Alverson, W.S., Vriesendorp,
C., del Campo, Á., Moskovits, D.K., Stotz, D.F., García, M.D.,
Borbor, L.A., Eds. Chicago, USA, The Field Museum.
Accepted by Fabrício Oda
Omar Rojas-Padilla et al.
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