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Are protected areas effective in preserving anurans and promoting biodiversity discoveries in the Brazilian Cerrado?
Journal for Nature Conservation 52 (2019) 125734
Contents lists available at ScienceDirect
Journal for Nature Conservation journal homepage: www.elsevier.com/locate/jnc
Are protected areas effective in preserving anurans and promoting biodiversity discoveries in the Brazilian Cerrado?
T
Seixas Rezende Oliveiraa,⁎, Matheus Souza Lima-Ribeirob, Antonio Olímpio de Souzaa, Carolina Emília dos Santosa, Kauê Vergilio Silvaa, Marlon Zórteac, Frederico Augusto Guimarães Guilhermed, Fabiano Rodrigues de Meloc, Steffan Eduardo Silva Carneirod, Wilian Vaz Silvae, Alessandro Ribeiro Moraisf a
Programa de Pós-Graduação em Biodiversidade e Conservação, Instituto Federal Goiano, Campus Rio Verde, 75901-970, Cx Postal 66, Rio Verde, Goiás, Brazil Laboratório de Macroecologia, Instituto de Biociências, Regional Jataí, Universidade Federal de Goiás, 75801-615, Jataí, Goiás, Brazil Laboratório de Biodiversidade Animal, Instituto de Biociências, Regional Jataí, Universidade Federal de Goiás, 75801-615, Jataí, Goiás, Brazil d Unidade Acadêmica Especial de Ciências Biológicas, Universidade Federal de Jataí, BR 364, Km 192, CEP 75801-615, Jataí (GO), Brasil e Escola de Ciências Agrárias e Biológicas, Centro de Estudos e Pesquisas Biológicas, e Programa de Pós-Graduação em Ciências Ambientais e Saúde, Pontifícia Universidade Católica de Goiás – PUC Goiás. Av. Engler, s/n, Bloco L, Setor Jardim Mariliza, 74.885-460, Goiânia, Goiás, Brazil f Instituto Federal Goiano, Campus Rio Verde, Caixa Postal 66, 75.901-970 Rio Verde, Goiás, Brazil b c
A R T I C LE I N FO
A B S T R A C T
Keywords: Body size Species richness Geographical range Neotropical savanna
The current biodiversity crisis has stimulated the creation of protected areas, a fundamental conservation tool for halting biodiversity loss. Moreover, protected areas are often accessed by researchers for field observations and natural experiments, thus representing also an important tool promoting biodiversity discoveries. Here, we investigated the importance of protected areas in achieving both conservation and scientific roles for anurans in the Brazilian Cerrado. We specifically compared species richness, species geographical range size, time since species description, and species body size from 173 anurans between 18 protected and seven non-protected areas. We expect that conservation role would be fulfilled if higher species richness is represented into protected than non-protected areas. Similarly, if reserves are effective tools in promoting biodiversity discoveries, we expect a higher number of less detectable (narrow-ranged and small-bodied) and recently described species into protected areas. The estimated species richness was significantly higher in protected than non-protected areas (t = 12.82; df = 6; p < 0.001), whereas species geographic range (t = -3.24; df = 65.9; p = 0.002) and time since the species description (t = -2.49; df = 86.4; p = 0.015) were significantly lower. Species body size did not differ between areas. Our results indicate that reserves positively achieved the conservation role, and have been promoting scientific discoveries of new anurans in the Brazilian Cerrado. However, although favorable for most narrow-ranged anurans surviving, reserves are spatially relatively limited and isolated from each other, precluding large populations and gene flow. Our findings reinforce the need to increase the coverage of protected areas in the Brazilian Cerrado to continue maintaining a considerable number of species, but potentially expanding their geographical ranges and populations, as well as fully supporting biodiversity discoveries.
1. Introduction
2000; Marques & Nucci, 2007). Besides being a relevant tool for halting the loss of biodiversity (i.e. conservation role), PAs are often accessed by researchers for field observations and natural experiments, supporting biodiversity discoveries (Vitorino, V. do Carvalho, Fontes, de O. Barra, & Pereira, 2016). Thus, protected areas have also an important scientific role in reducing biodiversity knowledge shortfalls (Barata, Correia, & Ferreira, 2016). Indeed, the conservation and scientific roles mutually promote each other; while PAs favor researchers to improve
The growing human population have persistently altered the Earth’s surface and promoted a substantial biological annihilation over the last century (Barnosky et al., 2011; Ceballos, Ehrlich, & Dirzo, 2017). As a consequence, conservationists have been proposing a number of complementary measures to mediate the ongoing biodiversity crisis, including the creation of protected areas (PA) (Margules and Pressey,
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Corresponding author. E-mail address: [email protected] (S. Rezende Oliveira).
https://doi.org/10.1016/j.jnc.2019.125734 Received 30 October 2018; Received in revised form 9 April 2019; Accepted 13 August 2019 1617-1381/ © 2019 Elsevier GmbH. All rights reserved.
Journal for Nature Conservation 52 (2019) 125734
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Fig. 1. Geographical location of surveyed protected (green polygons) and non-protected areas (red dots). The identity of sampling units follows tables S1-S2 (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article).
biodiversity knowledge from pristine landscapes, the presence of field researchers benefit PAs by inhibiting improper users, such as poachers and encroachers (Laurance, 2013). In Brazil, the number and coverage of PAs have progressively grown over recent decades, but particularly restricted to the Amazon domain (Araújo, 2007; Cabral & Brito, 2013; Jenkins & Joppa, 2009). The Brazilian Cerrado, one of the 25 global biodiversity hotspots identified by Myers et al. (2000), presents a high concentration of endemic species, yet also experiencing increasing habitat loss in the last fifty years (Drummond, Franco, de, & de Oliveira, 2010). Around 46% of its original vegetation has already been converted into anthropogenic land cover (mainly cattle pastures and cash crops; Strassburg et al., 2017) and only 8.3% of its territory is legally protected (Françoso et al., 2015). Around 45.61% of PAs across Brazilian Cerrado are strictly designated for conservation purposes (i.e., Integral Protection Areas Group; SNUC 2000), while the remaining 54.39 permit sustainable use of the natural resource (i.e., Sustainable Use Areas Group; SNUC 2000), including private natural heritage reserves (RPPNs) (Françoso et al., 2015). Because sustainable use areas are less effective in preventing habitat loss (Françoso et al., 2015), together with the increasing anthropogenic pressures, about 290 animal species are now endangered
with extinction in the Brazilian Cerrado (ICMBio, 2018). Amphibians are among the most potentially human-threatened organisms (IUCN 2018). Their behavioral, ecological and physiological specificities (e.g., permeable skin and limited mobility) give them a reduced capacity to support and adapt to the human-altered landscapes (Navas, Bevier, & Carnaval, 2012). Currently, approximately 210 anuran species are known from the Brazilian Cerrado (Valdujo, Silvano, Colli, & Martins, 2012), although this is likely an underestimate of the potential true diversity given the cryptic nature of many taxa (Fouquet et al., 2007, [Fouquet et al., 2006]2006). Thus, PAs have long been expected to both maintain anurans and challenge its Linnaean shortfall (promote discoveries of new species) in Brazilian Cerrado (Bini, DinizFilho, Rangel, Bastos, & Pinto, 2006). Here, we investigated if protected areas have effectively been achieving the conservation and scientific roles for anurans in the Brazilian Cerrado. We compared species richness, species geographical range size, time since species description, and species body size from 173 anurans between 18 protected and seven non-protected areas. Because anurans are potentially sensitive to habitat conversion, we expect that conservation role would be fulfilled if protected areas keep considerably higher species richness than non-protected areas.
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of anuran species (species composition) from each protected area.
Similarly, if reserves are effective tools in promoting biodiversity discoveries, we expect a higher number of less detectable species (smallbodied and narrow-ranged), so recently described ones (Diniz-Filho et al., 2005), into than out of PAs. By showing favorable for most anurans surviving (165 species into vs. 54 species out of PAs), protected areas achieved its expected conservation role, but have partially been promoting discoveries of less detectable anurans in the Brazilian Cerrado; PAs significantly encompass narrower-ranged anurans and recently described species, but not smaller-bodied ones. We reinforce the need to increase the coverage of protected areas in the Brazilian Cerrado to effectively continue maintaining a considerable number of anuran species with larger populations and reducing their Linnaean shortfall.
2.2. Statistical analysis We built cumulative species curves to evaluate the effectiveness of sampling effort in satisfactorily representing the anurans biodiversity in our study. Three arrangements were adopted for this analysis: (i) total area (protected + non-protected areas), (ii) only protected areas, and (iii) only non-protected areas. To build cumulative species curves, we estimated species richness by using a first-order nonparametric Jackknife estimator, with 100 random repetitions, performed in Estimates 7.5 (Colwell, 2005). We established surveyed areas as units for statistical comparisons between protected and non-protected areas. Each protected area was considered a sampling unit from studies in literature, whereas each field area surveyed in this study was considered a sampling unit in nonprotected areas. Then, we used Student’s t-test to compare species richness, the time since the species description, geographical range size, and body size of the anuran species between protected and non-protected areas. To control the sampling effort and undesirable effects of species-area relationship, we compared species richness by accumulating equal numbers of protected and non-protected areas from Jackknife estimator.
2. Material and methods 2.1. Data sampling The lists of anuran species in protected and non-protected areas were obtained from both field and literature searches. Because inventories of anuran biodiversity into protected areas are more commonly available in the scientific literature, the fieldworks were intentionally developed to survey species in non-protected areas. For each species registered from the field and literature searches, we established the following information: the endemism level, from Valdujo et al. (2012); the time since the description of the species, from Frost (2018); the known current species range size, from IUCN (2018); and species body size (snout-vent length; SVL), from Oliveira et al. (2017). Field survey– we conducted field surveys between 2009 and 2017 at 59 sampling units across non-protected areas in seven municipalities (Jataí, Aporé, Itajá, Pilar de Goiás, Campo Alegre de Goiás, Catalão, and Aparecida do Rio Doce) of the Brazilian state of Goiás (Fig. 1, Table S1). The field sampling units entirely occurs into Brazilian Cerrado, which presents a tropical climate (AW from Köppen classification) with a welldefined rainy season from October to March, and a dry season from April to September. Anurans were sampled using complementary methods, including pitfall traps, active searches at breeding sites, and auditory censuses. To maximize the representativeness of anuran species in field surveys, we selected sampling units covering a considerable diversity of environments (e.g., different phytophysiognomies, ponds and streams) favorable to these animals occur (see Table S1). The pitfall traps were made from four 60-liter buckets, which were buried in the ground spacing 10 m from each other and arranged in a Y configuration (Cechin & Martins, 2009). The buckets were interlinked using a plastic mesh with 50 cm high and 35 m length, and checked every 24 h for specimens’ capture. The active searches at breeding sites and auditory censuses were conducted at the same sampling units, following the procedure proposed by Scott & Woodward (1994). Searches were systematically conducted during a period of 60 min between 18 h and 24 h. The observed individuals were visually taxonomically identified or their vocalizations were recorded for later taxonomical identification based on advertisement calls. Voucher specimens were gathered for each species; individuals were euthanized with 5% xylocaine, fixed in 10% formalin, and then conserved in 70% alcohol. All voucher specimens were deposited in the zoological collection at the Jataí campus of the Federal University of Goiás. Literature search - we performed the literature search in the Thompson ISI Web of Science (http://www.isiknowledge.com/), Scopus (https://www.scopus.com/), and Scielo (http://www.scielo. org/) databases to identify studies describing anurans biodiversity in protected areas across the Brazilian Cerrado. We specifically combined the terms “Cerrado anurans” and “anurans conservation unit” to assemble studies from each database. For each study, we gathered the list
3. Results A total of 18 studies related to our search criteria were identified from scientific literature between 2005 and 2016 (Table S2). These studies describe anurans biodiversity from 152 surveyed field localities into 18 protected areas, whereas we surveyed 59 sampling units across seven non-protected areas (Fig. 1; see also Tables S1-S2). The cumulative species richness curves for both protected and non-protected areas approached the asymptote (Fig. 2), indicating enough sampling effort to represent the anurans biodiversity of Brazilian Cerrado in our analyses. Overall, we recorded 173 anuran species belonging to 10 families, namely: Centrolenidae, Brachycephalidae, Bufonidae, Craugastoridae, Cycloramphidae, Dendrobatidae, Hylidae, Hylodidae, Leptodactylidae, and Microhylidae (Table S3). Of these species, 165 (from all 10 families) were recorded in protected areas, with an overall estimated richness of 222 species. The rarefied richness was estimated in 142.50 ± 16.33 (mean ± sd) species by randomly accumulating only seven protected areas. In non-protected areas, only 54 species were recorded, representing six families (Bufonidae, Craugastoridae, Dendrobatidae, Hylidae, Leptodactylidae, and Microhylidae), with an estimated richness of 68 species. A total of 62 species endemic to the Brazilian Cerrado were identified in this study, of which 58 were found
Fig. 2. Cumulative species richness curves for protected (green) and non-protected areas (red). Dotted line indicates the rarefied richness from seven protected areas (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article). 3
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areas in the Brazilian Cerrado, which would contribute to continue maintaining a significant diversity of anuran species, but also expanding their geographical ranges and, consequently, populations, as well as promoting biodiversity discoveries and scientific research of less detectable anurans. More extensive protected areas would increase the effectiveness of both conservation and scientific roles in the Brazilian Cerrado.
in protected areas, and only 16 in non-protected areas. The geographic range size of the species found in protected areas varied from 13.7 to 12,815,573.4 km2, while distribution size of species registered in non-protected areas varied from 494.6 to 12,815,573.4 km2. In protected areas, the time since the species description ranged from 8 to 260 years (100.35 ± 67.86), and species body size from 23 to 307 mm (71.93 ± 53.58). In non-protected areas, the time since the species description ranged from 15 to 250 years (127.2 ± 62.38), and species body size from 25 to 213 mm (64.75 ± 38.61). The estimated species richness was significantly higher in protected than non-protected areas (t = 12.82; df = 6; p < 0.001), whereas species geographic range size (t = -3.24; df = 65.9; p = 0.002) and time since the species description (t = -2.49; df = 86.4; p = 0.015) were significantly lower. Although opposing to our prediction (larger body size in protected than non-protected areas), species body size did not statistically differ between protected and non-protected areas (t = 0.92; df = 92.2; p = 0.36).
Acknowledgments FAG Guilherme, SRO and ARM are grateful to the Fundação de Amparo à Pesquisa do Estado de Goiás (CNPq/FAPEG - 2012/ 10267001108), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for their fellowships, respectively. We acknowledge CNPq, CAPES, FAPEG and Fundação Grupo O Boticário de Proteção à Natureza for the financial support to multiple grants from our research group. We thank the Ambiental consultoria, Estudos e Projetos support in obtaining data.
4. Discussion Appendix A. Supplementary data Except for body size, the findings corroborate all our predictions and indicate that protected areas fulfil both conservation and scientific roles regarding anuran diversity in the Brazilian Cerrado. Most known anuran species (n = 165) from the Brazilian Cerrado were predominantly found into protected areas (n = 18 protected areas). Because anurans are bio-indicators of environmental quality (Verdade et al., 2012) and generally require habitats with low levels of disturbance that guarantee access to feeding, reproduction, and vocalization sites (Wells, 2007), a considerable higher species richness into reserves indicates that protected areas have been offering suitable habitats and reflect relevant negative anthropogenic impacts across surrounding, non-protected areas. Additionally, the ecological determinants of anurans’ detectability (range and body size) (Diniz-Filho et al., 2005) partially contrast the protected and non-protected areas. Geographically restricted anurans are most likely present into reserves, but not smaller-bodied ones. Anyway, protected areas have supported discoveries of the newest-described anurans species across the Brazilian Cerrado. Protected areas retain higher diversity of habitats closer to its pristine conditions than human-altered landscapes, consequently, supporting species exploring its specific niches (Benton, Vickery, & Wilson, 2003; MacArthur & MacArthur, 2006). Particularly, the habitat heterogeneity at fine spatial scales better explains the local distribution of anurans than the size of reserves (Jorge, Simões, Magnusson, & Lima, 2016). Together, these aspects explain why most species, including the narrow-ranged anurans, preferentially occupy the protected areas across a biodiversity hotspot as the Brazilian Cerrado. Although achieving its overall conservation and scientific roles, our findings show actually a conflicting role of protected areas to safeguard anurans in the Brazilian Cerrado. First, while reserves benefit anurans by protecting natural habitats, their small and isolated areas may limit resources and gene flow. Species restricted to relatively small areas into reserves become generally more prone to extinction because of low resource availability, as well as demographic (e.g. Allee effect) and genetic consequences (e.g. inbreeding) (Thomas et al., 2004). Second, while protected areas favor the occurrence of locally distributed species (narrow-ranged), they do not promote smaller-bodied anurans. A higher fine-scale habitat heterogeneity may support narrow-ranged anurans, but the scarce resources across small reserves might not support the naturally dense populations from small-bodied species (Brown and Maurer, 1989). In conclusion, our findings elucidate that protected areas have been essential to preserve and research anurans across the Brazilian Cerrado in comparison with the surround, human-altered habitats. Additionally, the findings reinforce the need to increase the coverage of protected
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Contents lists available at ScienceDirect
Journal for Nature Conservation journal homepage: www.elsevier.com/locate/jnc
Are protected areas effective in preserving anurans and promoting biodiversity discoveries in the Brazilian Cerrado?
T
Seixas Rezende Oliveiraa,⁎, Matheus Souza Lima-Ribeirob, Antonio Olímpio de Souzaa, Carolina Emília dos Santosa, Kauê Vergilio Silvaa, Marlon Zórteac, Frederico Augusto Guimarães Guilhermed, Fabiano Rodrigues de Meloc, Steffan Eduardo Silva Carneirod, Wilian Vaz Silvae, Alessandro Ribeiro Moraisf a
Programa de Pós-Graduação em Biodiversidade e Conservação, Instituto Federal Goiano, Campus Rio Verde, 75901-970, Cx Postal 66, Rio Verde, Goiás, Brazil Laboratório de Macroecologia, Instituto de Biociências, Regional Jataí, Universidade Federal de Goiás, 75801-615, Jataí, Goiás, Brazil Laboratório de Biodiversidade Animal, Instituto de Biociências, Regional Jataí, Universidade Federal de Goiás, 75801-615, Jataí, Goiás, Brazil d Unidade Acadêmica Especial de Ciências Biológicas, Universidade Federal de Jataí, BR 364, Km 192, CEP 75801-615, Jataí (GO), Brasil e Escola de Ciências Agrárias e Biológicas, Centro de Estudos e Pesquisas Biológicas, e Programa de Pós-Graduação em Ciências Ambientais e Saúde, Pontifícia Universidade Católica de Goiás – PUC Goiás. Av. Engler, s/n, Bloco L, Setor Jardim Mariliza, 74.885-460, Goiânia, Goiás, Brazil f Instituto Federal Goiano, Campus Rio Verde, Caixa Postal 66, 75.901-970 Rio Verde, Goiás, Brazil b c
A R T I C LE I N FO
A B S T R A C T
Keywords: Body size Species richness Geographical range Neotropical savanna
The current biodiversity crisis has stimulated the creation of protected areas, a fundamental conservation tool for halting biodiversity loss. Moreover, protected areas are often accessed by researchers for field observations and natural experiments, thus representing also an important tool promoting biodiversity discoveries. Here, we investigated the importance of protected areas in achieving both conservation and scientific roles for anurans in the Brazilian Cerrado. We specifically compared species richness, species geographical range size, time since species description, and species body size from 173 anurans between 18 protected and seven non-protected areas. We expect that conservation role would be fulfilled if higher species richness is represented into protected than non-protected areas. Similarly, if reserves are effective tools in promoting biodiversity discoveries, we expect a higher number of less detectable (narrow-ranged and small-bodied) and recently described species into protected areas. The estimated species richness was significantly higher in protected than non-protected areas (t = 12.82; df = 6; p < 0.001), whereas species geographic range (t = -3.24; df = 65.9; p = 0.002) and time since the species description (t = -2.49; df = 86.4; p = 0.015) were significantly lower. Species body size did not differ between areas. Our results indicate that reserves positively achieved the conservation role, and have been promoting scientific discoveries of new anurans in the Brazilian Cerrado. However, although favorable for most narrow-ranged anurans surviving, reserves are spatially relatively limited and isolated from each other, precluding large populations and gene flow. Our findings reinforce the need to increase the coverage of protected areas in the Brazilian Cerrado to continue maintaining a considerable number of species, but potentially expanding their geographical ranges and populations, as well as fully supporting biodiversity discoveries.
1. Introduction
2000; Marques & Nucci, 2007). Besides being a relevant tool for halting the loss of biodiversity (i.e. conservation role), PAs are often accessed by researchers for field observations and natural experiments, supporting biodiversity discoveries (Vitorino, V. do Carvalho, Fontes, de O. Barra, & Pereira, 2016). Thus, protected areas have also an important scientific role in reducing biodiversity knowledge shortfalls (Barata, Correia, & Ferreira, 2016). Indeed, the conservation and scientific roles mutually promote each other; while PAs favor researchers to improve
The growing human population have persistently altered the Earth’s surface and promoted a substantial biological annihilation over the last century (Barnosky et al., 2011; Ceballos, Ehrlich, & Dirzo, 2017). As a consequence, conservationists have been proposing a number of complementary measures to mediate the ongoing biodiversity crisis, including the creation of protected areas (PA) (Margules and Pressey,
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Corresponding author. E-mail address: [email protected] (S. Rezende Oliveira).
https://doi.org/10.1016/j.jnc.2019.125734 Received 30 October 2018; Received in revised form 9 April 2019; Accepted 13 August 2019 1617-1381/ © 2019 Elsevier GmbH. All rights reserved.
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Fig. 1. Geographical location of surveyed protected (green polygons) and non-protected areas (red dots). The identity of sampling units follows tables S1-S2 (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article).
biodiversity knowledge from pristine landscapes, the presence of field researchers benefit PAs by inhibiting improper users, such as poachers and encroachers (Laurance, 2013). In Brazil, the number and coverage of PAs have progressively grown over recent decades, but particularly restricted to the Amazon domain (Araújo, 2007; Cabral & Brito, 2013; Jenkins & Joppa, 2009). The Brazilian Cerrado, one of the 25 global biodiversity hotspots identified by Myers et al. (2000), presents a high concentration of endemic species, yet also experiencing increasing habitat loss in the last fifty years (Drummond, Franco, de, & de Oliveira, 2010). Around 46% of its original vegetation has already been converted into anthropogenic land cover (mainly cattle pastures and cash crops; Strassburg et al., 2017) and only 8.3% of its territory is legally protected (Françoso et al., 2015). Around 45.61% of PAs across Brazilian Cerrado are strictly designated for conservation purposes (i.e., Integral Protection Areas Group; SNUC 2000), while the remaining 54.39 permit sustainable use of the natural resource (i.e., Sustainable Use Areas Group; SNUC 2000), including private natural heritage reserves (RPPNs) (Françoso et al., 2015). Because sustainable use areas are less effective in preventing habitat loss (Françoso et al., 2015), together with the increasing anthropogenic pressures, about 290 animal species are now endangered
with extinction in the Brazilian Cerrado (ICMBio, 2018). Amphibians are among the most potentially human-threatened organisms (IUCN 2018). Their behavioral, ecological and physiological specificities (e.g., permeable skin and limited mobility) give them a reduced capacity to support and adapt to the human-altered landscapes (Navas, Bevier, & Carnaval, 2012). Currently, approximately 210 anuran species are known from the Brazilian Cerrado (Valdujo, Silvano, Colli, & Martins, 2012), although this is likely an underestimate of the potential true diversity given the cryptic nature of many taxa (Fouquet et al., 2007, [Fouquet et al., 2006]2006). Thus, PAs have long been expected to both maintain anurans and challenge its Linnaean shortfall (promote discoveries of new species) in Brazilian Cerrado (Bini, DinizFilho, Rangel, Bastos, & Pinto, 2006). Here, we investigated if protected areas have effectively been achieving the conservation and scientific roles for anurans in the Brazilian Cerrado. We compared species richness, species geographical range size, time since species description, and species body size from 173 anurans between 18 protected and seven non-protected areas. Because anurans are potentially sensitive to habitat conversion, we expect that conservation role would be fulfilled if protected areas keep considerably higher species richness than non-protected areas.
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of anuran species (species composition) from each protected area.
Similarly, if reserves are effective tools in promoting biodiversity discoveries, we expect a higher number of less detectable species (smallbodied and narrow-ranged), so recently described ones (Diniz-Filho et al., 2005), into than out of PAs. By showing favorable for most anurans surviving (165 species into vs. 54 species out of PAs), protected areas achieved its expected conservation role, but have partially been promoting discoveries of less detectable anurans in the Brazilian Cerrado; PAs significantly encompass narrower-ranged anurans and recently described species, but not smaller-bodied ones. We reinforce the need to increase the coverage of protected areas in the Brazilian Cerrado to effectively continue maintaining a considerable number of anuran species with larger populations and reducing their Linnaean shortfall.
2.2. Statistical analysis We built cumulative species curves to evaluate the effectiveness of sampling effort in satisfactorily representing the anurans biodiversity in our study. Three arrangements were adopted for this analysis: (i) total area (protected + non-protected areas), (ii) only protected areas, and (iii) only non-protected areas. To build cumulative species curves, we estimated species richness by using a first-order nonparametric Jackknife estimator, with 100 random repetitions, performed in Estimates 7.5 (Colwell, 2005). We established surveyed areas as units for statistical comparisons between protected and non-protected areas. Each protected area was considered a sampling unit from studies in literature, whereas each field area surveyed in this study was considered a sampling unit in nonprotected areas. Then, we used Student’s t-test to compare species richness, the time since the species description, geographical range size, and body size of the anuran species between protected and non-protected areas. To control the sampling effort and undesirable effects of species-area relationship, we compared species richness by accumulating equal numbers of protected and non-protected areas from Jackknife estimator.
2. Material and methods 2.1. Data sampling The lists of anuran species in protected and non-protected areas were obtained from both field and literature searches. Because inventories of anuran biodiversity into protected areas are more commonly available in the scientific literature, the fieldworks were intentionally developed to survey species in non-protected areas. For each species registered from the field and literature searches, we established the following information: the endemism level, from Valdujo et al. (2012); the time since the description of the species, from Frost (2018); the known current species range size, from IUCN (2018); and species body size (snout-vent length; SVL), from Oliveira et al. (2017). Field survey– we conducted field surveys between 2009 and 2017 at 59 sampling units across non-protected areas in seven municipalities (Jataí, Aporé, Itajá, Pilar de Goiás, Campo Alegre de Goiás, Catalão, and Aparecida do Rio Doce) of the Brazilian state of Goiás (Fig. 1, Table S1). The field sampling units entirely occurs into Brazilian Cerrado, which presents a tropical climate (AW from Köppen classification) with a welldefined rainy season from October to March, and a dry season from April to September. Anurans were sampled using complementary methods, including pitfall traps, active searches at breeding sites, and auditory censuses. To maximize the representativeness of anuran species in field surveys, we selected sampling units covering a considerable diversity of environments (e.g., different phytophysiognomies, ponds and streams) favorable to these animals occur (see Table S1). The pitfall traps were made from four 60-liter buckets, which were buried in the ground spacing 10 m from each other and arranged in a Y configuration (Cechin & Martins, 2009). The buckets were interlinked using a plastic mesh with 50 cm high and 35 m length, and checked every 24 h for specimens’ capture. The active searches at breeding sites and auditory censuses were conducted at the same sampling units, following the procedure proposed by Scott & Woodward (1994). Searches were systematically conducted during a period of 60 min between 18 h and 24 h. The observed individuals were visually taxonomically identified or their vocalizations were recorded for later taxonomical identification based on advertisement calls. Voucher specimens were gathered for each species; individuals were euthanized with 5% xylocaine, fixed in 10% formalin, and then conserved in 70% alcohol. All voucher specimens were deposited in the zoological collection at the Jataí campus of the Federal University of Goiás. Literature search - we performed the literature search in the Thompson ISI Web of Science (http://www.isiknowledge.com/), Scopus (https://www.scopus.com/), and Scielo (http://www.scielo. org/) databases to identify studies describing anurans biodiversity in protected areas across the Brazilian Cerrado. We specifically combined the terms “Cerrado anurans” and “anurans conservation unit” to assemble studies from each database. For each study, we gathered the list
3. Results A total of 18 studies related to our search criteria were identified from scientific literature between 2005 and 2016 (Table S2). These studies describe anurans biodiversity from 152 surveyed field localities into 18 protected areas, whereas we surveyed 59 sampling units across seven non-protected areas (Fig. 1; see also Tables S1-S2). The cumulative species richness curves for both protected and non-protected areas approached the asymptote (Fig. 2), indicating enough sampling effort to represent the anurans biodiversity of Brazilian Cerrado in our analyses. Overall, we recorded 173 anuran species belonging to 10 families, namely: Centrolenidae, Brachycephalidae, Bufonidae, Craugastoridae, Cycloramphidae, Dendrobatidae, Hylidae, Hylodidae, Leptodactylidae, and Microhylidae (Table S3). Of these species, 165 (from all 10 families) were recorded in protected areas, with an overall estimated richness of 222 species. The rarefied richness was estimated in 142.50 ± 16.33 (mean ± sd) species by randomly accumulating only seven protected areas. In non-protected areas, only 54 species were recorded, representing six families (Bufonidae, Craugastoridae, Dendrobatidae, Hylidae, Leptodactylidae, and Microhylidae), with an estimated richness of 68 species. A total of 62 species endemic to the Brazilian Cerrado were identified in this study, of which 58 were found
Fig. 2. Cumulative species richness curves for protected (green) and non-protected areas (red). Dotted line indicates the rarefied richness from seven protected areas (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article). 3
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areas in the Brazilian Cerrado, which would contribute to continue maintaining a significant diversity of anuran species, but also expanding their geographical ranges and, consequently, populations, as well as promoting biodiversity discoveries and scientific research of less detectable anurans. More extensive protected areas would increase the effectiveness of both conservation and scientific roles in the Brazilian Cerrado.
in protected areas, and only 16 in non-protected areas. The geographic range size of the species found in protected areas varied from 13.7 to 12,815,573.4 km2, while distribution size of species registered in non-protected areas varied from 494.6 to 12,815,573.4 km2. In protected areas, the time since the species description ranged from 8 to 260 years (100.35 ± 67.86), and species body size from 23 to 307 mm (71.93 ± 53.58). In non-protected areas, the time since the species description ranged from 15 to 250 years (127.2 ± 62.38), and species body size from 25 to 213 mm (64.75 ± 38.61). The estimated species richness was significantly higher in protected than non-protected areas (t = 12.82; df = 6; p < 0.001), whereas species geographic range size (t = -3.24; df = 65.9; p = 0.002) and time since the species description (t = -2.49; df = 86.4; p = 0.015) were significantly lower. Although opposing to our prediction (larger body size in protected than non-protected areas), species body size did not statistically differ between protected and non-protected areas (t = 0.92; df = 92.2; p = 0.36).
Acknowledgments FAG Guilherme, SRO and ARM are grateful to the Fundação de Amparo à Pesquisa do Estado de Goiás (CNPq/FAPEG - 2012/ 10267001108), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for their fellowships, respectively. We acknowledge CNPq, CAPES, FAPEG and Fundação Grupo O Boticário de Proteção à Natureza for the financial support to multiple grants from our research group. We thank the Ambiental consultoria, Estudos e Projetos support in obtaining data.
4. Discussion Appendix A. Supplementary data Except for body size, the findings corroborate all our predictions and indicate that protected areas fulfil both conservation and scientific roles regarding anuran diversity in the Brazilian Cerrado. Most known anuran species (n = 165) from the Brazilian Cerrado were predominantly found into protected areas (n = 18 protected areas). Because anurans are bio-indicators of environmental quality (Verdade et al., 2012) and generally require habitats with low levels of disturbance that guarantee access to feeding, reproduction, and vocalization sites (Wells, 2007), a considerable higher species richness into reserves indicates that protected areas have been offering suitable habitats and reflect relevant negative anthropogenic impacts across surrounding, non-protected areas. Additionally, the ecological determinants of anurans’ detectability (range and body size) (Diniz-Filho et al., 2005) partially contrast the protected and non-protected areas. Geographically restricted anurans are most likely present into reserves, but not smaller-bodied ones. Anyway, protected areas have supported discoveries of the newest-described anurans species across the Brazilian Cerrado. Protected areas retain higher diversity of habitats closer to its pristine conditions than human-altered landscapes, consequently, supporting species exploring its specific niches (Benton, Vickery, & Wilson, 2003; MacArthur & MacArthur, 2006). Particularly, the habitat heterogeneity at fine spatial scales better explains the local distribution of anurans than the size of reserves (Jorge, Simões, Magnusson, & Lima, 2016). Together, these aspects explain why most species, including the narrow-ranged anurans, preferentially occupy the protected areas across a biodiversity hotspot as the Brazilian Cerrado. Although achieving its overall conservation and scientific roles, our findings show actually a conflicting role of protected areas to safeguard anurans in the Brazilian Cerrado. First, while reserves benefit anurans by protecting natural habitats, their small and isolated areas may limit resources and gene flow. Species restricted to relatively small areas into reserves become generally more prone to extinction because of low resource availability, as well as demographic (e.g. Allee effect) and genetic consequences (e.g. inbreeding) (Thomas et al., 2004). Second, while protected areas favor the occurrence of locally distributed species (narrow-ranged), they do not promote smaller-bodied anurans. A higher fine-scale habitat heterogeneity may support narrow-ranged anurans, but the scarce resources across small reserves might not support the naturally dense populations from small-bodied species (Brown and Maurer, 1989). In conclusion, our findings elucidate that protected areas have been essential to preserve and research anurans across the Brazilian Cerrado in comparison with the surround, human-altered habitats. Additionally, the findings reinforce the need to increase the coverage of protected
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