Amphibian conservation, land-use changes and protected areas: A
, Nicolás Urbina-Cardona
, Diego Baldo
, Julián Lescano
, Rafael Loyola
Centro de Zoología Aplicada, Facultad de Ciencias Exactas Físicas y Naturales, Universidad Nacional de Córdoba and Instituto de Diversidad y Ecología Animal —CONICET-UNC, Argentina
Conservation Biogeography Lab, Departmento de Ecologia, Universidade Federalde Goiás, Brazil
Department of Ecology and Territory, Faculty of Environmental and Rural Studies, Pontiﬁcia Universidad Javeriana, Bogota, Colombia
Laboratorio de GenéticaEvolutiva, Instituto de Biología Subtropical (CONICET-UNaM),Facultad de CienciasExactas Químicas y Naturales, UniversidadNacional de Misiones,N3300LQF Posadas,
Received 23 February 2015
Received in revised form 19 July 2015
Accepted 23 July 2015
Available online xxxx
Amphibians are undergoing a globalconservation crisis, and theyare one of the most underrepresented groups of
vertebrates in the global network of protected areas (PAs). In this study, we evaluated the ability of the world's
PAs to represent extant amphibian species. We also estimated the magnitude of the human footprint along the
geographic distributions of gap species (i.e., those with distributions totally outside PAs). Twenty-four percent
of species (n = 1535) are totally unrepresented, and another 18% (n = 1119) have less than 5% of their distribu-
tion inside PAs. Nearly half of all species with ranges under 1000 km
do not occur inside any PA. Furthermore,
more than 65% of the distribution of gap species is in human-dominated landscapes. Although the Earth's PAs
have greatly increased during the last ten years, the numberof unprotected amphibians has also grown. Tropical
countries in particular should strongly consider (1) the importance of using amphibians to drive conservation
policies that eventually lead to the implementation and management of PAs, given amphibians' extinction risk
and ability to act as bioindicators; (2) the effectiveness of national recovery plans for threatened amphibian spe-
cies; and (3) the need for increased funding for scientiﬁc research to expand our knowledge of amphibian spe-
cies. Meanwhile, data-deﬁcient amphibian species should receive a higher priority than they usually receive in
conservation planning, as a precautionary measure. Throughout this paper, we point out several challenges in
creating more comprehensive amphibian conservation strategies and opportunities in the next decade.
© 2015 Elsevier Ltd. All rights reserved.
Amphibians are undergoing a global conservation crisis characterized
by widespread species extinctions and population declines (Butchart
et al., 2010;IUCN, 2013), with more than 41% of the living amphibian spe-
cies currently considered to be threatened (Pimm et al., 2014). Although
this is a difﬁcult topic to address (Collins and Halliday, 2005; Scheffers
et al., 2012), forecasts of extinction risks in the group are not optimistic
(Hof et al., 2011; Sodhi et al., 2008; Wake and Vredenburg, 2008). Threats
include the synergistic effect of many extinction drivers, such as habitat
fragmentation and degradation, diseases and climate change (Stuart
et al., 2004; Gardner et al., 2007; Becker and Zamudio, 2011; Hof et al.,
2011). For all of these reasons, amphibians have become a high-priority
group for which conservation efforts have become focused (Pous et al.,
2010; Urbina-Cardona and Flores-Villela, 2010;Trindade-Filho et al.,
2012; Nori et al., 2013; Nori and Loyola, 2015).
Protected areas (PAs) cover about 13% of the Earth's terrestrial
surface (Bertzky et al., 2012), but several studies have revealed the
relative inefﬁciency of PAs in representing biodiversity in general
(Rodrigues et al., 2004a,b; Venter et al., 2014; Butchart et al., 2015;
Nori and Loyola, 2015; Sánchez-Fernández and Abellán, 2015). Am-
phibians are the group with the most species whose geographic
ranges are totally outside of the world's PAs. In particular, previous
research revealed that 17% of these species live completely outside
of PAs (Rodrigues et al., 2004b). Recent studies have further shown
that most threatened amphibian species are inadequately represent-
ed in PAs worldwide (Venter et al., 2014). In Europe, PAs do not rep-
resent amphibian species signiﬁcantly better than would be
expected by chance (Sánchez-Fernández and Abellán, 2015). In ad-
dition, many amphibian species have restricted geographic ranges,
highlighting the importance of choosing a scale that can be used to
develop more accurate conservation strategies for this group
(Cushman, 2006). Amphibians are rarely considered in conservation
policy decisions (Rodrigues et al., 2004b), and in some regions, prior-
ity areas for amphibian conservation do not spatially match the pri-
ority areas for other vertebrate groups (Urbina-Cardona and Flores-
Villela, 2010). Therefore, the underrepresentation of amphibians in
conservation decisions involving PAs is much more problematic for
range-restricted species that inhabit highly human-modiﬁed
Biological Conservation 191 (2015) 367–374
⁎Corresponding author at: Laboratório de BiogeograﬁadaConservação,Departmento
de Ecologia, Universidade Federal de Goiás, CP 131, CEP 74001-970, Goiânia, Goiás, Brasil.
E-mail address: firstname.lastname@example.org (R. Loyola).
0006-3207/© 2015 Elsevier Ltd. All rights reserved.
Contents lists available at ScienceDirect
journal homepage: www.elsevier.com/locate/bioc
Considering the global panorama of amphibian conservation,
previous studies were undertaken over 10 years ago (Rodrigues et al.,
2004a,b). However, these studies left out many details regarding am-
phibian conservation (e.g., the degree of protection at lower taxonomi-
cal levels within the group). Today, more information about the
distribution of many amphibian species is currently available (including
862 additional species), and the area of the planet's PAs has greatly in-
creased in the last ten years, from 11% to more than 13% of the world's
surface (IUCN and UNEP-WCMC, 2013). Consequently, it is now possi-
ble to incorporate other useful information into analyses, such as the
different types of land use within species' geographic ranges.
The overview presented above suggests that, currently, there is a gap
in information regarding amphibian representation inside the global
network of PAs and that, at the global scale, existing information is
out-of-date and lacking useful, speciﬁc details to support conservation
strategies. These reasons have motivated the present study, in which
we provide both a new and comprehensive overview of the global PA
network's ability to protect amphibian species and new information
about the overlap of amphibian geographic distributions with different
types of human land use. Additionally, we consider different taxa, con-
servation statuses and geographic regions, making special distinctions
for gap species and range-restricted species.
In particular, we aim to: (1) determine the proportion of represent-
ed amphibian species inside the world's PAs in different management
categories (according to the IUCN) for each taxonomic family by sepa-
rately evaluating all species and range-restricted species; (2) assess
the number of species unrepresented or poorly represented in PAs
and those species' locations; (3) assess the proportion of each amphib-
ian species' total distribution represented in PAs; (4) estimate the num-
ber of gap species per unit area for each continent and country;
(5) estimate the magnitude of human-modiﬁed landscapes inside the
geographic ranges of gap species; and, ﬁnally, (6) evaluate the conser-
vation status of gap species, especially the statusof range-restrictedspe-
cies that inhabit human-modiﬁed environments.
We obtained shape ﬁles for terrestrial PAs around the globe from the
World Database of Protected Areas website (IUCN and UNEP-WCMC,
2013). We selected only those PAs with “designated”status (i.e., we
did not consider “inscribed,”“non-reported,”or “proposed”PAs) from
all six management categories deﬁned by the IUCN (I to VI), totaling
126,280 PAs. Some PAs are not represented in the WDPA database, in-
cluding subregional and private PAs; we did not include these areas in
our study. It would be important to include these PAs in future studies
with similar analyses at regional scales.
To build the amphibian dataset, we downloaded vector ﬁles of range
maps for the 6316 species available in the IUCN database (IUCN, 2013),
which includes 86.5% of all extant amphibian species, according to Frost
(2014). These vector maps were generated and/or validated by experts
in each taxonomic group. They are available in the shapeﬁle format and
contain the known range of each species, depicted as polygons. Our re-
sults did not include taxonomic changes arising from the inclusive phylo-
genetic analysis of Brachycephaloidea (=Terrarana) undertaken by
Padial et al. (2014). Overall, the range maps accurately represent the
known distribution of most of the species included (Ficetola et al.,
2013), and they are useful and appropriate for global extent analyses.
However, their use implies the need to assume commission and omission
errors (mainly the former) in species distributions, especially in the trop-
ical areas of South America and Asia (Ficetola et al., 2013).
We also compiled data on each species' current conservation status
(IUCN, 2013) and its taxonomic order and family (Frost, 2013;
downloaded from Amphibian Species of the World 5.6, available at
http://research.amnh.org/vz/herpetology/amphibia/). Using ArcGis 10.2,
we joined this information with the range map of each species. We ob-
tained information about human impact on natural environments from
the “Anthropogenic Biomes of the World (v. 1)”website (http://
ecotope.org/anthromes/v1/guide/). Ellis and Ramankutty (2008) pro-
posed these biomes using different sources of information, such as land
use and human population density. The database offers 21 different cate-
gories of anthropogenic biomes in raster ﬁles. For this study, using a re-
classiﬁcation tool in ArcGis 10.2, we regrouped those 21 categories into
four. Our categories have a decreasing order of human population densi-
ty: (a) highly urbanized areas with up to 440 persons/km
, (b) rural vil-
lages and sparsely urbanized areas with up to 210 persons/km
(c) crop areas with up to 6 persons/km
and (d) wild areas with no per-
. These categories were modiﬁed from Brum et al. (2013),where
more details can be found. For another source of human inﬂuence on the
landscape, we extracted information on deforestation between 2000 and
2012 for each country from Hansen et al. (2013).
For each amphibian family, we calculated the percentage of species
(a) unrepresented in PAs (i.e., gap species), (b) only represented in PAs
under categories I to IV, which have speciﬁc conservation objectives,
and (c) represented in PAs under categories V and VI, which have no strict
biological conservation goals. We replicated these analyses considering
only species with geographic ranges smaller than 1000 km
restricted species; see Rodrigues et al., 2004a). There were 2323 total
range-restricted species, nearly 37% of our database.
We have calculated, shown and discussed thepercentageof overlap
between each species distribution and PAs. Hereafter, we refer to those
species whose ranges fall totally outside of PAs as “unrepresented”or
“gap”species. Following our reasoning, “represented”species are
those whose geographic distribution overlaps with PAs. To determine
both the number and location of gap species, we superimposed the PA
range polygons onto the geographic range map for each species, and
by implementing the “select by location tool”in ArcGis 10.2, we select-
ed those species that overlapped with at least onePA. Then, we inverted
this selection in order to select from all the gap species. The location of
each species was graphically represented as the centroid of their
Then, using ArcGis 10.2, we overlaid the polygons of gap species
with the political boundaries of countries and quantiﬁed the number
of species occurring in each country. Using this information, we were
able to calculate the number of gap species per unit area for each coun-
try. In order to determine the percentage of representation per species,
ﬁrst we calculated the area of each species' range and the area of that
range that overlaps with PAs. Finally, we calculated the proportion of
each species' range that is protected.
Finally, to determine the magnitude of human inﬂuence for eachgap
species' range, we calculated the percentage of each range occupied by
each of our four anthropogenic biome categories. We did this by
implementing the zonal statistic tool of ArcGis 10.2. In addition, we re-
trieved each gap species' IUCN threat status. We also investigated the
criteria IUCN used to classify these species under a given threat catego-
ry: critically endangered (CR), endangered (EN) and vulnerable (VU).
We calculated the percentage of species assigned to each threat catego-
ry and mapped them worldwide; we also replicated this analysis both
for gap species having more than 50% of their distribution ranges over-
lapping human-modiﬁed environments and for species with very re-
stricted ranges (i.e., smaller than 1000 km
The majority of described amphibian species are indeed represented
in PAs: 4781 species (75.69%). Furthermore, we found that 64% of
368 J. Nori et al. / Biological Conservation 191 (2015) 367–374
amphibianspecies (n = 4045) are represented in atleast one PA under
categories I to IV, while 11.6% (n = 732) of amphibian species can be
found only within PAs under categories V and VI. The remaining 24.4%
of species (n = 1535) are totally unrepresented in the global network
of PAs (Figs. 1–3).
Eighteen percent (n= 1119) of amphibian species haveless than 5%
of their distribution represented in PAs, and 22% of those (n = 240)
have less than 1% of their ranges protected. Many species (37%, n =
2350) have between 5% and 25% of their distribution protected, but
only 662 species (10.5%) have more than 50% of their ranges protected.
Of these most-protected species, the majority (n = 449) is range-
restricted (Fig. 2).
The only amphibian family totally unrepresented in PAs is the mono-
typic Nasikabatrachidae (Frost, 2013). All other families have at least half
of their species represented in at least one PA (Fig. 1a). Among range-
restricted species, 49% (n = 1145) are represented in at least one PA,
and 33.7% (n = 784) occur in PAs with categories I to IV. A total of 51%
of range-restricted species (n = 1180) are not represented in any PA.
Our results show that range-restricted species from the families of
Nasikabatrachidae, Conrauidae, Rhinatrematidae, Hemisotidae and
Ascaphidae are completely unprotected today. On the other hand, ﬁve
families have all of their range-restricted species represented in at least
one PA, and the families Leiopelmatidae, Limnodynastidae, Proteidae
and Sooglossidae are totally represented in PAs of categories I to IV
North America has 232 species (94% of those occurring there) repre-
sented in at least one PA, 84% of which are in PAs with categories I–IV.
Europe has 88% of its species (n = 82) represented in at least one PA,
with 84% of those in PA categories I–IV. The scenario is worse for Latin
America, which has 26% gap species (n = 832), and Asia, which has
20% gap species (n = 283). Ecuador, Colombia, Peru, Panama,
Guatemala and Papua New Guinea are the countries with the highest
number of gap species per unit of area (Fig. 3). Independent of country
borders, the areas with the greatest number of gap species are located in
the Andean mountain region (Peru, Ecuador and Colombia); southern
Mexico; eastern Brazil; Papua New Guinea and Indonesia; and parts of
Madagascar, Cameroon and southern India (see centroids in Fig. 4).
On average, the degree of spatial congruence between human-
modiﬁed landscapes and the geographic ranges of gap species is
65.4%. Nevertheless, this congruence is highly variable among regions.
Africa has the largest proportion of species affected by human-
induced alterations, and only 16% of its gap species' ranges were free
of human inﬂuence. Oceania, despite having one of the largest percent-
ages of gap species, also has the lowest level of human inﬂuence on spe-
cies' ranges, with 75% of its gap species' ranges falling outside human-
modiﬁed landscapes. Rural villages and sparsely populated areas were
the most common anthropogenic units inhabited by gap species on
this continent (Fig. 5).
Considering all gap species, 51% are currently classiﬁed as Data Deﬁ-
cient (DD), 16% as CR, 15% as EN and 7% as VU, according to the IUCN
(2013). Of the 585 threatened gap species (i.e., those classiﬁed as CR,
EN or VU), 424 (72%), were assigned to a threat category based on
IUCN's criterion B1, which considers species' extent of occurrence;
8.5% were assigned based on criterion B2, which considers species'
area of occupancy; and 13% were considered threatened under criterion
D2, which considers species' restricted areas of occupancy or locations
(for further details, see the IUCN categories at www.iucnredlist.org).
When considering only species that occur in areas with high human in-
ﬂuence, according to Ellis and Ramankutty (2008),w
sults: 47% of these species are categorized as DD, 20% are CR, and 18%
Fig. 1. Percentageof amphibian speciesin each family for range-restricted speciesand for all species. Greenbars stand for the percentage of speciesfound in at least one protectedarea (PA)
under strict protection (IUCNcategory I–IV),yellow stands for species foundin PAs under sustainableuse (IUCN categoryV–VI), and red standsfor the percentageof unprotectedspecies in
each family. Amphibian species: Pseudophilautus femoralis. (For interpretation of the references to color in this ﬁgure legend, the reader is referred to the web version of this article.)
369J. Nori et al. / Biological Conservation 191 (2015) 367–374
are EN. This pattern is also similar for range-restricted gap species: 55%
of these species are DD, 19% are CR, and 15% are EN (Figs. 2 and 4).
Our analyses revealed that almost 25% of all extant amphibian spe-
cies, more than 1500 in all, still remain totally outside PAs. Furthermore,
for some other species, only a small proportion of their total geographic
range lies within PAs. Continents harboringan abundance of gap species
(such as LatinAmerica, Asia and Africa; Fig. 3) are beinghighly impacted
by human activities (Fig. 5). It is important to highlight that our maps do
not consider mining and industrial development, activities that are
deemed harmful for amphibians (Becker and Zamudio, 2011). The on-
going modiﬁcation of landscapes by humans could negatively and irre-
versibly affect the survival of many taxa (Laurance et al., 2012).
Therefore, the overview presented here has critical implications for
both conservation actions and policy.
Despite the increase in the extentof terrestrial PAs in the last decade
(about 10% more area designated as protected and 13,000 additional
PAs), the proportion of amphibian species falling totally outside of PAs
has also increased.This pattern could bedue to the increase in taxonom-
ic description of new amphibian species (especially those with a limited
distribution), the split of widely distributed taxa into new species, and
the lack of available information on amphibian ecology and natural his-
tory (for a general discussion on this topic, see Diniz-Filho et al., 2013;
Oliver et al., 2013). However, this pattern also emphasizes that only a
few designated PAs provide an effective safeguard against extinction
for amphibians (Rodrigues et al., 2004a,b). In recent years, additional
private reserves not included in the WDPA database have been
established with the sole purpose of conserving amphibians (see the
Methods section); however, as threatened amphibian species are
often not the focus of conservation planning, this group is currently
not adequately represented (Venter et al., 2014).
It is worth noting the particular situation faced by amphibians in
central and western Africa (see also Nori and Loyola, 2015). In this re-
gion, on average, 84% of gap species have geographic ranges that overlap
with human-modiﬁed landscapes. Considering future scenarios of glob-
al change (Pereira et al., 2010; Dobrovolski et al., 2011; Hof et al., 2011),
opportunities to conserve species in highly disturbed regions could be
increasingly diminished due to the expansion of agricultural areas and
continued human modiﬁcation (Faleiro et al., 2013; Nori et al., 2013;
Dobrovolski et al., 2014). The implementation of conservation planning
protocols that consider amphibians is therefore urgently needed in
these areas. Postponing the implementation of these protocols could
delay and threaten the protectionof many amphibian gap species. Final-
ly, while considering future scenarios, it is important to highlight that
our analyses consider only the current distributions of species; howev-
er, it is known that global climate change is already affectingbiodiversi-
ty distribution patterns (Garciaet al., 2014). Hence, these c hanges might
have a strong effect in the representativeness of PAs (Araujo et al., 2004;
Ferro et al., 2014; Lemes et al., 2014; Loyola et al., 2014). Thus, ideally,
the mentioned conservation planning protocols should incorporate
the uncertainty associated with this particular threat in order to gener-
ate accurate and lasting policies.
While widely distributed families have, on average, a large percentage
of species that currently occur in at least one PA, those families with spe-
cies restricted to only a few regions exhibit extensive variation (from 0%
to 100%) in terms of protection by at least one PA. This result could either
be due to chance, given that these families contain a relatively small num-
ber of species, or it could be linked to the degree of human impact and the
level of protection found in species' native regions. This pattern is ex-
plained by the fact that well-represented range-restricted families
(i.e., those with bounded geographic coverage and a great proportion of
their species overlapping in PAs) are endemic to countries or regions
with large PAs, such as those found in the Amazon rainforest
(Allophrynidae), North America (Amphiumidae, Rhyacotritonidae, and
Sirenidae) or the Andean-Patagonian Forest (Calyptocephalellidae,
Fig. 2. Histograms showing the percentage of the distribution of thespecies included in PAs foreach species (A) and the numberof species assigned to eachIUCNstatuswhenconsidering
all species (B) and only the gap species (C). All the histograms discriminate range-restricted species. Amphibian species: Hemiphractus bubalus.
370 J. Nori et al. / Biological Conservation 191 (2015) 367–374
Rhinodermatidae). However, families with the largest percentage of
gap species are endemic to regions with little relationship between
the extent of PAs and amphibian species richness, such as the
Western Ghats in India (Nasikabatrachidae and Micrixalidae), the
tropical Andes (Rhinatrematidae and Telmatobiidae) and Southeast Asia
(Ceratobatrachidae) (Frost, 2014; IUCN, 2013; IUCN and UNEP-WCMC,
2013). Range-restricted species (and families) are highly vulnerable
(Villalobos et al., 2013)andthereforemustbeconsideredinconservation
policies (Rosenﬁeld, 2002; Whittaker et al., 2005).
In most countries that harbor a great number (and density) of gap
species, recent trends are not compatible with amphibian conservation.
For example, countries with tropical and subtropical forests in Asia
(including Indonesia and Thailand), Africa (including Angola, Zambia
and Congo), and Latin America (including Nicaragua and Bolivia) have
also recently suffered exceptionally high deforestation rates (Hansen
et al., 2013; see also Fig. 4). In addition, unfortunately, these countries
have experienced only a small increase in the extent of their PAs during
the same period (IUCN and UNEP-WCMC, 2013; see Supplementary
Fig. S1). Regions with the largest number and density of gap species
are located in species-rich countries that have areas identiﬁed as high
priority for conservation on the global scale (Mittermeier et al., 2004;
Brooks et al., 2006). Given the high irreplaceability of many PAs in
these regions, scientists have proposed a high level of protection and
encouraged global recognition for 137 current PAs as World Heritage
sites (Le Saout et al., 2013). Combining the results presented here
with those of previous studies (e.g., Rodrigues et al., 2004a,b), we sug-
gest that conservation efforts should be mainly focused on strategically
expanding the network of PAs in these species-rich countries, based on
the known conservation gaps, to ensure the protection of many gap
Accordingto the IUCN Red List of Threatened Species, many gap spe-
cies are highly threatened, and most of them are also range-restricted
(Fig. 2). However, our ﬁndings may be highly inﬂuenced by the
narrow distributions of these species. It is also noticeable than 45%
of gap species are currently classiﬁed as DD species by the IUCN and
that many of these species inhabit highly disturbed environments. Un-
fortunately, DD species are generally ignored or considered as species
of least concern in conservation policies, plans and recommendations
(e.g., Rodrigues et al., 2004a; Trindade-Filho et al., 2012; Le Saout
et al., 2013) even though many researchers have devoted their efforts
to showing that this could be a wrong decision (Trindade-Filho et al.,
2012; Morais et al., 2013; Howard and Bickford, 2014; Nori and Loyola,
Fig. 3. Map showing the number of unprotected species per unit areain the world's countries andpie charts with the percentage of species occurring in different protected area manage-
ment categories. This ﬁgure is illustrated with an amphibian species from each region: Eurycea latitance (NorthAmerica), Hemiphractus bubalus(Latin America), Ranapyrenaica (Europe),
Mantella aurantiaca (Africa), Helioporus australiacus (Oceania) and Philautus umbra (Asia).
371J. Nori et al. / Biological Conservation 191 (2015) 367–374
Fig. 4. Map showing the location (centroidof species' distribution) of unprotected species, their conservation status and the recentdeforestation in each country. This ﬁgure is illustrated
with an amphibian species from each region: Ascaphus montanus (North America), Melanophryniuscus krauczuki (Latin America), Calotriton arnoldi (Europe), Gracixalus supercornutus
(Asia), Litoria myola (Oceania) and Boophis andohahela (Africa).
Fig. 5. Percentage of spatial overlapbetween species'geographic rangeand different typesof human land use and the rate of deforestationper unit area in the world'scountries. Amphibian
species: Atelopus certus.
372 J. Nori et al. / Biological Conservation 191 (2015) 367–374
2015). Information regarding the geographic range of many DD species
is likely to be incomplete, andwe were not able to discriminate between
DD species that have been recently assessed and those that are DD due
to taxonomic problems. Hence, it is essential to increase ourknowledge
of many biological aspects of these species (such as taxonomy, system-
atics, demography, ecology, naturalhistory and threats) in order to gen-
erate adequate conservation policies (see Diniz-Filho et al., 2013).
We identiﬁed several key regions (such as part of thetropical Andes,
Southeast Asia and central Africa) in which the combined effect of deﬁ-
cits in the PA network and steady human inﬂuence will inevitably aggra-
vate the current crisis scenario for amphibians. Urgent conservation
policies, including governmental and social initiatives aimed at strategi-
cally expanding current PA networks, are needed (Ochoa-Ochoa et al.,
2009). Fortunately, many opportunities are available. The 10th United
Nations Convention on Biological Diversity Conference of the Parties,
which took place in October 2010 in Nagoya (Japan), resulted in an im-
pressive revised and updated Strategic Plan for Biodiversity Conserva-
tion that will last until 2020. The Parties made the bold commitment
to protect at least 17% of terrestrial and inland waters protected by
2020 (Butchart et al., 2010).
Major gaps in PA coverage preclude the protection of many species
and ecosystems, not just those of amphibians (Butchart et al., 2010;
Jenkins and Joppa, 2009; Le Saout et al., 2013). Thus, this international
agreement to expand the global network of PAs is timely. Nearly 13.6%
of the terrestrial land area is currently protected (Le Saout et al.,
2013), although the effectiveness of this protection has been disputed
(e.g., Jenkins and Joppa, 2009). Hence, there are still large opportunities
to achieve such a target by ﬁlling the gaps in the network. The scientiﬁc
community is workingtirelessly to take ﬁrm and decisive steps in order
to achieve these targets (Pimm et al., 2014; Rodrigues et al., 2004a;
Venter et al., 2014). The efforts of the scientiﬁc community must be ac-
companied by bilateral or multilateral institutions (e.g., World Bank and
UNEP) and NGOs, which will be indispensable when ﬁlling these gaps,
making it possible to develop improved policies for conservation of am-
phibians and other groups in a human-altered world.
Supplementary data to this article can be found online at http://dx.
This work was supported by “Escala Docente”of the Asociación de
Universidades Grupo Montevideo (AUGM) together with the Pro-
secretary of International Relations of National University of Córdoba
(UNC) and the Coordination Ofﬁce of International Affairs of Federal
University of Goiás (UFG). JN and JNL research has been funded by
MINCyT (PID 2010, proyecto #000113/2011), FONCyT (PICT-2013-
1607) and the Rufford Small Grants Foundation. RL research has been
constantly funded by CNPq (grants #308532/2014-7, 479959/2013-7,
407094/2013-0, 563621/2010-9) and the O Boticário Group Foundation
for the Protection of Nature (PROG_0008_2013). DB acknowledges
ANPCyT for their ﬁnancial support: PICTs 1524/2011, 1895/2011,
2687/2012, PIP 112201101/00875. PL has received a fellowship from
CNPq (grant #150480/2014-8). We thank two anonymous reviewers
and John Lamoreux for insightful comments on the manuscript. Thanks
also to Aaron Payne, Jodie Rowley, Jorge Brito, Milivoje Krvavac, Brian
Gratwicke, Frank Lemckert, Daniel Erickson and Benny Trapp for per-
mission to use the photos and illustrations in the ﬁgures. We are grateful
to John Karpinski for English edition.
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