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Introduction
The Neotropics is the region with the greatest
biological diversity on the planet (Antonelli et al., 2015)
and home to about one third of the world’s amphibian
diversity (almost 3000 described species; Menéndez-
Guerrero et al., 2020). This incredible diversity is
mostly due to the rise of the Andes (Esquerré et al.,
2019; Hoorn et al., 2022), which created biogeographic
isolates and high endemism, particularly in the Amazon
Basin (Hazzi et al., 2018). In 2022, 152 new amphibian
species were described in the world, of which 25 were
from the Amazon Basin (AmphibiaWeb, 2023). The
protected areas of the Amazon Basin are therefore
very important for the conservation of this rich species
diversity in the future.
About 17% of Bolivia’s territory is included in 22
established national protected areas (Ibisch, 2003),
and Madidi National Park and Natural Integrated
Management Area (hereafter Madidi) includes the
largest representation of ecoregions and sub-ecoregions
(Ibisch et al., 2003). The Yungas ecoregion is the most
representative within the park, covering 42.88% of its
area (Ibisch, 2003), and includes the highest level of
amphibian endemism level in the country (De la Riva
and Reichle, 2014). Nevertheless, very few amphibian
surveys have been conducted in Madidi (Emmons,
1991; Pérez-Bejar, 1997; Pérez et al., 2002; Cortez-
Fernandez, 2005), and since there is such a diversity of
ecosystems represented in the park, it is likely that only
a small fraction of the true diversity has been reported.
The Identidad Madidi project (https://madidiid.org/en/)
carried out from 2015–2017 by the Wildlife Conservation
Society (WCS), aimed to record biodiversity and promote
environmental awareness in Madidi and elsewhere
(Identidad Madidi and SERNAP, 2017, 2019; Wallace et
al., 2017; Identidad Madidi, 2020). Based on eldwork
of the Identidad Madidi project, published reports, and
a survey of scientic collections, we here report the
most complete analysis of amphibian diversity in the
region, to increase knowledge across all the ecoregions
and altitudinal ranges of Madidi. We conducted
analyses of alpha, beta, gamma, and dark diversity to
better understand the richness within and among the
ecoregions, and thus communicate the importance of
conserving Madidi for Bolivia and the world.
Herpetology Notes, volume 17: 371-389 (2024) (published online on 09 June 2024)
Amphibian diversity in Madidi National Park and Natural
Integrated Management Area, Bolivia, one of the most
diverse parks in South America
Mauricio Ocampo1,2,*, James Aparicio1, Nuria Bernal Hoverud3, Enrique Domic3, and Robert B. Wallace3
1 Red de Investigadores en Herpetología - Bolivia, Avenida José
Aguirre 260, Los Pinos, Zona Sur, La Paz, Bolivia.
2 Unidad de Zoología, Instituto de Ecología, Universidad Mayor
de San Andrés, Casilla 10077, Correo Central, La Paz,
Bolivia.
3 Wildlife Conservation Society, Greater Madidi-Tambopata
Landscape Conservation Program, Calle Jaime Mendoza
987, Torre Soleil, San Miguel Calacoto, La Paz, Bolivia.
* Corresponding author. E-mail: mauiocampo@gmail.com
© 2024 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0.
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 eld work to
understand the alpha, beta, gamma, and dark diversity of amphibians in dierent ecoregions of Madidi. We conrmed the
presence of 127 amphibian species in the park. Diversity indices indicate that the ecoregions are quite dierent 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.
Keywords. Biodiversity survey, range extension, conservation, Tropical Andes, Bolivia.
Mauricio Ocampo et al.
372
Methods
Study area. Madidi covers an area of 18,957.4 km
2
including an elevational range between 180 m in the
Amazonian lowlands and 6044 m at the Chaupi Orco
mountain peak in the Andes. The park’s geographic
location in the Tropical Andes and headwaters
of the Amazon Basin, combined with the diverse
representation of ecoregions and altitudinal range,
suggests that Madidi could be the most biodiverse
protected area in Bolivia (Salinas and Wallace, 2012)
and even in the world (Remsen and Parker, 1995). Since
its creation as a protected area in September 1995,
Madidi conserves portions of six ecoregions: Sub-
Andean Amazon Forests, Pre-Andean Amazon Forests,
Cerrado Paceño, Yungas, Inter-Andean Dry Forests, and
High Andean Vegetation (Ibisch et al., 2003) (Fig. 1).
Baseline. We conducted a comprehensive literature
search of amphibian records from within Madidi
boundaries and close surroundings, including data
from publications, collections, technical reports, and
photographic records from the WCS photographic
database (https://bolivia.wcs.org). To be included in
the analysis, each record had to meet the requirement
of having reliable coordinates, which were veried
accompanying information and had to be congruent with
the known distribution of each species. The identication
of vouchers in Bolivian collections were veried and
corroborated to species level, and photographic records
were only used when there could be no doubt about their
taxonomic allocations. Throughout the process, we relied
on dichotomous keys, species descriptions, and online
data sources, such as the database Amphibians of the
World (https://amphibiansoftheworld.amnh.org), thus
creating a georeferenced baseline of conrmed species
and species recorded near the outer boundary of the park,
which could potentially be within the protected area.
We dened two buer areas (at 1-km and 50-km
distances) around the limits of the park. Species included
within the 1-km buer were considered as present in
the park, given the limited precision in georeferencing
localities in the past and the natural shifts in the riverbed
that dene the eastern and western borders in the
northern area of the park (Seminara, 2006). The 50-km
buer includes species that could possibly occur in the
park, which also added three additional ecoregions not
found within the strict limits of the park: Amazonian
Flood Forest, Pando Amazon Forest, and Llanos de
Moxos Flooded Savannah. The species recorded in
the second buer zone were used to estimate the “dark
diversity” of the park (i.e., accounting for all species in
the region that could potentially inhabit the protected
area; Pärtel et al., 2011).
Fieldwork. To increase the representation of
amphibian records, from 2015–2017 we surveyed 15
new sites located at an elevational range of 198–4814
m, covering all major ecoregions in the park (Fig. 1;
Appendix 1). We applied complete inventory techniques
(Heyer et al., 1994), including intensive diurnal and
nocturnal searches (usually two people for 16 h a day)
in possible refuges under rocks, logs, and leaf litter, as
well as in water bodies (Simmons, 2002). We also used
straight-line drift fences and pitfall traps (Parris, 1999),
which consisted of 10-m fencing and three buckets,
one at each end and a third in the middle (Rueda et al.,
2006). We used 60- and 10-l buckets depending on the
type of soil (Table 1). However, the substrate in the high
Andes is mostly rocky and with limited accessibility,
and this technique was not possible at all study sites.
Traps were active on all sampling days at each site
and were checked twice a day. We also included some
species whose call was recognized, even if the calling
individual was not captured.
A representative number of captured individuals were
euthanized with an overdose of sodium thiopental, xed
in formalin, and preserved in 70% ethanol (Angulo et
al., 2006; Leary et al., 2020). We deposited vouchers
in the Colección Boliviana de Fauna, La Paz, Bolivia
(CBF), and identied specimens through comparisons
with reference collections. These voucher specimens
represent a key resource for future taxonomic revisions.
Data analyses. We calculated alpha and beta diversity
from the data obtained during eldwork, since this
analysis requires abundance values. We plotted species
accumulation, samples-based rarefaction (i.e., 15 sites
sampled in Madidi), and individual-based rarefaction
curves. We calculated non-parametric species richness
estimators (Chao2, ACE, Jackknife2) that allowed us to
estimate the total number of species in our study area
from the eldwork data. The Chao2 estimator is based
on the number of rare species (species that are only
found in a few locations or on very few occasions) and
common species (species that are repeatedly found in
the sample). This method uses information about the
frequency of rare species to estimate the total number
of species, including those that have not been observed
in the sample. The ACE estimator is based on species
abundance, that is, the number of individuals of each
species present in the sample. It uses information about
rare and uncommon species that are present in the
sample but have not been observed frequently and uses
Amphibian Diversity in Madidi National Park and Natural Integrated Management Area 373
Figure 1. Map of the study area showing Madidi National Park and Natural Integrated Management Area, Bolivia (yellow line),
the 50-km buer area (light blue line), eldwork camps (stars), amphibian records from the database and eldwork (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).
Mauricio Ocampo et al.
374
this information to estimate the total number of species,
including those that have not been detected. Finally,
the Jackknife2 estimator is based on a resampling
approach, where a fraction of the data from the original
sample is sequentially removed. Then, the number of
species present in each of these smaller subsets of data
is calculated, and an estimation of the total richness is
obtained based on the variability among subsets. With
the calculation of these estimators, we will be able to
verify if sampling eort was sucient to estimate the
total richness obtained with the baseline and thus have
a better idea of the eort required to approach the actual
diversity of an area like Madidi.
For these analyses, we used the vegan package in R
v4.2.1 (R Core Team, 2022), and the functions rarefy,
where the sample is a vector with sequences every
50 individuals; the function specaccum, run with the
random method and 100 permutations; the function
estimateR to estimate ACE with the sample size; and
the function specpool to estimate Chao2 and Jackknife2
from the matrix.
For the beta diversity analysis, we measured
dissimilarity between ecoregions and sub-regions using
the BiodiversityR package, and we used the function
betadiver to calculate Whittaker’s Index, which shows
the relative dierence in species composition among
plots. The index is calculated as
βW = S/α − 1
where S is the total number of species and α is the
average number of species per site. A drawback of this
Table 1. Numbers of species found in the ecoregions of Madidi National Park, Bolivia, and surrounding, according to record
criteria. The rst numeric column lists the number of eective evaluation days spent in each surveyed ecoregion. Column headings
for the number of species found under the listed criterion include: FW – our eldwork; 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.
model is that S increases with sample size, while the
expectation of α remains constant, causing the beta
diversity to increase with sample size. A solution to this
problem is to study the beta diversity of pairs of sites.
We used a dendrogram and ternary diagram to visualize
the dissimilarities by ecoregions. The gamma diversity
is represented by all the species recorded in this study,
both inside and outside the park (those within a 50-
km buer). We measured the dark diversity from the
Beals Index on species co-occurrence likelihood with
95% condence (Lewis et al., 2016), which is more
accurate with far fewer negative mismatches. This
index provides new and complementary information
on species that should be present in an ecoregion and
that for unknown reasons could not be recorded. It
is calculated from the frequency of co-occurrence
with other species, providing a complementary list of
species with a reasonable degree of precision (Lewis
et al., 2017). We used the dark function in the vegan
package in R to conduct the analysis (R Core Team,
2022).
Results
Baseline. The total number of records was 2068 (557
inside Madidi, 1511 outside Madidi), representing
149 species, 114 inside Madidi, 121 in the buer
areas outside Madidi, and 82 shared species (Table 1,
Appendix 2). We also identied three putative new
species to science in the photographic records of WCS
(Table 2).
Ecoregion
Days
FW
BLI
BLO
Madidi
Gamma
Amazonian Flood Forest
-
-
-
34
-
34
Pando Amazon Forest
-
-
-
25
-
25
Sub-Andean Amazon Forests
44
21
78
57
81
92
Pre-Andean Amazon Forests
44
38
55
73
68
93
Cerrado Paceño
22
1
0
12
1
13
Llanos de Moxos Flooded Savannah
-
-
-
8
-
8
Yungas
72
18
35
56
46
80
Inter-Andean Dry Forests
15
11
12
-
16
16
High Andean Vegetation
12
5
8
9
12
19
Total
209
64
114
121
127
162
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 eldwork), 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.
Taxon
Rec
CS
AFF
SAF
PAF
PNF
CP
FSM
YU
IDF
HAV
FROGS
Aromobatidae
Allobates femoralis (Boulenger, 1884) bl LC
in bo
Allobates mcdiarmidi
(Reynolds & Foster, 1992)
bl
CR
in
ou
Allobates trilineatu s (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, 1 862)
bl
DD
ou
Rhinella exostosica Ferrão et al., 2020
bo
bo
bo
ou
ou
ou
bo
in
Rhinella fissipe s (Boulenger, 1903)
bl
DD
bo
ou
Rhinella leptosce lis (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 (L ötters & 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 (Cannatell a, 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 (Boulenge r, 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 trivitta ta (Spix, 1824)
bl
LC
ou
ou
Ranitomeya sirensis (Aichinger, 1991)
bl
LC
ou
ou
Hemiphra ctidae
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, 1 898)
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
Mauricio Ocampo et al.
376
Table 2. Cont.
Taxon
Rec
CS
AFF
SAF
PAF
PNF
CP
FSM
YU
IDF
HAV
Boana raniceps (Cope, 1862)
bl
LC
in
ou
Boana steinbachi (Boulenge, 1905)
bo
ou
bo
bo
ou
Dendropsophus acreanus (Bokermann, 1964)
bl
LC
ou
in
in
Dendropsophus arndti Caminer et al., 2017 bo
in bo ou
Dendropsophus bifurcus (Andersson, 1945)
bl
LC
in
ou
Dendropsophus delarivai
(Köhler & Lötters, 2001)
bl
LC
in
ou
Dendropsophus leali
(Bokermann, 1964)
bl
LC
in
ou
ou
Dendropsophus marmoratus (Laurenti, 1768) bl LC ou ou in
Dendropsophus melanargyreus (Cope, 1887) bl LC
in
Dendropsophus minutus (Peters, 1872) bl LC
in ou
Dendropsophus nanus (Boulenger, 1889) bl LC
in bo
Dendropsophus parviceps (Boulenger, 1882) bl LC
ou ou ou
Dendropsophus pauiniensis (Heyer, 1977) bl LC ou bo in
Dendropsophus rhodopeplus (Günther, 1858) bl LC
bo
ou
in
Dendropsophus riveroi (Cochran & Goin, 1970) bl LC
ou in
Dendropsophus rozenmani Jansen et al., 2019 bl
in
*Dendropsophus salli Jungfer et al., 2010
fw
in
Dendropsophus sarayacuensis (Shreve, 1935)
bl
LC
ou
in
ou
Dendropsophus schubarti (Bokermann, 1963) bl LC
in
Dryaderces pearsoni (Gaige, 1929)
bo
LC
ou
bo
bo
ou
Hyloscirtus armatus
(Boulenger, 1902)
bl
NT
bo
bo
Hyloscirtus charazani (Vellard, 1970) bl CR
ou ou
Lysapsus bolivianus Gallardo, 1961 bl DD
ou
Lysapsus limellum Cope, 1862 bl LC
ou
Osteocephalus buckleyi (Boulenger, 1882) bl LC ou bo
Osteocephalus leprieurii (Duméril & Bibron, 1841) bl LC ou ou ou
Osteocephalus taurinus Steindachner, 1862 bo LC ou bo bo
ou bo
Pseudis paradoxa (Linnaeus, 1758) bl LC
in
Scarthyla goinorum (Bokermann, 1862 ) bl LC
ou ou
Scinax castrovi ejoi De la Riva, 1993 bl LC
ou
Scinax chiquitanus (De la Riva, 1990)
bl
LC
bo
Scinax fuscomarginatus (Lutz, 1925)
bl
LC
bo
Scinax fuscovarius (Lutz, 1925)
bl
LC
in
Scinax garbei (Miranda-Ribeiro, 1926) bo LC
bo bo
ou
Scinax ictericu s Duellman & Wiens, 1993
bl
LC
ou
ou
ou
Scinax nasicus
(Cope, 1862)
bl
LC
in
Scinax pedromedinae (Henle, 1991) bl LC ou
Scinax ruber (Laurenti, 1768)
bo
LC
ou
bo
bo
ou
Scinax squalirostris (Lutz, 1925)
bl
LC
ou
Sphaenorhynchus lacteus (Daudin, 1800)
bl
LC
bo
ou
Trachycephalus coriaceus (Peters, 1867)
bl
LC
ou
ou
ou
Trachycephalus cunauaru Gordo et al., 2013
bl
in
Trachycephalus typhonius (Linnaeus, 1758)
bl
LC
bo
bo
ou
in
Leptodactylidae
Adenomera chicom endesi 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 lep todactyloides (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.
Taxon
Rec
CS
AFF
SAF
PAF
PNF
CP
FSM
YU
IDF
HAV
Leptodactylus mystaceus (Spix, 1824)
bo
LC
in
bo
in
Leptodactylus pentadactylus (Laurenti, 1768)
bo
LC
bo
bo
bo
Leptodactylus petersii (Steindachner, 1864)
bl
LC
ou
bo
ou
Leptodactylus podicipinu s (Cope, 1862) bl LC
in ou
Leptodactylus rhodomystax Boulenger, 1884
bo
LC
bo
bo
Leptodactylus rhodonotus
(Günther, 1869)
bo
LC
ou
ou
bo
in
Leptodactylus vastus
Lutz, 1930
bl
LC
in
Lithodytes lineatus (Schneider, 1799) bo LC
bo bo ou
in
Pleurodema marmoratum (Duméril & Bibron, 1840) bo VU
bo bo
Pseudopaludicola bolivia na Parker, 1927 bl LC
ou
Microhylidae
Chiasmocleis bassleri Dunn, 1949 bl LC
ou
Chiasmocleis ro yi (Morales, 2007) bl
ou
Chiasmocleis ventrimaculata (Andersson, 1945)
bl
LC
ou
Ctenophryne geayi Mocquard, 1904
bo
LC
ou
in
in
Elachistocleis helianne ae 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 Boule nger, 1902
bo
LC
bo
in
in
Phyllomedusa ca mba De la Riva, 1999 bl LC ou bo bo
ou
bo
Phyllomedusa vailla ntii 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 Ri va, 2007)
bl
CR
ou
Microkayla kallawaya (De la Riva & Martínez-Solano, 2007)
bl
CR
ou
Microkayla katan tika (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
Mauricio Ocampo et al.
378
Table 2. Cont.
Fieldwork. At the 15 sites surveyed, we gathered
272 records, corresponding to 64 species, 15 of which
represent new records for the park, seven of which are
also putative new species to science, and three are new
records for Bolivia. Eleven families were registered,
and the family Strabomantidae was represented by 16
species, the highest number of the survey (Tables 1, 2,
Appendix 3).
Alpha diversity. We recorded 64 species during
eldwork in Madidi (Table 1), and the intensive search
method was the most ecient (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
than what we obtained. The Chao 2 and Jackknife 2
estimators had a better t compared to the total list
obtained by including the baseline and eld work.
Beta diversity. The dissimilarity index shows
that Sub-Andean Amazon Forests and Pre-Andean
Amazon Forests are the most similar, while the High
Andean Vegetation and the Cerrado Paceño are unique
and completely dissimilar to all the other ecoregions
present in Madidi. The Inter-Andean Dry Forests are
more similar to Pre-Andean and Sub-Andean Amazon
Forests (Fig. 3).
Figure 3. Dendrogram of dissimilarities among ecoregions.
The colours correspond to the map, and the scale represents
the degree of dierence between ecoregions.
Taxon
Rec
CS
AFF
SAF
PAF
PNF
CP
FSM
YU
IDF
HAV
*,aPristimantis diadematus (Jiménez de la Espada, 1875) fw LC
in
Pristimantis fenestratus (Steindachner, 1864) bo LC ou bo bo ou ou
bo in
*
,aPristimantis lacrimosus
(Jiménez de la Espada, 1875)
fw
LC
in
in
Pristimantis ockendeni (Boulenger, 1912)
bo
LC
bo
Pristimantis pharangobat es (Duellman, 1978) bl LC
in
bo
Pristimantis plat ydactylus (Boulenger, 1903) bo LC
bo
bo
Pristimantis reichlei Padial & De la Riva, 2009 bo
in
in in
Pristimantis toftae (Duellman, 1978) bo LC ou
bo
Pristimantis ventrimarmoratus (Boulenger, 1912) bl LC
ou
ou
Yunganastes mercedesae (Lynch & McDiarmid, 1987)
bl
LC
in
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, 18 22)
bl
LC
in
ou
ou
Amphibian Diversity in Madidi National Park and Natural Integrated Management Area 379
Figure 2. Species accumulation curves developed from eldwork 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 eldwork and the species from the baseline.
The ternary diagram shows that more than half of
the pairwise comparisons between the ecoregions in
Madidi do not share any species (comparison 2, 3, 6,
7, 10, 12, 13, and 14), and that there are consistently
large dierences in the number of unique species (Fig.
4). The Sub-Andean Amazon Forests and Pre-Andean
Amazon Forests (Comparison 1) share the greatest
number of species, but still the index value is barely
a third. Therefore, we can infer that all the ecoregions
in Madidi include, for the most part, unique amphibian
species.
Gamma diversity. The total gamma diversity within
the nine ecoregions inside and outside Madidi is 162
species – including both baseline and eldwork data
(Table 1). Sixteen families were recorded throughout
the study, and the family Hylidae had the most
representation with 51 species. Five families were
represented by only one species, and the most diverse
genus was Dendropsophus with 17 species (Table 2).
Dark diversity. The dark diversity index was 0 for all
ecoregions, which means that there are no additional
species that should be recorded due to the high
probability of co-occurrence with others.
New records for the country. We report three new
country records at three separate localities, which we
describe in the following paragraphs.
Boana appendiculata (Boulenger, 1882).—Two
individuals were collected at Alto Madidi, a subadult
(CBF-7080) on 24 October 2015 at 13.6372°S,
68.7528°W, elevation 241 m (Fig. 5a), and a juvenile
(CBF-7081) on 29 October 2015 at 13.6363°S,
68.7516°W, elevation 264 m (Fig. 5b). We used the
following diagnostic characters to identify the species:
nely granular dorsal skin, brown dorsal coloration
with irregular dark brown markings that include an
irregular X-shaped mark in the scapular region, hidden
thigh surfaces with dark vertical stripes. This species
can be confused with B. geographica (Spix, 1824) but
diers from it by having yellow interdigital membranes
when alive, while B. geographica has red membranes
(Boulenger, 1882; Fouquet et al., 2016; Caminer and
Ron, 2020).
Pristimantis diadematus (Jiménez de la Espada,
1875).—One individual was collected at Sarayoj (CBF-
7452) on 16 September 2017 at 14.6193°S, 68.1939°W,
elevation 1328 m (Fig. 6a, b). The diagnostic characters
that conrmed species identity are: round head, smooth
dorsal skin with scattered tubercles, ngers without
webbing; rst nger shorter than second, digits end in
wide, truncated discs; dorsum brown with dark brown
longitudinal markings, groin and proximal anterior and
posterior surfaces of the thighs orange with dark brown
Mauricio Ocampo et al.
380
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
diagonal bars in the groin and horizontal bars in the
extremities, pale pink venter with dark spots (Fig. 6b).
This species can be confused with P. altamazonicus
(Barbour & Dunn, 1921), which diers by having a
truncated head, rough back, and dark belly (Rodriguez
and Duellman, 1994). Another very similar species is
P. sinschi Moravec et al., 2020, but this species has a
black groin (Moravec et al., 2020).
Pristimantis lacrimosus (Jiménez de la Espada,
1875).—One individual was collected at Mamacona
(CBF-7465) on 30 June 30 2016 at 14.4759°S;
68.1880°W, elevation 1621 m (Fig. 7). We used the
following diagnostic characters to identify the species:
smooth dorsal skin, granular belly; snout rounded, top
of the head at. 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 diers 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 eldwork in previously unsampled ecoregions.
With the Identidad Madidi project we were able to
increase knowledge of anuran diversity for Madidi
by 15.4%, and from our eldwork alone we were able
to record 50% of the amphibian diversity previously
reported for the park. Previous eorts had produced
a maximum of 43.2% of the conrmed amphibian
species (Emmons, 1991; Pérez-Bejar, 1997; Pérez et
al., 2002; Cortez-Fernandez, 2005). Since Identidad
Madidi was a three-year eort, it represents the most
complete survey to date, but also underlines that the
study of diversity in such heterogeneous environments
requires a long-term eort.
Figure 6. First record of Pristimantis diadematus for Bolivia from Sarayoj (CBF-7452). Photos by Mauricio Ocampo.
Figure 7. First record of Pristimantis lacrimossus for Bolivia
from Mamacona (CBF-7465). Photo by Mauricio Ocampo.
Mauricio Ocampo et al.
382
The collected specimens are very important for
identication since new morphological and molecular
analyses are regularly being published and gradually
help us better understand the true diversity of
ecosystems (Fouquet et al., 2007). For example, our
record of Boana appendiculata was originally assigned
to B. geographica until a recent taxonomic update
(Caminer and Ron, 2020) allowed us to conrm the
record as new to the Bolivian anurofauna. Similarly,
the species richness of the genus Microkayla in Madidi
is likely under-represented because each species has
a naturally restricted distribution. These frogs are
physiologically dependent on high levels of humidity,
and their small and robust bodies and short limbs give
them limited dispersal capacity (De la Riva et al., 2017;
Burrowes et al., 2020; De la Riva, 2020). For this
reason, De la Riva (2007) proposed that every valley
on the Amazonian slopes of the Andes with an adequate
patch of habitat could contain an endemic species (De
la Riva, 2007; Burrowes et al., 2020), so we are certain
that even more new species of this genus can be found
in Madidi.
The same situation occurs with the genus Noblella,
which is distributed from northern Ecuador to central
Bolivia, and dierent species have been found with a
separation of < 10 km (i.e., N. coloma and N. worleyae;
Guayasamin and Terán-Valdez, 2009; Reyes-Puig et al.,
2020). This highly endemic genus has a very restricted
distribution (Lehr and Catenazzi, 2009; Reyes-Puig et al.,
2021), and it contains the smallest species in the Andes
(11.4 mm on average body length in N. pygmaea Lehr
and Catenazzi, 2009). The dierences in designs and
coloration of the individuals we found in Madidi, along
with a distance greater than 130 km from the nearest
species (N. peruviana [Noble, 1921]), provide enough
evidence to suspect that it is a putative new species.
The true diversity of the genus Adenomera is just
becoming known, since eight new species were described
in the last three years (de Carvalho et al., 2020a–c). The
morphological dierences, overall colouration, and a
distribution restricted to the Cerrado Paceño, makes
our specimens (which we list as Adenomera sp.) quite
dierent from other known species. Similarly, the
morphological dierences we found in the individuals
of the genus Oreobates suggests that these specimens
could be members of an undescribed species. In all
cases, tissue samples from the putative new species
found in this study are being genetically analysed, and
with careful morphological comparisons, we will be
able to solidly test our hypotheses.
The taxonomy of Rhinella margaritifera (Laurenti,
1768) was uncertain for a long time, mainly because
the holotype was lost for over two centuries. In 2011
a specimen housed in the Academy of Sciences in St.
Petersburg, Russia, was identied as the holotype
of R. margaritifera, although the type locality
remains uncertain (Milto and Barabanov, 2011). This
provided greater clarity regarding the morphology
of R. margaritifera, allowing for the description and
validation of other species (Ferrão et al., 2020). In
Bolivia, R. stanlaii (Lötters and Köhler, 2000), a species
in the R. margaritifera group, had already been recorded
in the central part of the country (Lötters and Köhler,
2000), and the rest of records were identied as R. a.
margaritifera. However, Ferraõ et al. (2020) determined
that the records from the north and northwest of Bolivia
corresponded to a new species they described, R.
exostosica, characterized by poorly developed cephalic
crests, while individuals with well-developed cephalic
crests are still referred to as R. a. margaritifera. In our
evaluations, we encountered both types, and therefore,
we maintain the designation of R. a. margaritifera for
the individuals with developed crests.
One result that stood out was that the amphibian
diversity of the Inter-Andean Dry Forests was more
similar to the Pre- and Sub-Andean Amazonian Forest
than to the Yungas ecoregion, even though the Inter-
Andean Dry Forests are almost completely surrounded
by Yungas. The geography determines many factors
such as temperature, humidity, and isolation, which
have a physicochemical eect that will determine the
presence of the species (Gallardo-Cruz et al., 2009;
McCain and Sanders, 2010). However, the geological
and biogeographical history of the Inter-Andean Dry
Forests is not yet well understood, and more detailed
studies could eventually lead to the discovery of species
new to science. Our results show that although there are
some similarities between the diversity of ecoregions, in
general the dierences are predominantly greater. The
turnover in the composition of species is high, supporting
the concept that the uplift of the Andes has been working
as a species pump (Hoorn et al., 2010, 2013).
Numerous nonparametric estimators for species
richness have been proposed, and the most used are
Bootstrap, Jackknife1, Jackknife2, Chao1, Chao2,
ACE, and ICE (Magurran, 2004). However, these were
evaluated and compared by numerous studies, and most
agree that the best estimators are Jackknife2 and Chao2
(Colwell and Coddington, 1994; Magurran, 2004;
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
estimator to the total number of records in Madidi. The
estimation of species through the dark diversity index
allows us to complement the ecoregion’s list from
the co-occurrence of species (Lewis et al., 2016). The
resulting value of zero in all ecoregions supports our beta
diversity result, in which there is high species turnover
and a higher number of unique species in ecoregions.
Moreover, it is an indication that the records to date can
be considered complete in terms of the most common
species that co-occur in Madidi and its surroundings.
However, this methodology underestimates rare or
cryptic species (Lewis et al., 2017), so we still hope to
nd new records for Madidi among those more elusive,
cryptic and/or rare species.
Amphibians are currently considered one of the most
threatened vertebrate groups worldwide (IUCN, 2020).
Around 278 amphibian species have been reported in
Bolivia to date (De la Riva and Reichle, 2014; Köhler
and Padial, 2016; Pansonato et al., 2016; Caminer
et al., 2017; Rivadeneira et al., 2018; de Fraga and
Torralvo, 2019; Jansen et al., 2019; De la Riva, 2020),
and the conrmed species list for Madidi represents
45.6% of this, making it the most important park for
amphibian conservation. Other megadiverse national
parks in the Tropical Andes and Amazon Basin are
Yasuní in Ecuador and Manu in Peru where, to date,
150 and 155 species of amphibians have been estimated
to occur, respectively (Bass et al., 2010; Catenazzi et
al., 2013). However, these lists also include many
species that could potential be present but have not
yet been conrmed by formal records. Our research
found 31 species registered outside of Madidi that
could eventually enter the list of expected species for
the park. Due to the large area and elevational range
of the park, we are sure that not all amphibian species
have been recorded yet, and more biodiversity studies
are needed to increase the list of species. This would
position Madidi as the most diverse protected area in
terms of amphibian diversity.
Acknowledgements. We are grateful for the support of the National
Protected Area Service (SERNAP) in facilitating our visits to
Madidi National Park and Natural Integrated Management Area,
as well to the park rangers for their valuable contribution to the
conservation of protected areas in Bolivia. We also acknowledge
the Wildlife Conservation Society (WCS) and the Gordon and
Betty Moore Foundation for their support to the Identidad Madidi
project, and the Bolivian Ministry of Environment and Water
and the Institute of Ecology that facilitated the execution of this
project through the research permit: MMAYA/VMABCCGDF/
DGBAP/UVSAP No. 354/2014.
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Accepted by Tuliana Brunes
Mauricio Ocampo et al.
386
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 (**).
Site
Latitude
(°S)
Longitude
(°W)
Elevation
(m)
Ecoregions
Chokollo 14.7369 69.2156 4814 High Andean Vegetation
Puina Alto 14.6107 69.1372 4750 High Andean Vegetation
Puina Medio 14.6107 69.1372 4250 High Andean Vegetation
Puina Bajo 14.6107 69.1372 3837 High Andean Vegetation
Isañuyoj* 14.6288 69.0464 3460 Yungas
Chullina 14.6896 69.0514 2851 Yungas
Cargadero 14.5772 68.9778 2155 Yungas
Machariapo* 14.6921 68.2853 1763 Yungas
Mamacona 14.4697 68.1921 1566 Yungas
Sarayoj 14.6134 68.1924 1158 Yungas
Sipia* 14.4081 68.5475 740 Inter-Andean Dry Forest
Hondo Alto** 14.6335 67.8509 301 Sub-Andean Amazon Forest
Alto Madidi** 13.6332 68.7417 252 Sub- and Pre-Andean Amazon Forest
Heath Bosque** 13.0163 68.8520 198 Pre-Andean Amazon Forest
Heath Pampa** 12.9683 68.7383 198 Cerrado Paceño
Amphibian Diversity in Madidi National Park and Natural Integrated Management Area 387
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Mauricio Ocampo et al.
388
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Madidi, Bolivia, y Pando, Bolivia, p. 58–65 Montambault, J.R.,
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Appendix 2. Cont.
Amphibian Diversity in Madidi National Park and Natural Integrated Management Area 389
Appendix 3. Voucher numbers of specimens deposited in the Colección Boliviana de Fauna, La Paz, Bolivia (CBF). In the
list below, specimen numbers are CBF numbers with the exceptions of some specimens of Microkayla sp. 6 and Pristimantis
platydactylus, whose accession into the collection is pending and which are listed by their eld numbers.
Adenomera. chicomendesi: 7093–97, 7209, 7387–88, 7391; sp.
1: 7404–06, 7421–22.
Allobates. trilineatus: 7084–88.
Ameerega. hahneli: 7090; picta: 7024, 7058–59, 7200–01,
7205–06.
Boana. appendiculata: 7080–81; balzani: 6938–39, 6943,
6957,7215–17, 7228, 7457–60; boans: 7019–20, 7190, 7212;
calcarata: 7410, 7424, 7429; cinerascens: 7055–56; geographica:
7194–95, 7213–14; lanciformis: 7070, 7203, 7418, 7428, 7453–
54; steinbachi: 7072–74, 7082–83.
Callimedusa. tomopterna: 7066.
Ceratophrys. cornuta: 7432.
Cochranella. nola: 7229–31.
Ctenophryne. geayi: 7117, 7392.
Dendropsophus. arndti 7394; salli 7415.
Dryaderces. pearsoni: 7126.
Elachistocleis. helianneae: 7034, 7423.
Engystomops. freibergi: 7112–15, 7426–27, 7431.
Hamptophryne. boliviana: 7068–69, 7393, 7402.
Leptodactylus. didymus: 7060–65, 7407–08, 7412, 7433;
griseigularis: 7031–33, 7103–06, 7395, 7411, 7425, 7430;
mystaceus: 7030; pentadactylus: 7202; rhodomystax: 7052–54.
rhodonotus: 7025–26.
Lithodytes. lineatus 7049–51.
Microkayla. sp. 3: 7261, 7264, 7272–73, 7275, 7278; sp. 4:
7262, 7270, 7276; sp. 5: 7263, 7271, 7274, 7277; sp. 6: [eld
numbers JAE-1720–25, LJZH-30–34].
Nannophryne. apolobambica: 7258.
Noblella. sp. 1: 7242–45.
Oreobates. cruralis: 7116, 7191, 7199, 7239–40; sanderi:
7232–38; sp. 1: 6447, 6859, 6941–42, 6946, 6958, 7259–60.
Osteocephalus. taurinus: 7089, 7098, 7399.
Phyllomedusa. boliviana 7021–23, 7456; vaillantii 7067, 7204.
Pipa. pipa: 7214.
Pristimantis. altamazonicus: 7119–21, 7123; diadematus:
7452, 7463. fenestratus: 7027–29, 7099–102, 7109–11, 7124,
7207–08, 7389, 7396, 7400, 7417, 7419, 7455; lacrimosus: 7122,
7465; ockendeni: 6447, 6940, 6945, 6948–49, 7226–27, 7253–56,
7257; platydactylus: [eld number JAE-1710]; reichlei: 7091–92,
7220–25, 7246–7252; toftae: 7118.
Rhaebo. guttatus: 7057.
Rhinella. leptoscelis: 7193; major: 7403, 7420; a.
margaritifera: 7041–48, 7196–98, 7210–11, 7390, 7409;
marina: 7037, 7071, 7398; poeppigii: 7036, 7192; tacana: 7464;
veraguensis: 6937, 6944, 7035, 7218–19.
Scinax. garbei: 7107–08; ruber: 7076, 7079, 7125, 7397, 7401.