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Ocampo Et Al 2024
Ocampo Et Al 2024
Ocampo Et Al 2024
Mauricio Ocampo1,2,*, James Aparicio1, Nuria Bernal Hoverud3, Enrique Domic3, and Robert B. Wallace3
Abstract. Bolivia has a great diversity of ecoregions and is home to a large number of amphibian species. Many of these
ecoregions are protected in several national parks. However, Madidi National Park and Natural Integrated Management Area
is especially striking among them, for having the largest number of ecoregions represented. In this study we carried out a
thorough literature search for information on amphibian records within the national park, as well as extensive field work to
understand the alpha, beta, gamma, and dark diversity of amphibians in different ecoregions of Madidi. We confirmed the
presence of 127 amphibian species in the park. Diversity indices indicate that the ecoregions are quite different from one
another, with high species turnover and many unique species in each ecoregion. Our results show that the amphibian diversity
found in this protected area exceeds the diversity reported for other megadiverse protected areas in the Tropical Andes, such
as Manu in Peru or Yasuní in Ecuador, further suggesting that it may be the most diverse national protected area in the world.
Figure 1. Map of the study area showing Madidi National Park and Natural Integrated Management Area, Bolivia (yellow line),
the 50-km buffer area (light blue line), fieldwork camps (stars), amphibian records from the database and fieldwork (red circles),
and ecoregions, with numbers representing Lake Titicaca (1), Wet Puna (2), High Andean Vegetation (3), Yungas (4), Inter-
Andean Dry Forests (5), Sub-Andean Amazon Forests (6), Pre-Andean Amazon Forests (7), Cerrado Paceño (8), Llanos de Moxos
Flooded Savannah (9), Pando Amazon Forest (10), and Amazonian Flood Forest (11).
374 Mauricio Ocampo et al.
Table 1. Numbers of species found in the ecoregions of Madidi National Park, Bolivia, and surrounding, according to record
criteria. The first numeric column lists the number of effective evaluation days spent in each surveyed ecoregion. Column headings
for the number of species found under the listed criterion include: FW – our fieldwork; BLI – baseline inside Madidi; BLO –
baseline outside Madidi; Madidi – total number of amphibians recorded in Madidi National Park (FW + BLI); and Gamma – total
number of species recorded in this study (FW+BLI+BLO). Dashes indicate the ecoregion is not relevant for the column.
this information to estimate the total number of species, model is that S increases with sample size, while the
including those that have not been detected. Finally, expectation of α remains constant, causing the beta
the Jackknife2 estimator is based on a resampling diversity to increase with sample size. A solution to this
approach, where a fraction of the data from the original problem is to study the beta diversity of pairs of sites.
sample is sequentially removed. Then, the number of We used a dendrogram and ternary diagram to visualize
species present in each of these smaller subsets of data the dissimilarities by ecoregions. The gamma diversity
is calculated, and an estimation of the total richness is is represented by all the species recorded in this study,
obtained based on the variability among subsets. With both inside and outside the park (those within a 50-
the calculation of these estimators, we will be able to km buffer). We measured the dark diversity from the
verify if sampling effort was sufficient to estimate the Beals Index on species co-occurrence likelihood with
total richness obtained with the baseline and thus have 95% confidence (Lewis et al., 2016), which is more
a better idea of the effort required to approach the actual accurate with far fewer negative mismatches. This
diversity of an area like Madidi. index provides new and complementary information
For these analyses, we used the vegan package in R on species that should be present in an ecoregion and
v4.2.1 (R Core Team, 2022), and the functions rarefy, that for unknown reasons could not be recorded. It
where the sample is a vector with sequences every is calculated from the frequency of co-occurrence
50 individuals; the function specaccum, run with the with other species, providing a complementary list of
random method and 100 permutations; the function species with a reasonable degree of precision (Lewis
estimateR to estimate ACE with the sample size; and et al., 2017). We used the dark function in the vegan
the function specpool to estimate Chao2 and Jackknife2 package in R to conduct the analysis (R Core Team,
from the matrix. 2022).
For the beta diversity analysis, we measured
dissimilarity between ecoregions and sub-regions using Results
the BiodiversityR package, and we used the function Baseline. The total number of records was 2068 (557
betadiver to calculate Whittaker’s Index, which shows inside Madidi, 1511 outside Madidi), representing
the relative difference in species composition among 149 species, 114 inside Madidi, 121 in the buffer
plots. The index is calculated as areas outside Madidi, and 82 shared species (Table 1,
βW = S/α − 1 Appendix 2). We also identified three putative new
where S is the total number of species and α is the species to science in the photographic records of WCS
average number of species per site. A drawback of this (Table 2).
Amphibian Diversity in Madidi National Park and Natural Integrated Management Area 375
Table 2. Checklist of amphibian species recorded in Madidi National Park and Natural Integrated Management Area, Bolivia.
Column heading abbreviations include Rec – a record of the species as fw (species was encountered during our fieldwork), bl
(record from baseline database), or bo (obtained by both methods); CS – conservation status, according to IUCN categories;
and ecoregions represented in the park: AFF (Amazonian Flood Forest), SAF (Sub-Andean Amazon Forests), PAF (Pre-Andean
Amazon Forests), PNF (Pando Amazon Forest), CP (Cerrado Paceño), FSM (Llanos de Moxos Flooded Savannah), YU (Yungas),
IDF (Inter-Andean Dry Forests), and HAV (High Andean Vegetation). In each ecoregion, the species may have been found inside
the park (in), outside the park (ou), or both (bo). A new record for the park is indicated by an asterisk (*) and a new record for
Bolivia by a superscripted letter a.
FROGS
Aromobatidae
Allobates femoralis (Boulenger, 1884) bl LC in bo
Allobates mcdiarmidi (Reynolds & Foster, 1992) bl CR in ou
Allobates trilineatus (Boulenger, 1884) bo LC ou ou bo ou ou
Bufonidae
Atelopus tricolor Boulenger, 1902 bl CR in bo
*Nannophryne apolobambica De la Riva et al., 2005 bo CR bo
Rhaebo ecuadorensis Mueses-Cisneros, 2012 bl ou
Rhaebo guttatus (Schneider, 1799) bo LC ou bo bo
Rhinella diptycha (Cope, 1862) bl DD ou
Rhinella exostosica Ferrão et al., 2020 bo bo bo ou ou ou bo in
Rhinella fissipes (Boulenger, 1903) bl DD bo ou
Rhinella leptoscelis (Boulenger, 1912) bo NT in in
Rhinella major (Müller & Hellmich, 1936) bo bo bo ou ou
Rhinella aff. margaritifera bo LC in
Rhinella marina (Linnaeus, 1758) bo LC ou bo bo ou bo in
Rhinella poeppigii (Tschudi, 1845) bo LC ou bo bo bo in
Rhinella spinulosa (Wiegmann, 1834) bl LC bo bo
Rhinella stanlaii (Lötters & Köhler, 2000) bl LC in
Rhinella tacana (Padial et al., 2006) bo LC in in
Rhinella veraguensis (Schmidt, 1857) bo LC bo in in ou
Centrolenidae
*Cochranella nola Harvey, 1996 fw LC in
Nymphargus bejaranoi (Cannatella, 1980) bl EN in in
Hyalinobatrachium bergeri (Cannatella, 1980) bl LC in ou ou
Hyalinobatrachium carlesvilai Castroviejo-Fisher et al., 2009 bl LC ou
Ceratophryidae
Ceratophrys cornuta (Linnaeus, 1758) bo LC ou bo bo ou
Dendrobatidae
Ameerega boliviana (Boulenger, 1902) bl NT ou
Ameerega hahneli (Boulenger, 1884) bo LC ou bo ou
Ameerega petersi (Silverstone, 1976) bl LC ou
Ameerega picta (Tschudi, 1838) bo LC ou bo bo ou in in
Ameerega trivittata (Spix, 1824) bl LC ou ou
Ranitomeya sirensis (Aichinger, 1991) bl LC ou ou
Hemiphractidae
Gastrotheca marsupiata (Duméril & Bibron, 1841) bl LC ou
Hemiphractus scutatus (Spix, 1824) bl LC ou
Hylidae
*,aBoana appendiculata (Boulenger, 1882) fw in in
Boana balzani (Boulenger, 1898) bo LC bo bo
Boana boans (Linnaeus, 1758) bo LC bo bo ou in in
Boana calcarata (Troschel, 1848) bo LC in bo
*Boana cinerascens (Spix, 1824) bo LC bo
Boana geographica (Spix, 1824) bo LC ou bo bo ou ou
Boana lanciformis (Cope, 1871) bo LC ou bo bo ou ou in in
Boana punctata (Schneider, 1799) bl LC bo bo
376 Mauricio Ocampo et al.
Table 2. Cont.
Leptodactylidae
Adenomera chicomendesi Carvalho et al., 2019 bo ou in bo ou
Adenomera hylaedactyla (Cope, 1868) bl LC ou ou ou
*Adenomera sp. 1 fw in
Engystomops freibergi (Donoso-Barros, 1969) bo LC ou bo bo bo
Leptodactylus bolivianus Boulenger, 1898 bl LC ou bo ou ou
Leptodactylus didymus Heyer et al., 1996 bo LC bo in ou ou
Leptodactylus elenae Heyer, 1978 bl LC bo bo in
Leptodactylus fuscus (Schneider, 1799) bl LC bo bo ou ou
Leptodactylus griseigularis (Henle, 1981) bo LC in in bo in
*Leptodactylus knudseni Heyer, 1972 fw LC in
Leptodactylus leptodactyloides (Andersson, 1945) bl LC ou bo bo ou ou in
Leptodactylus macrosternum Miranda-Ribeiro, 1926 bl LC bo ou
Amphibian Diversity in Madidi National Park and Natural Integrated Management Area 377
Table 2. Cont.
Microhylidae
Chiasmocleis bassleri Dunn, 1949 bl LC ou
Chiasmocleis royi (Morales, 2007) bl ou
Chiasmocleis ventrimaculata (Andersson, 1945) bl LC ou
Ctenophryne geayi Mocquard, 1904 bo LC ou in in
Elachistocleis helianneae Caramaschi, 2010 bo LC bo in in
Elachistocleis magna Toledo, 2010 bl in
Elachistocleis muiraquitan Nunes-de-Almeida & Toledo, 2012 bl ou bo ou
Hamptophryne boliviana bo LC ou bo bo ou
Pipidae
Pipa pipa (Linnaeus, 1758) bo LC ou in bo ou
Phyllomedusidae
Callimedusa atelopoides (Duellman et al., 1988) bl LC ou ou
Callimedusa tomopterna (Cope, 1868) bo LC in bo ou bo
Cruziohyla craspedopus (Funkhouser, 1957) bl LC in
Phyllomedusa bicolor (Boddaert, 1772) bl LC in bo ou
Phyllomedusa boliviana Boulenger, 1902 bo LC bo in in
Phyllomedusa camba De la Riva, 1999 bl LC ou bo bo ou bo
Phyllomedusa vaillantii Boulenger, 1882 bo LC bo bo ou ou
Pithecopus hypochondrialis (Daudin, 1800) bl LC in
Pithecopus palliatus (Peters, 1873) bl LC ou in ou ou
Ranidae
Lithobates palmipes (Spix, 1824) bl LC bo bo ou
Strabomantidae
Noblella myrmecoides (Lynch, 1976) bl LC ou ou
*Noblella sp. 1 fw in
Microkayla chaupi (De la Riva & Aparicio, 2016) bl VU in
Microkayla colla (De la Riva et al., 2016) bl VU in
Microkayla guillei (De la Riva, 2007) bl CR ou
Microkayla kallawaya (De la Riva & Martínez-Solano, 2007) bl CR ou
Microkayla katantika (De la Riva & Martínez-Solano, 2007) bl VU ou
Microkayla saltator (De la Riva et al., 2007) bl CR ou
Microkayla sp. 0 bl in
Microkayla sp. 1 bl in
Microkayla sp. 2 bl in
*Microkayla sp. 3 fw in
*Microkayla sp. 4 fw in
*Microkayla sp. 5 fw in
*Microkayla sp. 6 fw in
Oreobates cruralis (Boulenger, 1902 bo LC bo bo bo
Oreobates discoidalis (Peracca, 1895) bl DD in
Oreobates madidi (Padial et al., 2005) bl LC in
Oreobates sanderi (Padial et al., 2005) bo LC in
*Oreobates sp. 1 fw in
Pristimantis altamazonicus (Barbour & Dunn, 1921) bo LC in bo
Pristimantis danae (Duellman, 1978) bl LC bo bo ou ou bo in
378 Mauricio Ocampo et al.
Table 2. Cont.
Telmatobiidae
Telmatobius bolivianus Parker, 1940 bl CR ou
Telmatobius marmoratus (Duméril & Bibron, 1841) bl EN ou ou
Telmatobius sanborni Schmidt, 1954 bl CR ou
Telmatobius timens De la Riva et al., 2005 bl CR in
CAECILIANS
Caeciliidae
Caecilia marcusi Wake, 1985 bl DD in
Siphonopidae
Siphonops annulatus (Mikan, 1822) bl LC in ou ou
Fieldwork. At the 15 sites surveyed, we gathered obtained by including the baseline and field work.
272 records, corresponding to 64 species, 15 of which Beta diversity. The dissimilarity index shows
represent new records for the park, seven of which are that Sub-Andean Amazon Forests and Pre-Andean
also putative new species to science, and three are new Amazon Forests are the most similar, while the High
records for Bolivia. Eleven families were registered, Andean Vegetation and the Cerrado Paceño are unique
and the family Strabomantidae was represented by 16 and completely dissimilar to all the other ecoregions
species, the highest number of the survey (Tables 1, 2, present in Madidi. The Inter-Andean Dry Forests are
Appendix 3). more similar to Pre-Andean and Sub-Andean Amazon
Alpha diversity. We recorded 64 species during Forests (Fig. 3).
fieldwork in Madidi (Table 1), and the intensive search
method was the most efficient (61 species). With the
pitfall method we recorded eight species, three of
which were recorded only using this method. The three
ecoregions with the highest richness were Pre-Andean
Amazon Forest (38 species), Sub-Andean Amazon
Forest (21 species), and Yungas (18 species). Only a
single species was registered in Cerrado Paceño.
The species accumulation curve shows a rapid
increase in species up to the fourth sampled site,
increasing therein very slowly up to the last site, almost
seeming to reach an asymptote (Fig. 2). However, the
samples-based rarefaction curve shows that we are not
yet close to reaching the asymptote. The individual-
based rarefaction curve estimates that we must registred
up to 501 individuals to be able to reach the 64 species
we recorded in the 15 visited sites. Species richness
estimators predict that richness should be higher Figure 3. Dendrogram of dissimilarities among ecoregions.
than what we obtained. The Chao 2 and Jackknife 2 The colours correspond to the map, and the scale represents
estimators had a better fit compared to the total list the degree of difference between ecoregions.
Amphibian Diversity in Madidi National Park and Natural Integrated Management Area 379
Figure 2. Species accumulation curves developed from fieldwork in Madidi National Park and Natural Integrated Management
Area, Bolivia. Individual-based rarefaction curve is the species records computed for every 50 recorded individuals. Samples-
based rarefaction curve is the species records computed for each site sampled. Total species richness is the sum of the species
recorded during fieldwork and the species from the baseline.
The ternary diagram shows that more than half of Boana appendiculata (Boulenger, 1882).—Two
the pairwise comparisons between the ecoregions in individuals were collected at Alto Madidi, a subadult
Madidi do not share any species (comparison 2, 3, 6, (CBF-7080) on 24 October 2015 at 13.6372°S,
7, 10, 12, 13, and 14), and that there are consistently 68.7528°W, elevation 241 m (Fig. 5a), and a juvenile
large differences in the number of unique species (Fig. (CBF-7081) on 29 October 2015 at 13.6363°S,
4). The Sub-Andean Amazon Forests and Pre-Andean 68.7516°W, elevation 264 m (Fig. 5b). We used the
Amazon Forests (Comparison 1) share the greatest following diagnostic characters to identify the species:
number of species, but still the index value is barely finely granular dorsal skin, brown dorsal coloration
a third. Therefore, we can infer that all the ecoregions with irregular dark brown markings that include an
in Madidi include, for the most part, unique amphibian irregular X-shaped mark in the scapular region, hidden
species. thigh surfaces with dark vertical stripes. This species
Gamma diversity. The total gamma diversity within can be confused with B. geographica (Spix, 1824) but
the nine ecoregions inside and outside Madidi is 162 differs from it by having yellow interdigital membranes
species – including both baseline and fieldwork data when alive, while B. geographica has red membranes
(Table 1). Sixteen families were recorded throughout (Boulenger, 1882; Fouquet et al., 2016; Caminer and
the study, and the family Hylidae had the most Ron, 2020).
representation with 51 species. Five families were Pristimantis diadematus (Jiménez de la Espada,
represented by only one species, and the most diverse 1875).—One individual was collected at Sarayoj (CBF-
genus was Dendropsophus with 17 species (Table 2). 7452) on 16 September 2017 at 14.6193°S, 68.1939°W,
Dark diversity. The dark diversity index was 0 for all elevation 1328 m (Fig. 6a, b). The diagnostic characters
ecoregions, which means that there are no additional that confirmed species identity are: round head, smooth
species that should be recorded due to the high dorsal skin with scattered tubercles, fingers without
probability of co-occurrence with others. webbing; first finger shorter than second, digits end in
New records for the country. We report three new wide, truncated discs; dorsum brown with dark brown
country records at three separate localities, which we longitudinal markings, groin and proximal anterior and
describe in the following paragraphs. posterior surfaces of the thighs orange with dark brown
380 Mauricio Ocampo et al.
Figure 4. Ternary diagram where a is number of species shared between two sites, and b and c are the numbers of unique
species (not shared). Ecoregions are abbreviated as Sub-Andean Amazon Forests (SAF), Pre-Andean Amazon Forests (PAF),
High Andean Vegetation (HAV), Cerrado Paceño (CP), Yungas (Y), and Inter-Andean Dry Forests (IDF).
Figure 5. First record of Boana appendiculata for Bolivia from Alto Madidi. (a) Adult (CBF-7080). (b) Juvenile (CBF-7081).
Photos by Mauricio Ocampo.
Amphibian Diversity in Madidi National Park and Natural Integrated Management Area 381
Figure 6. First record of Pristimantis diadematus for Bolivia from Sarayoj (CBF-7452). Photos by Mauricio Ocampo.
diagonal bars in the groin and horizontal bars in the increase knowledge of anuran diversity for Madidi
extremities, pale pink venter with dark spots (Fig. 6b). by 15.4%, and from our fieldwork alone we were able
This species can be confused with P. altamazonicus to record 50% of the amphibian diversity previously
(Barbour & Dunn, 1921), which differs by having a reported for the park. Previous efforts had produced
truncated head, rough back, and dark belly (Rodriguez a maximum of 43.2% of the confirmed amphibian
and Duellman, 1994). Another very similar species is
species (Emmons, 1991; Pérez-Bejar, 1997; Pérez et
P. sinschi Moravec et al., 2020, but this species has a
al., 2002; Cortez-Fernandez, 2005). Since Identidad
black groin (Moravec et al., 2020).
Madidi was a three-year effort, it represents the most
Pristimantis lacrimosus (Jiménez de la Espada,
1875).—One individual was collected at Mamacona complete survey to date, but also underlines that the
(CBF-7465) on 30 June 30 2016 at 14.4759°S; study of diversity in such heterogeneous environments
68.1880°W, elevation 1621 m (Fig. 7). We used the requires a long-term effort.
following diagnostic characters to identify the species:
smooth dorsal skin, granular belly; snout rounded, top
of the head flat. Toes without webbing, digits end in
large, rounded discs. Dorsum olive green with cream
markings covering the head, venter creamy yellow.
Only P. acuminatus (Shreve, 1935) can have the same
colouration, but it differs from P. lacrimosus because
it lacks a tympanum (Rodriguez and Duellman, 1994).
Discussion
In this study, we gathered a large amount of scattered,
unpublished, and little-known information on the
amphibians of Madidi, completing the list with three
years of fieldwork in previously unsampled ecoregions. Figure 7. First record of Pristimantis lacrimossus for Bolivia
With the Identidad Madidi project we were able to from Mamacona (CBF-7465). Photo by Mauricio Ocampo.
382 Mauricio Ocampo et al.
The collected specimens are very important for The taxonomy of Rhinella margaritifera (Laurenti,
identification since new morphological and molecular 1768) was uncertain for a long time, mainly because
analyses are regularly being published and gradually the holotype was lost for over two centuries. In 2011
help us better understand the true diversity of a specimen housed in the Academy of Sciences in St.
ecosystems (Fouquet et al., 2007). For example, our Petersburg, Russia, was identified as the holotype
record of Boana appendiculata was originally assigned of R. margaritifera, although the type locality
to B. geographica until a recent taxonomic update remains uncertain (Milto and Barabanov, 2011). This
(Caminer and Ron, 2020) allowed us to confirm the provided greater clarity regarding the morphology
record as new to the Bolivian anurofauna. Similarly, of R. margaritifera, allowing for the description and
the species richness of the genus Microkayla in Madidi validation of other species (Ferrão et al., 2020). In
is likely under-represented because each species has Bolivia, R. stanlaii (Lötters and Köhler, 2000), a species
a naturally restricted distribution. These frogs are in the R. margaritifera group, had already been recorded
physiologically dependent on high levels of humidity, in the central part of the country (Lötters and Köhler,
and their small and robust bodies and short limbs give 2000), and the rest of records were identified as R. aff.
them limited dispersal capacity (De la Riva et al., 2017; margaritifera. However, Ferraõ et al. (2020) determined
Burrowes et al., 2020; De la Riva, 2020). For this that the records from the north and northwest of Bolivia
reason, De la Riva (2007) proposed that every valley corresponded to a new species they described, R.
on the Amazonian slopes of the Andes with an adequate exostosica, characterized by poorly developed cephalic
patch of habitat could contain an endemic species (De crests, while individuals with well-developed cephalic
la Riva, 2007; Burrowes et al., 2020), so we are certain crests are still referred to as R. aff. margaritifera. In our
that even more new species of this genus can be found evaluations, we encountered both types, and therefore,
in Madidi. we maintain the designation of R. aff. margaritifera for
The same situation occurs with the genus Noblella, the individuals with developed crests.
which is distributed from northern Ecuador to central One result that stood out was that the amphibian
Bolivia, and different species have been found with a diversity of the Inter-Andean Dry Forests was more
separation of < 10 km (i.e., N. coloma and N. worleyae; similar to the Pre- and Sub-Andean Amazonian Forest
Guayasamin and Terán-Valdez, 2009; Reyes-Puig et al., than to the Yungas ecoregion, even though the Inter-
2020). This highly endemic genus has a very restricted Andean Dry Forests are almost completely surrounded
distribution (Lehr and Catenazzi, 2009; Reyes-Puig et al., by Yungas. The geography determines many factors
2021), and it contains the smallest species in the Andes such as temperature, humidity, and isolation, which
(11.4 mm on average body length in N. pygmaea Lehr have a physicochemical effect that will determine the
and Catenazzi, 2009). The differences in designs and presence of the species (Gallardo-Cruz et al., 2009;
coloration of the individuals we found in Madidi, along McCain and Sanders, 2010). However, the geological
with a distance greater than 130 km from the nearest and biogeographical history of the Inter-Andean Dry
species (N. peruviana [Noble, 1921]), provide enough Forests is not yet well understood, and more detailed
evidence to suspect that it is a putative new species. studies could eventually lead to the discovery of species
The true diversity of the genus Adenomera is just new to science. Our results show that although there are
becoming known, since eight new species were described some similarities between the diversity of ecoregions, in
in the last three years (de Carvalho et al., 2020a–c). The general the differences are predominantly greater. The
morphological differences, overall colouration, and a turnover in the composition of species is high, supporting
distribution restricted to the Cerrado Paceño, makes the concept that the uplift of the Andes has been working
our specimens (which we list as Adenomera sp.) quite as a species pump (Hoorn et al., 2010, 2013).
different from other known species. Similarly, the Numerous nonparametric estimators for species
morphological differences we found in the individuals richness have been proposed, and the most used are
of the genus Oreobates suggests that these specimens Bootstrap, Jackknife1, Jackknife2, Chao1, Chao2,
could be members of an undescribed species. In all ACE, and ICE (Magurran, 2004). However, these were
cases, tissue samples from the putative new species evaluated and compared by numerous studies, and most
found in this study are being genetically analysed, and agree that the best estimators are Jackknife2 and Chao2
with careful morphological comparisons, we will be (Colwell and Coddington, 1994; Magurran, 2004;
able to solidly test our hypotheses. López-Gómez and Williams-Linera, 2006; Milutinović
Amphibian Diversity in Madidi National Park and Natural Integrated Management Area 383
et al., 2015), and in our case, Jackknife2 was the closest References
estimator to the total number of records in Madidi. The AmphibiaWeb (2023): AmphibiaWeb. Available at: https://
estimation of species through the dark diversity index amphibiaweb.org. Accessed on 30 January 2023.
allows us to complement the ecoregion’s list from Angulo, A., Rueda-Almonacid, J.V., Rodríguez-Mahecha, J.V.,
the co-occurrence of species (Lewis et al., 2016). The La Marca, E. (2006): Técnicas de Inventario y Monitoreo para
resulting value of zero in all ecoregions supports our beta los Anfibios de la Región Tropical Andina. Bogotá, Colombia,
Panamericana Formas e Impresos.
diversity result, in which there is high species turnover
Antonelli, A., Zizka, A., Silvestro, D., Scharn, R., Cascales-
and a higher number of unique species in ecoregions.
Miñana, B., Bacon, C.D. (2015): An engine for global plant
Moreover, it is an indication that the records to date can diversity: highest evolutionary turnover and emigration in the
be considered complete in terms of the most common American tropics. Frontiers in Genetics 6: 130.
species that co-occur in Madidi and its surroundings. Bass, M.S., Finer, M., Jenkins, C.N., Kreft, H., Cisneros-Heredia,
However, this methodology underestimates rare or D.F., McCracken, S.F., et al. (2010): Global conservation
cryptic species (Lewis et al., 2017), so we still hope to significance of Ecuador’s Yasuní National Park. PLoS ONE
find new records for Madidi among those more elusive, 5(1): e8767.
Boulenger, G.A. (1882): Catalogue of the Batrachia Salientia s.
cryptic and/or rare species.
Ecaudata in the Collection of the British Museum. Second
Amphibians are currently considered one of the most Edition. London, UK, Trustees of the British Museum.
threatened vertebrate groups worldwide (IUCN, 2020). Burrowes, P.A., Navas, C.A., Jiménez-Robles, O., Delgado, P., De
Around 278 amphibian species have been reported in la Riva, I. (2020): Climatic heterogeneity in the Bolivian Andes:
Bolivia to date (De la Riva and Reichle, 2014; Köhler are frogs trapped? South American Journal of Herpetology 18:
and Padial, 2016; Pansonato et al., 2016; Caminer 1–12.
et al., 2017; Rivadeneira et al., 2018; de Fraga and Caminer, M.A., Ron, S.R. (2020): Systematics of the Boana
semilineata species group (Anura: Hylidae), with a description
Torralvo, 2019; Jansen et al., 2019; De la Riva, 2020),
of two new species from Amazonian Ecuador. Zoological
and the confirmed species list for Madidi represents
Journal of the Linnean Society 190(1): 149–180.
45.6% of this, making it the most important park for Caminer, M.A., Milá, B., Jansen, M., Fouquet, A., Venegas, P.J.,
amphibian conservation. Other megadiverse national Chávez, G., et al. (2017): Systematics of the Dendropsophus
parks in the Tropical Andes and Amazon Basin are leucophyllatus species complex (Anura: Hylidae): cryptic
Yasuní in Ecuador and Manu in Peru where, to date, diversity and the description of two new species. PLoS ONE
150 and 155 species of amphibians have been estimated 12(3): e0171785.
Catenazzi, A., Lehr, E., Von May, R. (2013): The amphibians and
to occur, respectively (Bass et al., 2010; Catenazzi et
reptiles of Manu National Park and its buffer zone, Amazon
al., 2013). However, these lists also include many
basin and eastern slopes of the Andes, Peru. Biota Neotropica
species that could potential be present but have not 13(4): 1–15.
yet been confirmed by formal records. Our research Colwell, R.K., Coddington, J.A. (1994): Estimating terrestrial
found 31 species registered outside of Madidi that biodiversity through extrapolation. Philosophical Transactions
could eventually enter the list of expected species for of the Royal Society B 345: 101–118.
the park. Due to the large area and elevational range Cortez-Fernandez, C. (2005): Herpetofauna de la zona norte del
Parque Nacional y Area Natural de Manejo Integrado Madidi
of the park, we are sure that not all amphibian species
(PNANMI-Madidi). Ecología en Bolivia 40(2): 10–26.
have been recorded yet, and more biodiversity studies
de Carvalho, T.R., Angulo, A., Barrera, D.A., Aguilar-Puntriano,
are needed to increase the list of species. This would C., Haddad, C.F.B. (2020a): Hiding in plain sight: a fourth
position Madidi as the most diverse protected area in new cryptic species of the Adenomera andreae clade (Anura:
terms of amphibian diversity. Leptodactylidae) from southwestern Amazonia. Herpetologica
76(3): 304–314.
Acknowledgements. We are grateful for the support of the National de Carvalho, T.R., Moraes, L.J.C.L., Lima, A.P., Fouquet, A.,
Protected Area Service (SERNAP) in facilitating our visits to Peloso, P.L.V., Pavan, D., et al. (2020b): Systematics and
Madidi National Park and Natural Integrated Management Area, historical biogeography of neotropical foam-nesting frogs
as well to the park rangers for their valuable contribution to the of the Adenomera heyeri clade (Leptodactylidae), with the
conservation of protected areas in Bolivia. We also acknowledge description of six new Amazonian species. Zoological Journal
the Wildlife Conservation Society (WCS) and the Gordon and of the Linnean Society 191(2): 395–433.
Betty Moore Foundation for their support to the Identidad Madidi de Carvalho, T.R., Simoes, P.I., Gagliardi-Urrutia, G., Rojas-
project, and the Bolivian Ministry of Environment and Water Runjaic, F.J.M., Haddad, C.F.B., Castroviejo-Fisher, S. (2020c):
and the Institute of Ecology that facilitated the execution of this A new forest-dwelling frog species of the genus Adenomera
project through the research permit: MMAYA/VMABCCGDF/ (Leptodactylidae) from northwestern Brazilian Amazonia.
DGBAP/UVSAP No. 354/2014. Copeia 108(4): 924–937.
384 Mauricio Ocampo et al.
de Fraga, R., Torralvo, K. (2019): New record of the fringed Hoorn, C., Palazzesi, L., Silvestro, D. (2022): Exploring the
leaf frog, Cruziohyla craspedopus (Anura: Phyllomedusidae) impact of Andean uplift and climate on life evolution and
extends its eastern range limit. Acta Amazonica 49(3): 208–212. landscape modification: from Amazonia to Patagonia. Global
De la Riva, I. (2007): Bolivian frogs of the genus Phrynopus, and Planetary Change 211: 103759.
with the description of twelve new species (Anura: Ibisch, P.L. (2003): Apuntes acerca de vacíos de protección en
Brachycephalidae). Herpetological Monographs 21: 241–277. Bolivia. In: Biodiversidad: la Riqueza de Bolivia. Estado
De la Riva, I. (2020): Unexpected beta-diversity radiations in de Conocimiento y Conservación, p. 391–417. Ibisch, P.L.,
highland clades of Andean Terraranae frogs. In: Neotropical Mérida, G., Eds., Santa Cruz de la Sierra, Bolivia, Editorial
Diversification: Patterns and Processes, p. 741–764. Rull, V., FAN.
Carnaval, A.C., Eds., Cham, Switzerland, Springer. Ibisch, P.L., Beck, S.G., Gerkmann, B., Carretero, A. (2003):
De la Riva, I., Reichle, S. (2014): Diversity and conservation of the Ecoregiones y ecosistemas. In: Biodiversidad: la Riqueza de
amphibians of Bolivia. Herpetological Monographs 28: 46–65. Bolivia. Estado de Conocimiento y Conservación, p. 47–88
De la Riva, I., Chaparro, J.C., Castroviejo-Fisher, S., Padial, J.M. Ibisch, P.L., and Mérida, G., Ed., Santa Cruz de la Sierra,
(2017): Underestimated anuran radiations in the high Andes: Bolivia, Editorial FAN.
five new species and a new genus of Holoadeninae, and their Identidad Madidi (2020): Informe de la Expedición Científica
phylogenetic relationships (Anura: Craugastoridae). Zoological Identidad Madidi 2017. Relevamientos de Biodiversidad en el
Journal of the Linnean Society 182(1): 129–172. Parque Nacional y Área Natural de Manejo Integrado Madidi.
Emmons, L.H. (1991): Observations on the herpetofauna. In: A La Paz, Bolivia, Wildlife Conservation Society.
Biological Assessment of the Alto Madidi Region and Adjacent Identidad Madidi, SERNAP (2017): Informe Científico 2015.
Areas of Northwest Bolivia, p. 74, Parker, T.A., III, Bailey, B., Relevamientos de Biodiversidad en el Parque Nacional y Área
Eds., Washington, D.C., USA, Conservation International. Natural de Manejo Integrado Madidi. La Paz, Bolivia, Wildlife
Esquerré, D., Brennan, I.G., Catullo, R.A., Torres-Pérez, F., Conservation Society.
Keogh, J.S. (2019): How mountains shape biodiversity: the role Identidad Madidi, SERNAP (2019): Informe de la Expedición
of the Andes in biogeography, diversification, and reproductive Científica Identidad Madidi 2016. Relevamientos de
biology in South America’s most species-rich lizard radiation Biodiversidad en el Parque Nacional y Área Natural de Manejo
(Squamata: Liolaemidae). Evolution 73(2): 214–230. Integrado Madidi. La Paz, Bolivia, Wildlife Conservation
Ferrão, M., Pimentel-Lima, A., Ron, S., dos Santos, S.P., Society.
Hanken, J. (2020): New species of leaf-litter toad of the Jansen, M., Santana, D.J., da Veiga-Teixeira, B.F., Köhler, G.
Rhinella margaritifera species group (Anura: Bufonidae) from (2019): A new striped species of Dendropsophus (Anura:
Amazonia. Copeia 108(4): 967–986. Hylidae) with a composite advertisement call and comments on
Fouquet, A., Martinez, Q., Zeidler, L., Courtois, E.A., Gaucher, the D. rubicundulus group. Vertebrate Zoology 69(3): 227–246.
P., Black, M., et al. (2016): Cryptic diversity in the Hypsiboas Köhler, J., Padial, J.M. (2016): Description and phylogenetic position
semilineatus species group (Amphibia, Anura) with the of a new (singleton) species of Oreobates Jiménez De la Espada,
description of a new species from the eastern Guiana Shield. 1872 (Anura: Craugastoridae) from the yungas of Cochabamba,
Zootaxa 4084(1): 79–104. Bolivia. Annals of the Carnegie Museum 84(1): 23–38.
Gallardo-Cruz, J.A., Pérez-García, E.A., Meave, J.A. (2009): Leary, S., Underwood, W., Anthony, R., Carter, S., Grandin,
β-Diversity and vegetation structure as influenced by slope T., Greenacre, C., et al. (2020): AVMA Guidelines for the
aspect and altitude in a seasonally dry tropical landscape. Euthanasia of Animals. 2020 Edition. Schaumburg, Illinois,
Landscape Ecology 24: 473–482. USA, American Veterinary Medical Association.
Guayasamin, J.M., Terán-Valdez, A. (2009): A new species of Lehr, E., Catenazzi, A. (2009): A new species of minute Noblella
Noblella (Amphibia: Strabomantidae) from the western slopes (Anura: Strabomantidae) from southern Peru: the smallest frog
of the Andes of Ecuador. Zootaxa 2161: 47–59. of the Andes. Copeia 2009(1): 148–156.
Hazzi, N.A., Moreno, J.S., Ortiz-Movliav, C., Palacio, R.D. Lewis, R.J., Szava-Kovats, R., Pärtel, M. (2016): Estimating dark
(2018): Biogeographic regions and events of isolation and diversity and species pools: an empirical assessment of two
diversification of the endemic biota of the tropical Andes. methods. Methods in Ecology and Evolution 7: 104–113.
Proceedings of the National Academy of Sciences USA Lewis, R.J., de Bello, F., Bennett, J.A., Fibich, P., Finerty, G.E.,
115(31): 7985–7990. Götzenberger, L., et al. (2017): Applying the dark diversity
Heyer, W.R., Donnelly, M.A., McDiarmid, R.W., Hayek, L.-A.C., concept to nature conservation. Conservation Biology 31(1):
Foster, M.S. (1994): Measuring and Monitoring Biological 40–47.
Diversity. Standard Methods for Amphibians. Washington, López-Gómez, A.M., Williams-Linera, G. (2006): Evaluación
D.C., USA, Smithsonian Institution Press. de métodos no paramétricos para la estimación de riqueza de
Hoorn, C., Wesselingh, F.P., ter Steege, H., Bermudez, M.A., Mora, especies de plantas leñosas en cafetales. Boletin de la Sociedad
A., Sevink, J., et al. (2010): Amazonia through time: Andean Botánica de México 78: 7–15.
uplift, climate change, landscape evolution, and biodiversity. Lötters, S., Köhler, J. (2000): A new toad of the Bufo typhonius
Science 330(6006): 927–931. complex from humid montane forests of Bolivia (Amphibia,
Hoorn, C., Mosbrugger, V., Mulch, A., Antonelli, A. (2013): Anura, Bufonidae). Spixiana 23(3): 293–303.
Biodiversity from mountain building. Nature Geoscience 6: Magurran, A.E. (2004): Measuring Biological Diversity. Oxford,
154. UK, Blackwell Science.
Amphibian Diversity in Madidi National Park and Natural Integrated Management Area 385
McCain, C.M., Sanders, N.J. (2010): Metabolic theory and Natural History Museum, University of Kansas.
elevational diversity of vertebrate ectotherms. Ecology 91(2): Rueda, J.V., Castro, F., Cortez, C. (2006): Técnicas para el
601–609. inventario y muestreo de anfibios: Una compilación. In:
Menéndez-Guerrero, P.A., Green, D.M., Davies, T.J. (2020): Técnicas de Inventario y Monitoreo para los Anfibios de la
Climate change and the future restructuring of neotropical Región Tropical Andina, p. 135–171. Angulo, A., Rueda-
anuran biodiversity. Ecography 43: 222–235. Almonacid, J.V., Rodríguez-Mahecha, J.V., La Marca, E., Eds.,
Milto, K.D., Barabanov, A.V. (2011): An annotated catalogue of Bogotá, Colombia, Conservación Internacional.
the amphibian types in the collection of the Zoological Institute, Salinas, E., Wallace, R.B. (2012): Conocimientos científicos
Russian Academy of Sciences, St. Petersburg. Russian Journal y prioridades de investigación en el Parque Nacional y Área
of Herpetology 18(2): 137–153. Natural de Manejo Integrado Madidi. La Paz, Bolivia, Servicio
Milutinović, T., Milanović, J., Stojanović, M. (2015): Application Nacional de Áreas Protegidas.
of species-richness estimators for the assessment of earthworm Seminara, G. (2006): Meanders. Journal of Fluid Mechanics 554:
diversity. Journal of Natural History 49(5–8): 273–283. 271–297.
Moravec, J., Lehr, E., Kodejš, K. (2020): A new species of Simmons, J.E. (2002): Herpetological Collecting and Collections
Pristimantis (Amphibia, Anura, Strabomantidae) from the Management. Revised Edition. Salt Lake Ciy, Utah, USA,
Pui Pui Protected Forest (central Peru), with comments on Society for the Study of Amphibians and Reptiles.
Pristimantis albertus Duellman & Hedges, 2007. ZooKeys Wallace, R., Ramírez, A., Salinas, E., Painter, L. (2017): Inspirando
994: 125–148. a la población urbana mediante información científica e
Pärtel, M., Szava-Kovats, R., Zobel, M. (2011): Dark diversity: imágenes de biodiversidad - Identidad Madidi. Ecología en
shedding light on absent species. Trends in Ecology and Bolivia 52(1): 1–6.
Evolution 26(3): 124–128.
Pansonato, A., Veiga-Menoncello, A.C.P., Mudrek, J.R., Jansen,
M., Recco-Pimentel, S.M., Martins, I.A., Strüssmann, C.
(2016): Two new species of Pseudopaludicola (Anura:
Leptodactylidae: Leiuperinae) from eastern Bolivia and
western Brazil. Herpetologica 72(3): 235–255.
Parris, K.M. (1999): Amphibian surveys in forests and woodlands.
Contemporary Herpetology 1999(1): 1–14.
Pérez, M.E., Pérez, J.M., Guerra, F., Cortez, C. (2002):
Herpetofauna del Parque Nacional Madidi. In: Informes de
las Evaluaciones Biológicas de Pampas del Heath, Perú, Alto
Madidi, Bolivia, y Pando, Bolivia, p. 58–65. Montambault,
J.R., Ed., Washington, D.C., USA, Conservation International.
Pérez-Bejar, M.E. (1997): Una evaluación preliminar de los
anfibios y reptiles de las Pampas del Heath (Provinvia Iturralde,
Departamento La Paz). Ecología en Bolivia 30: 43–54.
R Core Team (2022): R: a language and environment for statistical
computing, v4.2.1. Vienna, Austria, R Foundation for Statistical
Computing.
Remsen, J.V., Parker, T.A. (1995): Bolivia has the opportunity
to create the planet’s richest park for terrestrial biota. Bird
Conservation International 5: 181–199.
Reyes-Puig, C., Maynard, R.J., Trageser, S.J., Vieira, J., Hamilton,
P.S., Lynch, R., et al. (2020): A new species of Noblella
(Amphibia: Strabomantidae) from the Río Manduriacu Reserve
on the Pacific slopes of the Ecuadorian Andes. Neotropical
Biodiversity 6(1): 162–171.
Reyes-Puig, C., Guayasamin, J.M., Koch, C., Brito-Zapata, D.,
Hollanders, M., Costales, M., Cisneros-Heredia, D.F. (2021): A
new species of the genus Noblella (Amphibia: Strabomantidae)
from Ecuador, with new information for Noblella worleyae.
Acta Herpetologica 16(2): 63–87.
Rivadeneira, C.D., Venegas, P.J., Ron, S.R. (2018): Species limits
within the widespread Amazonian treefrog Dendropsophus
parviceps with descriptions of two new species (Anura,
Hylidae). ZooKeys 726: 25–77. Accepted by Tuliana Brunes
Rodriguez, L.O., Duellman, W.E. (1994): Guide to the Frogs of
the Iquitos Region, Amazonian Perú. Lawrence, Kansas, USA,
386 Mauricio Ocampo et al.
Appendix 1. Location of the Identidad Madidi study sites in Madidi National Park and Natural Integrated Management Area,
Bolivia. Sites where a 10-l bucket trap was used are indicated by an asterisk (*), those where the 60-l buckets were used by a
double asterisk (**).
Aguilar-Kirigin, A.J. (2012): Osteocephalus castaneicola Harvey, M.B., Sheehy, C.M. (2005): A new species of Ischnocnema
Moravec, Aparicio, Guerrero-Reinhard, Calderón, Jungfer & (Anura: Leptodactylidae) from La Paz, Bolivia. Herpetologica
Gvoždík, 2009 (Anura: Hylidae). Extensión de su distribución 61(3): 268–275.
geográfica y nuevo registro para el departamento de La Paz, Jungfer, K.-H., Faivovich, J., Padial, J.M., Castroviejo-Fisher,
Bolivia. Cuadernos de Herpetología 26(2): 107–109. S., Lyra, M.M., Berneck, B.V.M., et al. (2013): Systematics
Andersson, R.C. (1938): Batrachians from Burma collected by Dr. of spiny-backed treefrogs (Hylidae: Osteocephalus): an
R. Malaise, and from Bolivia and Ecuador collected by Dr. C. Amazonian puzzle. Zoologica Scripta 42(4): 351–380.
Hammarlund. Arkiv för Zoologi A 30: 1–24. Köhler, J., Koscinski, D., Padial, J.M., Chaparro, J.C., Handford,
Castroviejo-Fisher, S., Padial, J.M., Chaparro, J.C., Aguayo, R., P., Lougheed, S.C., De la Riva, I. (2010): Systematics of
De la Riva, I. (2009): A new species of Hyalinobatrachium Andean gladiator frogs of the Hypsiboas pulchellus species
(Anura: Centrolenidae) from the Amazonian slopes of the group (Anura, Hylidae). Zoologica Scripta 39: 572–590.
central Andes, with comments on the diversity of the genus in Lötters, S., Haas, W., Schick, S., Böhme, W. (2002): On the
the area. Zootaxa 2143: 24–44. systematics of the harlequin frogs (Amphibia: Bufonidae:
Cortez, C., Domic, E. (2007): Anfibios Comunes de San Miguel Atelopus) from Amazonia. II. Redescription of Atelopus
del Bala - Bolivia. La Paz, Bolivia, Conservación Internacional pulcher (Boulenger, 1882) from the eastern Andean versant in
Andes. Peru. Salamandra 38(3): 165–184.
de Fraga, R., Torralvo, K. (2019): New record of the fringed MacQuarrie, K., Bärtschi, A., Mittermeier, R. (2001): Donde los
leaf frog, Cruziohyla craspedopus (Anura: Phyllomedusidae) Andes Encuentran al Amazonas. Bahuaja-Sonene y Madidi,
extends its eastern range limit. Acta Amazonica 49(3): 208–212. Parques Nacionales de Perú y Bolivia. Barcelona, Spain, Jordi
De la Riva, I. (1990): Lista preliminar comentada de los anfibios Blassi.
de Bolivia con datos sobre su distribución. Bolletino Museo Ministerio de Medio Ambiente y Agua (2009): Libro rojo de la
Regionale di Scienze Naturali Torino 8(1): 261–319. Fauna Silvestre de Vertebrados de Bolivia. La Paz, Bolivia,
De la Riva, I. (2002): Taxonomy and distribution of the South Ministerio de Medio Ambiente y Agua.
American toad Bufo poeppigii Tschudi, 1845 (Amphibia, Morales, V.R. (1992): Dos especies nuevas de Dendrobates
Anura, Bufonidae). Graellsia 58(1): 49–57. (Anura: Dendrobatidae) para Perú. Caribbean Journal of
De la Riva, I. (2007): Bolivian frogs of the genus Phrynopus, Science 28(3–4): 191–199.
with the description of twelve new species (Anura: USNM [United States National Museum of Natural History] (2014):
Brachycephalidae). Herpetological Monographs 21: 241–277. Tambopata Reserve Survey. Available at: https://collections.
De la Riva, I. (2011): A new species of Atelopus (Anura: nmnh.si.edu/search/herps/?ark=ark:/65665/3c1f05e476a0c409f
Bufonidae) from the Amazonian slopes of the Andes in south- b48c1df6916d64f2#new-search. Accessed on 1 December 2014.
eastern Peru. Salamandra 47(3): 161–168. Padial, J.M., Bielskis, S., Castroviejo, J. (2000): Sobre los anfibios
De la Riva, I., Aparicio, J. (2016): Three new Bolivian species del Pie de Monte del Departamento de La Paz (Bolivia). Boletin
of Psychrophrynella (Anura: Craugastoridae), and comments de la Asociación Herpetológica Española 11(2): 59–62.
on the amphibian fauna of the Cordillera de Apolobamba. Padial, J.M., Castroviejo-Fisher, S., Merchan, M., Cabot, J.,
Salamandra 52(4): 283–292. Castroviejo, J. (2003): The herpetological collection from
De la Riva, I., Aparicio, J., Ríos, J.N. (2005a): New species of Bolivia in the “Estación Biológica de Doñana” (Spain).
Telmatobius (Anura: Leptodactylidae) from humid paramo of Graellsia 59(1): 5–13.
Peru and Bolivia. Journal of Herpetology 39(3): 409–416. Padial, J.M., Gonzáles, L., Reichle, S., Aguayo, R., De la
De la Riva, I., Ríos, J.N., Aparicio, J. (2005b): A new species Riva, I. (2004): First records of five species of the genus
of Bufo (Anura: Bufonidae) from the Andes of Bolivia. Eleutherodactylus Duméril and Bobron, 1841 (Anura,
Herpetologica 61(3): 280–286. Leptodactylidae) from Boliva. Graellsia 60(2): 167–174.
Duellman, W.E., de Sá, R.O. (1988): A new genus and species Padial, J.M., Gonzáles, L., De la Riva, I. (2005): A new
of South American hylid frog with a highly modified tadpole. species of the Eleutherodactylus discoidalis group (Anura:
Tropical Zoology 1: 117–136. Leptodactylidae) from Andean Humid Montane Forests of
Emmons, L.H. (1991): Observations on the herpetofauna. In: A Bolivia. Herpetologica 61(3): 318–325.
Biological Assessment of the Alto Madidi Region and Adjacent Padial, J.M., Reichle, S., McDiarmid, R., De la Riva, I. (2006):
Areas of Northwest Bolivia, p. 74. Parker, T.A., III, Bailey, B., A new species of arboreal toad (Anura: Bufonidae: Chaunus)
Eds., Washington, D.C., USA, Conservation International. from Madidi National Park, Bolivia. Zootaxa 1278: 57–68.
Foster, R.B., Carr, J.R., Forsyth, A.B. (1994): RAP6: the Padial, J.M., Chaparro, J.C., De la Riva, I. (2008): Systematics of
Tambopata-Candamo Reserved Zone of Southeastern Perú: a Oreobates and the Eleutherodactylus discoidalis species group
Biological Assessment. Washington, D.C., USA, Conservation (Amphibia, Anura), based on two mitochondrial DNA genes
International. and external morphology. Zoological Journal of the Linnean
GBIF [Global Biodiversity Information Facility] (2013): Society 152: 737–773.
Amphibia, Peru, Bolivia. Available at: https://www.gbif.org. Padial, J.M., Chaparro, J.C., Köhler, J., De la Riva, I. (2009):
Accessed on 23 May 2024. Rediscovery, resurrection and redescription of Rhinella
388 Mauricio Ocampo et al.
Appendix 2. Cont.