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Amphibians are undergoing a global conservation crisis, and they are 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 distribution inside PAs. Nearly half of all species with ranges under 1000 km2 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 number of 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 species; and (3) the need for increased funding for scientific research to expand our knowledge of amphibian species. 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.
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Amphibian conservation, land-use changes and protected areas: A
global overview
Javier Nori
a
,PriscilaLemes
b
, Nicolás Urbina-Cardona
c
, Diego Baldo
d
, Julián Lescano
a
, Rafael Loyola
b,
a
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
b
Conservation Biogeography Lab, Departmento de Ecologia, Universidade Federalde Goiás, Brazil
c
Department of Ecology and Territory, Faculty of Environmental and Rural Studies, Ponticia Universidad Javeriana, Bogota, Colombia
d
Laboratorio de GenéticaEvolutiva, Instituto de Biología Subtropical (CONICET-UNaM),Facultad de CienciasExactas Químicas y Naturales, UniversidadNacional de Misiones,N3300LQF Posadas,
Argentina
abstractarticle info
Article history:
Received 23 February 2015
Received in revised form 19 July 2015
Accepted 23 July 2015
Available online xxxx
Keywords:
Aichi targets
Conservation assessment
Environmental policy
Gap analysis
Human impact
Population decline
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
2
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 scientic research to expand our knowledge of amphibian spe-
cies. Meanwhile, data-decient 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.
1. Introduction
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 difcult 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 inefciency 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 signicantly 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-modied
landscapes.
Biological Conservation 191 (2015) 367374
Corresponding author at: Laboratório de BiogeograadaConservação,Departmento
de Ecologia, Universidade Federal de Goiás, CP 131, CEP 74001-970, Goiânia, Goiás, Brasil.
E-mail address: loyola@ufg.br (R. Loyola).
http://dx.doi.org/10.1016/j.biocon.2015.07.028
0006-3207/© 2015 Elsevier Ltd. All rights reserved.
Contents lists available at ScienceDirect
Biological Conservation
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, specic 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-modied landscapes inside the
geographic ranges of gap species; and, nally, (6) evaluate the conser-
vation status of gap species, especially the statusof range-restrictedspe-
cies that inhabit human-modied environments.
2. Methods
2.1. Data
We obtained shape les 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 designatedstatus (i.e., we
did not consider inscribed,”“non-reported,or proposedPAs) from
all six management categories dened 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 les 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 shapele 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 les. For this study, using a re-
classication 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
2
, (b) rural vil-
lages and sparsely urbanized areas with up to 210 persons/km
2
,
(c) crop areas with up to 6 persons/km
2
and (d) wild areas with no per-
sons/km
2
. These categories were modied from Brum et al. (2013),where
more details can be found. For another source of human inuence on the
landscape, we extracted information on deforestation between 2000 and
2012 for each country from Hansen et al. (2013).
2.2. Analyses
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 specic 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
2
(i.e., range-
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 unrepresentedor
gapspecies. Following our reasoning, representedspecies 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 toolin 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
distribution.
Then, using ArcGis 10.2, we overlaid the polygons of gap species
with the political boundaries of countries and quantied 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,
rst 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 inuence 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-modied environments and for species with very re-
stricted ranges (i.e., smaller than 1000 km
2
).
3. Results
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) 367374
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. 13).
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, ve
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
(Fig. 1b).
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 IIV.
Europe has 88% of its species (n = 82) represented in at least one PA,
with 84% of those in PA categories IIV. 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-
modied 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 inuence. Oceania, despite having one of the largest percent-
ages of gap species, also has the lowest level of human inuence on spe-
cies' ranges, with 75% of its gap species' ranges falling outside human-
modied 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 classied as Data De-
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 classied 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-
uence, according to Ellis and Ramankutty (2008),w
efoundsimilarre-
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 IIV),yellow stands for species foundin PAs under sustainableuse (IUCN categoryVVI), and red standsfor the percentageof unprotectedspecies in
each family. Amphibian species: Pseudophilautus femoralis. (For interpretation of the references to color in this gure legend, the reader is referred to the web version of this article.)
369J. Nori et al. / Biological Conservation 191 (2015) 367374
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).
4. Discussion
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 modication 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-modied 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 modication (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) 367374
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 (Roseneld, 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 identied 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
species.
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 ndings may be highly inuenced by the
narrow distributions of these species. It is also noticeable than 45%
of gap species are currently classied 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 gure 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) 367374
Fig. 4. Map showing the location (centroidof species' distribution) of unprotected species, their conservation status and the recentdeforestation in each country. This gure 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) 367374
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 identied several key regions (such as part of thetropical Andes,
Southeast Asia and central Africa) in which the combined effect of de-
cits in the PA network and steady human inuence 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 lling the gaps in the network. The scientic
community is workingtirelessly to take rm 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 scientic community must be ac-
companied by bilateral or multilateral institutions (e.g., World Bank and
UNEP) and NGOs, which will be indispensable when lling 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.
doi.org/10.1016/j.biocon.2015.07.028.
Acknowledgments
This work was supported by Escala Docenteof the Asociación de
Universidades Grupo Montevideo (AUGM) together with the Pro-
secretary of International Relations of National University of Córdoba
(UNC) and the Coordination Ofce 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 nancial 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 gures. We are grateful
to John Karpinski for English edition.
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... Amphibians are facing severe global declines (Beebee and Griffiths 2005;Collins, Crump and Lovejoy III 2009;Stuart et al. 2008;Wake and Vredenburg 2008;WWF 2018), with about 40% of species threatened with extinction worldwide (Alroy 2015;Nori et al. 2015;Pimm et al. 2014;IUCN 2019). Multiple factors are related to this decline, the introduction of alien predators being one of the most important (Bucciarelli et al. 2014;Crossland et al. 2008;McGeoch et al. 2010;Nunes et al. 2019;Scheele et al. 2019;Winandy et al. 2015), especially for amphibian populations inhabiting mountain ranges (Denoël et al. 2016;Kats and Ferrer 2003;Wake and Vredenburg 2008). ...
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Amphibians inhabiting mountainous water bodies are frequently documented as the most affected by alien species, being trout one of the introduced aquatic predators that most affect them globally. Strikingly, there are some records of co-occurrence between native amphibians and introduced trout in the same water bodies. We intended to elucidate which variables at the landscape scale explain the occurrence of the endemic frog Boana cordobae in streams invaded by alien trout (Sierras Grandes, central Argentina). We surveyed mountainous streams occupied by alien trout, measuring landscape variables and recording the occurrence of B. cordobae and found co-occurrence in almost 20% of surveyed streams (n = 81). We used Generalized Linear Models and LASSO regression to relate amphibian occurrence in invaded streams to landscape composition and configuration variables. The presence of tussock grasslands around streams appears to be the most critical variable explaining co-occurrence between B. cordobae and trout in our study site. Our study contributes with specific elements relevant to consider for invaded streams management actions, suggesting that alien trout management should consider the spatial features surrounding streams to concentrate trout eradication efforts in sites where amphibian populations are more likely to recover.
... The fact that this productive activity development in this landscape presents the greatest accumulated species richness is particularly relevant for the conservation of amphibians in the Iberá region. In this sense, it should be noted that, currently, 25% of all known amphibian species are found outside the protected area perimeter (Nori et al., 2015), highlighting the importance of including productive areas of the private sector in the creation of preserved areas dedicated to biodiversity conservation (Borrini-Feyerabend et al., 2014;Stolton et al., 2014). In particular, the complexity in the articulation of conservation strategies between the public and the private sector, along with the complex socio-economic characteristics, demands the development of conservation strategies that aim towards a framework that preserves landscapes, regardless of ownership (Kamal et al., 2015). ...
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... We then relativized the direct protection raster on a scale of 0 -100, where 0 represented no formal landscape protection and 100 represented landscapes with the greatest landscape protection (Fig. 2), which corresponded with GAP status code 1. Although amphibian populations are under-represented under current global protected areas (Nori et al., 2015), protected areas with formal habitat protection are invaluable for eastern Hellbender conservation (Freake and DePerno, 2017). ...
... Las tres dimensiones evaluadas son la intensidad del suelo, el tiempo de intervención antrópica y la vulnerabilidad biofísica. Este método ha sido ampliamente usado para evaluar el cambio en los paisajes, y el potencial impacto que tiene el humano tanto en el hábitat de las especies como en su conectividad (Correa Ayram et al. 2017;Nori et al. 2015). ...
Book
El presente libro resume gran parte de los resultados del proyecto “Distribución histórica, actual y futura de mamíferos y sus relaciones e importancia sociocultural en el departamento de Cundinamarca: herramientas de planificación de conservación” desarrollado por la Corporación Universitaria Minuto de Dios y ProCAT Colombia, con financiamiento del Ministerio de Ciencia, Tecnología e Innovación (MinCiencias).
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Information obtained via individual identification is invaluable for ecology and conservation. Physical tags, such as PIT tags and GPS, have been used for individual identification; however, these methods could impact on animal behavior and survival rates, and the tags may become lost. Although non-invasive methods that do not affect the target species (such as manual photoidentification) are available, these techniques utilize stripes and spots that are unique to the individual, which requires training, and applying them to large datasets is challenging. Many studies that have applied deep learning for identification have focused on species-level identification, but few have addressed individual-level identification. In this study, we developed an image-based identification method based on deep learning that uses the head spot pattern of the Japanese giant salamander (Andrias japonicus), an endemic and endangered species in Japan. We trained and evaluated a dataset collected over two days from 11 individuals in captivity, which included 7075 images taken by a smartphone camera. Individuals were photographed three times a day at approximately 11:00 (morning), 15:00 (afternoon), and 18:00 (evening). As a result, individual identification by our method, which used the EfficientNetV2 achieved 99.86% accuracy, kappa coefficient of 0.99, and an F1 score of 0.99. Performance was lower for the evening model than for the morning and afternoon models, which were trained and evaluated using photographs taken at the corresponding time of the day. The proposed method does not require direct contact with the target species, and the effect on the animals is minimal; moreover, individual-level information can be obtained under natural conditions. In the future, smartphone images can be applied to citizen science surveys and individual-level big data collection, which is difficult using current methods.
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To identify the national hotspots for amphibians based on their richness and rarity and assess the effectiveness of the current protected areas for their conservation, we curated 1700 species occurrence points for 22 amphibians, including 16 species of Anura and 6 species of Caudata. We used these occurrence points along with bioclimatic, anthropogenic, and geographical variables to model the distribution of species. We then calculated richness and rarity maps of amphibians and identified the hotspots based on the top 10% of areas with the highest richness and rarity values. Finally, we overlaid the protected areas to evaluate the current coverage of hotspots and identify future conservation priorities. Although approximately 12% of the country is currently protected, our findings indicate that the current network of protected areas is considerably ineffective for the conservation of amphibians; over 90% of hotspots for amphibians lie outside the current national protected area network. The most important hotspots are located in the Caspian Hyrcanian Mixed Forest, the western margin of the North Zagros, and the Central Zagros Mountains Forest-Steppe ecoregions of the country. Among different types of protected areas that overlap with amphibian hotspots, protected areas, and wildlife refuges, respectively, ranked the highest in terms of quantity and size, while national parks ranked the lowest. In this study, we provided a baseline of top candidate areas for expanding protected areas where habitats can be managed to protect amphibians in Iran. To further improve the coverage of protected areas, we suggested priorities in Zagros Mountains Forest-Steppe hotspots.
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Climate change affects biodiversity, notably by modifying species habitats. In the West African savannahs, amphibian species are widespread. Despite their importance in ecosystems, little is known about the potential impacts of future climate change on these amphibians, hence the need to study the future distribution patterns of West African savannah amphibian species. We performed species distribution modelling to forecast the current and future distribution of two species Hyperolius nitidulus and Ptychadena bibroni in West Africa. Based on the global climate model MIROC5 and two future climate scenarios (RCP 4.5 and RCP 8.5), we assessed trends in the evolution of suitable habitat areas of these two amphibian species. We found that H. nitidulus is likely to lose significant proportions of their current habitats in the future due to climate change, while P. bibroni is likely to gain new suitable habitats. Our study suggests that some savannah amphibian species that are currently classified as Least Concern by the IUCN would be negatively affected by future climate change as shown by the distribution patterns of H. nitidulus . It is therefore necessary to consider all amphibian species, whether widely distributed or endemic, in future conservation strategies for amphibians in West Africa.
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Background and Research Aims: Globally, Colombia is the country with the largest extent of Páramos (delimited in 36 complexes) and with the greatest number of amphibian species in this ecosystem. This work consolidated scientific literature on the amphibians of the Colombian Páramos to characterize temporal, taxonomic, thematic, and geographic patterns, which allow us to identify information gaps that must be fulfilled to achieve effective species conservation. Methods: We conducted a systematic literature survey with seven different search strategies and generated a database. We read each document's Abstract, Methods, Study Area, Results, and supplementary material, following the PRISMA (Preferred Reporting Items for Systematic reviews and Meta-Analyses) protocol. Results: We found 405 documents published between 1863 and 2021. The composition and richness of 142 amphibian species (95 endemics to Colombia), presented significant differences in Páramo complexes and between sectors. Since 2000, the diversity of research topics has increased with a high proportion of studies on Natural History, Systematics and Taxonomy, and Conservation, distributed between 19 and 22 of the departments with Páramos in their jurisdiction. However, much of this knowledge concentrates in less than 20% of total species in just 6% of Páramos complexes. Conclusion: We found critical shortfalls in taxonomy, spatial information, and conservation actions on Páramos amphibians. We need to increase studies that include field data in more geographic areas and research topics, such as Population and Community ecology, Natural history (from a quantitative approach), Infectious disease, and Ecophysiology. Implications for Conservation: The scientific information gaps represent a challenge in generating effective strategies to conserve Páramo amphibians, considering the high degree of endemism and threats to these species. More than 80% of the Páramo amphibian species only have the information of their descriptions and little is known about their ecological requirements, population size, or data related to specific threats.
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The 'Data Deficient' (DD) category of the IUCN Red List assembles species that cannot be placed in another category due to insufficient information. This process generates uncertainty about whether these species are safe or actually in danger. Here, we give a global overview on the current situation of DD amphibian species (almost a quarter of living amphibians) considering land-use change through habitat modification, the degree of protection of each species and the socio-political context of each country harboring DD species. We found that DD amphibians have, on average, 81% of their ranges totally outside protected areas. Worryingly, more than half of DD species have less than 1% of their distribution represented in protected areas. Furthermore, the percentage of overlap between species' range and human-modified landscapes is high, at approximately 58%. Many countries harboring a large number of DD species show a worrying socio-political trend illustrated by substantial, recent incremental increases in the Human Development Index and lower incremental increases in the establishment of protected areas. Most of these are African countries, which are located mainly in the central and southern regions of the continent. Other countries with similar socio-political trends are in southeastern Asia, Central America, and in the northern region of South America. This situation is concerning, but it also creates a huge opportunity for considering DD amphibians in future conservation assessments, planning, and policy at different levels of government administration.
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Humans have fundamentally altered global patterns of biodiversity and ecosystem processes. Surprisingly, existing systems for representing these global patterns, including biome classifications, either ignore humans altogether or simplify human influence into, at most, four categories. Here, we present the first characterization of terrestrial biomes based on global patterns of sustained, direct human interaction with ecosystems. Eighteen "anthropogenic biomes" were identified through empirical analysis of global population, land use, and land cover. More than 75% of Earth's ice-free land showed evidence of alteration as a result of human residence and land use, with less than a quarter remaining as wildlands, supporting just 11% of terrestrial net primary production. Anthropogenic biomes offer a new way forward by acknowledging human influence on global ecosystems and moving us toward models and investigations of the terrestrial biosphere that integrate human and ecological systems.
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Governments have committed to conserving ≥17% of terrestrial and ≥10% of marine environments globally, especially “areas of particular importance for biodiversity” through “ecologically representative” Protected Area (PA) systems or other “area-based conservation measures,” while individual countries have committed to conserve 3–50% of their land area. We estimate that PAs currently cover 14.6% of terrestrial and 2.8% of marine extent, but 59–68% of ecoregions, 77–78% of important sites for biodiversity, and 57% of 25,380 species have inadequate coverage. The existing 19.7 million km2 terrestrial PA network needs only 3.3 million km2 to be added to achieve 17% terrestrial coverage. However, it would require nearly doubling to achieve, cost-efficiently, coverage targets for all countries, ecoregions, important sites, and species. Poorer countries have the largest relative shortfalls. Such extensive and rapid expansion of formal PAs is unlikely to be achievable. Greater focus is therefore needed on alternative approaches, including community- and privately managed sites and other effective area-based conservation measures.This article is protected by copyright. All rights reserved.
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Protected areas are a cornerstone of global efforts to conserve biodiversity. The Protected Planet Report 2012 reviews progress towards the achievement of international protected area targets through analysis of status and trends in global biodiversity protection. The resulting synthesis is a key source of information for decision makers and the conservation community.
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Climate change leads to species' range shifts, which may end up reducing the effectiveness of protected areas. These deleterious changes in biodiversity may become amplified if they include functionally important species, such as herbivores or pollinators. We evaluated how effective protected areas in the Brazilian Atlantic Forest are in maintaining the diversity of tiger moths (Arctiinae) under climate change. Specifically, we assessed whether protected areas will gain or lose species under climate change and mapped their locations in the Atlantic Forest, in order to assess potential spatial patterns of protected areas that will gain or lose species richness. Comparisons were completed using modeled species occurrence data based on the current and projected climate in 2080. We also built a null model for random allocation of protected areas to identify where reductions in species richness will be more severe than expected. We employed several modern techniques for modeling species' distributions and summarized results using ensembles of models. Our models indicate areas of high species richness in the central and southern regions of the Atlantic Forest both for now and the future. However, we estimate that in 2080 these regions should become climatically unsuitable, decreasing the species' distribution area. Around 4% of species were predicted to become extinct, some of them being endemic to the biome. Estimates of species turnover from current to future climate tended to be high, but these findings are dependent on modeling methods. Our most important results show that only a few protected areas in the southern region of the biome would gain species. Protected areas in semideciduous forests in the western region of the biome would lose more species than expected by the null model employed. Hence, current protected areas are worse off, than just randomly selected areas, at protecting species in the future.
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If the growing needs of humans are to be met, food production must increase; however, increasing food production will further compromise biodiversity. Can this seemingly irreconcilable conflict be mitigated? The solutions proposed so far include reducing food waste and closing yield gaps. Here, we investigate an alternative approach to reducing the impact of agricultural expansion on biodiversity without compromising food production by combining two strategies: taking agricultural production into consideration to solve the biodiversity crisis and promoting the definition of protected areas on the basis of a globalized blueprint. We found that combining these strategies could result in a 78% reduction in the agricultural opportunity costs incurred in the implementation of protected areas. Furthermore, a 30% increase in biodiversity protection could be achieved. We show that the movement toward global governance of natural resources would lead to reduced conflict between the needs of food production and biodiversity conservation.
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One of the main issues in conservation biology is assessing how much biodiversity is currently represented in protected areas (PA). Traditional approaches such as ‘gap analysis’ require the choice of arbitrary targets and thresholds that can greatly influence the obtained results. We present here a complementary approach that avoids typical methodological uncertainties being particularly useful when the aim is to explore differences in the effectiveness of PA networks in representing species with distinct features and varying range sizes. Firstly, we calculated how far the distribution of a species overlaps with a network. Then, null models were used to test if this value is significantly different from random expectations (i.e. compared with random species of the same number of occurrences), which allowed over and under-represented species to be identified. Using this approach, we aimed to determine how well amphibian and terrestrial reptile species in Europe were represented by two protected area networks: nationally designated protected areas (NPAs) and the Natura 2000 network (N2000). We also tested to see if there were any differences in species representation depending upon their conservation status, range size and distribution type. Although N2000 is more effective than NPAs, both PA networks performed poorly in representing European amphibians and reptiles, as the level of representativeness for most species (excepting reptiles in N2000) within these networks was either not significantly different or significantly lower than expected by chance. A combination of this approach with traditional gap analyses could provide valuable information to improve the future effectiveness of PAs.
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Padial et al. (2014) applied the name Pristimantinae Ohler & Dubois, 2012 to a taxon including the genera Ceuthomantis, Dischidodactylus, Pristimantis, and Yunganastes. However, Ceuthomantidae Heinicke, Duellman, Trueb, Means, MacCulloch & Hedges, 2009, type genus Ceuthomantis Heinicke, Duellman, Trueb, Means, MacCulloch & Hedges, 2009, has priority over Pristimantinae Ohler & Dubois, 2012, a fact that we overlooked and correct herein. Ceuthomantinae is thus the correct subfamily name for the taxon including Ceuthomantis, Dischidodactylus, Pristimantis, and Yunganastes, and Pristimantinae Ohler & Dubois, 2012 is its junior synonym. We provide an amended Figure 22 (page 50) reflecting the current classification of Brachycephaloidea as now listed in Frost (2014) and provide the pertinent correction to page 125 of Appendix 2, which should read as follows: