At What Point Do Amphibians Give Ecosystem Services
Sci Adv. 2017 Jun; three(half-dozen): e1602929.
Cost-effective conservation of amphibian ecology and development
Felipe South. Campos
aneDepartament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia, Universitat de Barcelona, ES-08028, Barcelona, Espana.
iiCoordination for the Improvement of College Education Personnel Foundation, Ministry building of Education of Brazil, 70040-020 Brasília, Distrito Federal, Brazil.
Ricardo Lourenço-de-Moraes
threeLaboratório de Herpetologia e Comportamento Animal, Departamento de Ecologia, Universidade Federal de Goiás, 74001-970 Goiânia, Goiás, Brazil.
Gustavo A. Llorente
1Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals, Facultat de Biologia, Universitat de Barcelona, ES-08028, Barcelona, Kingdom of spain.
Mirco Solé
4Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, 45662-000 Ilhéus, Bahia, Brazil.
Received 2016 Nov 22; Accepted 2017 Apr 28.
- Supplementary Materials
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http://advances.sciencemag.org/cgi/content/full/three/6/e1602929/DC1
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Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/3/6/e1602929/DC1
fig. S1. Plots of the relationships betwixt FD (Petchey and Gaston'south FD), PD (Religion's PD), TD, and TS of amphibians in the Brazilian Atlantic Woods.
fig. S2. Mismatch maps amongst FD (Petchey and Gaston'south FD), PD (Faith's PD), TD, and TS of amphibians in the Brazilian Atlantic Forest.
fig. S3. Spatial distribution of the PAs, the forest remnants outside of the PAs, and the very high priority sites covered by the proposed model 1 to amphibian conservation in the Brazilian Atlantic Wood.
fig. S4. Spatial distribution of the PAs, the wood remnants outside of the PAs, and the high-priority sites covered by the proposed model 2 to amphibian conservation in the Brazilian Atlantic Forest.
fig. S5. Spatial distribution of the PAs, the wood remnants exterior of the PAs, and the medium-priority sites covered by the proposed model 3 to amphibian conservation in the Brazilian Atlantic Forest.
fig. S6. Woods remnants and complementary fieldwork areas sampled in the Brazilian Atlantic Forest.
table S1. Results from the PERMANOVA on the land price-effectiveness by the FD (Petchey and Gaston's FD), PD (Organized religion's PD), TD, and TS of amphibians in the Brazilian Atlantic Forest.
table S2. Specific functions, ecosystem-supporting services, and references related to the amphibian functional traits assessed in the Brazilian Atlantic Forest.
data file S1. Functional traits and references for 453 amphibian species sampled in the Brazilian Atlantic Wood (.xlsx as a divide file).
data file S2. GenBank accession numbers for 207 amphibian species sampled in the Brazilian Atlantic Woods (.xlsx equally a split up file).
Abstract
Habitat loss is the most important threat to species survival, and the efficient selection of priority areas is central for good systematic conservation planning. Using amphibians as a conservation target, we designed an innovative assessment strategy, showing that prioritization models focused on functional, phylogenetic, and taxonomic variety can include cost-effectiveness–based assessments of state values. Nosotros report new primal conservation sites within the Brazilian Atlantic Wood hot spot, revealing a congruence of ecological and evolutionary patterns. We suggest payment for ecosystem services through environmental ready-asides on private land, establishing potential trade-offs for ecological and evolutionary processes. Our findings innovate additional effective area-based conservation parameters that set new priorities for biodiversity assessment in the Atlantic Wood, validating the usefulness of a novel approach to cost-effectiveness–based assessments of conservation value for other species-rich regions.
Keywords: Conservation planning, land cost-effective, biodiversity cess, Atlantic Forest hotspot, Amphibians
INTRODUCTION
Ecosystem functioning and evolutionary processes are usually linked, carrying a serial of short-term implications for ecological and human well-being (ane). The consequences of man activities get across species loss, with various studies as well reporting losses of functional traits and evolutionary history in various man-influenced landscapes (2). These losses are increasing demands for effective strategies on biodiversity conservation (3), which accept been also bailiwick to the incorporation of economical costs with the objective of providing more feasible conservation strategies on the ground (4). Given that habitat loss is the well-nigh of import threat to species survival, the protected sites chosen by conclusion makers determine what species and how many of these volition exist able to survive in nature (v). The effectiveness of these selected sites in achieving conservation goals depends on how well the ecological variety is represented in a given expanse (6). Several studies have focused on spatial prioritization to represent taxonomic multifariousness (TD), non highlighting the importance of capturing other biodiversity components, such as functional diverseness (FD) and phylogenetic diversity (PD) (7). Moreover, to date, their conservation strategies have been bullheaded to the functions these other components perform in a cost-constructive conservation policy.
FD is a biodiversity dimension that represents the extent of functional differences among species based on the stardom of their morphological, physiological, and ecological traits (8). PD adds value to theoretical and practical environmental studies by distinguishing species according to their evolutionary histories (9), reflecting the time and mode of divergence across the tree of life (10). In improver, FD and PD can better predict ecosystem part and stability than TD (xi, 12). Withal, using TD, FD, and PD in a simultaneous approach can help predict differential effects of contest and environmental filtering on the community assembly (thirteen). Nonetheless, consistency in the relationships between TD, FD, and PD can provide insights into the extent to which community assembly is driven past deterministic versus stochastic processes (xiv).
A cardinal question in community ecology and conservation biology is related to determining how biodiversity patterns tin can influence ecosystem functioning (xv–17). The key strategy to accost this issue is to assess the relationships betwixt functional and phylogenetic biodiversity components of the ecosystem (xi, eighteen). Understanding the associations between ecological similarity and phylogenetic relatedness amid species helps in the formulation of a hypothesis virtually the touch of evolutionary changes on functional environmental (19). Focusing on both functional and phylogenetic traits of a community can ameliorate our agreement of the consequences of biodiversity loss (20). Still, to describe how environmental actions can protect multiple dimensions of biodiversity, comparative methods on the consequences of species extinction in relation to ecological and evolutionary traits nonetheless need to be applied (21).
Approaches to setting conservation priorities recommend ranking ecosystems on several criteria, including level of endangerment and metrics of species value such as evolutionary distinctiveness, ecological importance, and social significance (21). On the other hand, these approaches accept not yet been implemented in practise and therefore remain every bit theoretical studies, not applied effectively in ecological landscape planning (22). Although the role of protected areas (PAs) in conserving biological communities is essential for natural systems (23), conservation planning needs to include the ecological functions performed by species that occur not only within PAs but too throughout the biome (24). In this context, environmental prepare-asides on private land accept been shown to be a promising strategy for conservation of species and ecological functions beyond farmlands (25). Nevertheless, set-asides of individual land for conservation generally come with economic costs to the landowners (26). Therefore, environmental strategies that contain payment for ecosystem services (Pes) can provide an efficient tool for increasing landowner participation in conservation programs (25). This strategy'due south feasibility is reflected in the e'er-increasing number of PES projects around the earth (27, 28). Despite this trend, almost PES projects are relatively local initiatives that may not fairly correspond the full range of conservation needs and economical issues observed throughout biodiversity hot spots (28). On the other paw, many ecology organizations are developing systematic planning tools to assist identify opportunities that offer the greatest render on investment in biodiversity protection (29). In a conservation context, this investment can exist indicated by cost-effectiveness–based estimates of land values, that is, the merchandise-off between biodiversity gains and economical costs of paying landowners to participate in set-aside programs (26).
A conservation dilemma arises from the question of how much cost and which biodiversity components should be chosen in large-scale conservation programs. This context suggests a demand for evolution of conservation plans that optimally residue economical costs and ecological constraints (30). Notwithstanding, constructive conservation plans should also have into account the maintenance of functional and evolutionary processes every bit a justification for investments, mainly in biodiversity hot spots (31–33). Here, we explore how FD, PD, and TD are distributed in the about endangered biodiversity hot spot on Earth—the Brazilian Atlantic Forest (34)—focusing on the most threatened vertebrate group worldwide, amphibians (35). Given that spatial patterns of diversity and distribution of tropical amphibians are a consequence of their ecological and phylogenetic relations (36), we conducted a spatial prioritization of conservation direction for the biodiversity components FD, PD, and TD, concerning threatened species (TS), PAs, and their respective state cost-effective values. We centered our land cost-effective estimations on the boilerplate Foot values of $13,273 for each foursquare kilometer given annually to the private forest landowners in the Brazilian Atlantic Forest (26, 28). We aimed to comprise the functions that amphibians perform with price-constructive considerations, exploring adequate conservation models that can allow us to preserve endangered species at a depression cost. Therefore, we report for the first fourth dimension that the pick of priority sites based on PD and FD can be extended to include non only high species richness and threatened taxonomic groups but also land cost-effective outcomes.
RESULTS
Our results revealed a high FD and PD in the eastern Atlantic Forest, with the highest rates in the east central region rising to the northeast (Fig. 1, A and B). We establish high correlations between TD with FD and PD (r 2 = 0.86, P < 0.001 and r 2 = 0.82, P < 0.001, respectively) (fig. S1, A and B). Still, we observed that the values of FD and PD significantly differ from the random expectation of the nil models (P < 0.001). Moreover, using paired t tests to validate these differences, we institute highly significant differences betwixt the observed distributions of FD and PD and the nil models (P < 10−16, t test). When we compared FD, PD, and TD with TS, we found low but significant correlations (r two = 0.31, P < 0.001; r ii = 0.26, P < 0.001; and r 2 = 0.33, P < 0.001, respectively) (fig. S1, D to F). Mapping these relationships, we revealed important spatial mismatches and congruencies among these biodiversity components (Fig. 1, A to D). Our spatial analysis revealed a wide disparity among the biodiversity these various measures of biodiversity: We observed a proportional deviation of 5% between FD and PD, fourteen% betwixt FD and TD, 12% between PD and TD, 44% between FD and TS, 42% betwixt PD and TS, and 29% between TD and TS (fig. S2).
Spatial distribution of FD (Petchey and Gaston's FD), PD (Faith'south PD), TD, and TS of amphibians in the Brazilian Atlantic Wood.
Through mapping and calculating the spatial data of the PAs, nosotros found that a 9309.15-km2 protected area in the Brazilian Atlantic Forest corresponded to only ix% of the region's entire area, comprising 2316.74 km2 of strict protection areas and 6992.41 kmtwo of sustainable use areas. This PA network comprises ~10% of FD, PD, and TD and almost 30% of TS, according to their spatial distributions across the Brazilian Atlantic Forest (Table 1). In total, nosotros found 38 TS, corresponding to 17 critically endangered, 10 endangered, and 11 vulnerable species, with ~70% of their total geographical range distributed outside the PAs (Table 1). Incorporating cost-effectiveness assessments of land values into evaluation of PAs and non-PAs, we showed the amount of investment needed for proportional values of FD, PD, TD, and TS of amphibians in the Brazilian Atlantic Woods (Table 1). Permutational multivariate analysis of variance (PERMANOVA) results reveal that cost-effectiveness assessment of land values tin can be considered as a strong predictor for those biodiversity attributes assessed as conservation targets (table S1).
Table 1
Land toll-effectiveness and pct land covered past PAs and non-PAs, according to the spatial distribution of the FD (Petchey and Gaston'southward FD), PD (Faith'southward PD), TD, and TS of amphibians in the Brazilian Atlantic Forest.
| FD | PD | TD | TS | |
| PAs | ||||
| Country cost-effectiveness (million dollars) | 159.49 | 152.71 | 127.86 | 36.36 |
| Land covered (%) | eleven.60 | 11.10 | nine.38 | 29.37 |
| Non-PAs | ||||
| Land price-effectiveness (million dollars) | 1215.45 | 1222.32 | 1245.97 | 87.07 |
| Land covered (%) | 88.twoscore | 88.90 | 90.62 | 70.63 |
Our 3 prioritization models illustrate several scenarios for integrative assessments of FD, PD, TD, and TS attributes (Fig. two). However, model 1 best represents the highest-priority regions for conservation (Table ii). Alternatively, models 2 and 3 testify larger state areas, which also crave higher investment. Although our results are area-dependent (square kilometers), we found a mismatch between pct forest embrace and overall land expanse in each model (Table 2). We recommend model 1 equally the best toll-effective strategy, which has a greater capability to safeguard larger forest areas in add-on to being the cheapest alternative (figs. S3 to S5). Moreover, model ane has the everyman presence of PAs, which reinforces the urgent demand to develop conservation efforts in these sites (Table two). We too annotation that the priority sites indicated past this model corroborate the two larger climatic refuges for Neotropical species during the belatedly Pleistocene [come across the study of Carnaval et al. (37) for details], located in the central corridor of the Atlantic Forest and the Serra exercise Mar coastal forests.
Spatial distribution of the PAs and the 3 prioritization models proposed to amphibian conservation in the Brazilian Atlantic Forest.
Table 2
Surface area, excluded PAs, forest cover, and land toll-effectiveness by 3 priority scenarios to amphibian conservation in the Brazilian Atlantic Wood.
Model 1, very loftier priority; model 2, high priority; model 3, medium priority.
| Priority scenarios | Surface area (kmii) | Excluded PAs (km2) | Forest embrace (%) | Country cost-effectiveness/year (meg dollars) |
| Model one | 1,995.28 | 293.62 | 24.25 | 26.48 |
| Model two | 4,555.12 | 934.02 | 15.thirty | 60.46 |
| Model 3 | 13,213.fifty | 1406.28 | xi.86 | 175.38 |
DISCUSSION
Our findings provide different optimization scenarios for the conservation of amphibian diversity aspects. FD and PD indices have been proposed as effective techniques for capturing potential niche complementarity in a community (11, 38). Some studies have highlighted the potential function of PD as a proxy for FD, yet this association is premised on the assumption that phylogenetic multifariousness generates ecological trait diversification, which in turn can result in greater niche complementarity (twenty). Despite the increasing prove for positive correlations between taxonomic, functional, and phylogenetic attributes and ecosystem stability (39), the mismatch among TD, FD, and PD (7) is creating a conservation impasse, which demands a practical arroyo to assessing relative conservation values of these components of biodiversity. From a conservation viewpoint, FD and PD tin be considered as two key attributes of variety for safeguarding ecosystem goods and services (xl), too as for representing evolutionary processes and features of conservation involvement (41). Therefore, measuring each of these biodiversity components in a complementary way is crucial for agreement the limerick and dynamics of natural communities (ten).
Bricklayer et al. (42) showed that the FD component may reveal changes in community assembly processes along an environmental gradient, suggesting that this index may be a strong predictor of complex processes structuring communities. A multifaceted framework of the FD metrics behind these associates processes facilitates the development of predictive models and more adequate tools for understanding how community construction is related to ecosystem functioning (43). In this context, the FD index tin can provide a potentially efficient power assay to differentiate assembly rules for dissimilar degrees of species richness (43). On the other mitt, null model approaches provide a robust means to exam whether species with similar functional traits are more or less likely to occur together than expected at random (44). Therefore, use of the FD index associated with null models has shown to be the approach that best relates to community functioning and ecosystem processes (viii, 43).
Considering the role of amphibian species in community functioning, the ecological contributions of these species can affect aquatic and terrestrial ecosystems every bit a whole, likewise as the flux between these ecosystems (45). Amphibians have varied and significant roles in ecosystems, from soil bioturbation and nutrient cycling to pest command and ecosystem technology (46). Some studies suggest that the loss of amphibians from stream ecosystems tin can alter primary production, algal community structure, faunal food bondage (from aquatic insects up to riparian predators), and reduce free energy transfers among diverse ecosystems through their role in nutrient cycling (45–47). Amphibians have frequently been cited every bit potential biological indicators of environmental change due to their permeable pare, high rates of contaminant bioaccumulation, climate-sensitive convenance cycles, and the fact that many species are dependent on both terrestrial and aquatic habitats during their life cycle (48–51). In addition, some amphibian taxa from small-scale areas within the Atlantic Wood have been identified as potential indicators of general biodiversity (52).
Although a particular individual diversity component could be used as a surrogate for other biological attributes, biodiversity assessment should do good from integrative approaches connecting evolutionary and functional ecology (twoscore). Using integrative conservation strategies, nosotros showed a congruence of ecological and evolutionary processes in the proposed models, yet they besides revealed mismatches between land expanse and priority rank. Because of the large area considered for conservation, economic costs become an obstruction; but if insufficient land area is set up aside, biological gains are weak (26). Our results thus demonstrate that local conservation policies for the Brazilian Atlantic Forest PAs do not guarantee the survival of about amphibian species in this region (~xc% of TD). Moreover, the current PA network finer protects only less than 10% of the total Atlantic Woods remnants (53). Although this reduced PA area seems inadquate, our results revealed that 28% of this network does nevertheless safeguard of import eco-evolutionary processes, represented past those areas showing a ≥fifty% FD, PD, and TD value of the full observed.
The pick of PAs is ordinarily aimed to preserve species of unlike taxonomic groups, communities of loftier biological relevance, or combinations of different abiotic conditions favorable to local ecosystems, assuming that these sites volition protect a wider range of biodiversity (54). However, many case studies reveal the inadequacy of the PA network in representing species diverseness (55). In north-eastern Brazil, Campos et al. (56) showed that the size of the PAs along the geographical range of threatened amphibian species does non necessarily safeguard their persistence, a finding also observed in this report. Moreover, it is predicted that the number of amphibian species of the Brazilian Atlantic Forest will decline within the PA network due to changing climate atmospheric condition (57). This network faces an additional risk because of its location within the economic center of Brazil (53), with a high human population density (~seventy% of the total Brazilian population) (58) and the presence of mining and logging industries in the region (57). To make matters worse, a recent mining dam burst on five November 2015 destroyed ane of the main river basins of the key corridor of Atlantic Woods, leading to the worst environmental disaster in the history of Brazil (59), which further accentuates the urgency for implementation of conservation strategies in this region. The federal and land Brazilian governments have sued the mine's possessor companies with $5 billion in amercement (59), which take been said to be designated for funding of conservation plans aimed to restore this highly degraded ecosystem.
We centered our prioritization models on a return-on-investment framework to simulate how limited conservation funds could exist spent on biodiversity protection, which were not based on agronomics land values, in accordance with the suggestions proposed past Sutton et al. (29). Our study demonstrates how the cost-effectiveness–based methods for assessing state values developed by our models could work equally a functional PES, which, in comparing with agrestal activities, corresponds to 24.13% of the median yearly gross profit per square kilometer of agricultural land distributed in the Atlantic Forest domain (26). Withal, considering that only 12.30% of the total area covered by our models is represented by forest remnants, we recommend agile reforestation practices in the nonforest areas (degraded livestock lands and abandoned agricultural lands). These practices would require an additional price of upwardly to $500,000/kmtwo for the start 3 years of restoration in the most degraded sites [see the study of Melo et al. (sixty) and Brancalion et al. (61) for details], respective to 0.02% of the Brazilian gross domestic product (26). On the other hand, about areas would follow natural regeneration simply by stopping the drivers of disturbance (sixty), taking into account that at to the lowest degree 20% of the area considered for restoration needs some active reforestation exercise (61).
Considered individually, no single forest remnant reaches the minimum land values proposed by the Aichi Biodiversity Target xi, which concluded that the terrestrial PAs should be expanded to at least 17% by 2020 (62). In this context, models i, two, and iii rise to most v, seven, and 16%, respectively, from the current Brazilian Atlantic Wood PAs. We draw attending to the disquisitional demand for amphibian conservation efforts in Atlantic Woods, and to the critical fact that ~xc% of FD, PD, and TD remain exterior the PAs. Conservation strategies such as Human foot are essential to maintain the ecological and evolutionary procedure. Although the forcefulness of this study is its innovative approach to incorporating biodiversity components into considerations of toll-effectiveness in conservation, our results residuum heavily on good research in ecosystem service provisioning. Co-ordinate to the environmental message reported by Naeem et al. (17), we also highlight the precautionary principle, in which "biodiversity conservation ensures ecosystem functions that in plow ensure ecosystem services benefiting humanity." Although we know that some ecosystem services cannot be bailiwick to pricing, they should exist considered on the basis of their biological value. Stakeholders and decision makers are central actors whose contribution is essential to putting these reports into practice. This situation demands political will and improved environmental services based on price-constructive designations of the highest-priority conservation areas, to reduce extinction hazard and avoid species loss. Our inquiry highlights the importance of maintaining the forest cover remnants in the Atlantic Wood, to provide a maximum representation of biodiversity components with the lowest economic toll. This innovative approach is not only amphibian-specific but can also be used in conservation plans for other taxonomic groups. This work has advanced knowledge of the analytical methods that tin be used to plan effective ecology actions to protect multiple biodiversity components with limited resources.
MATERIALS AND METHODS
Study area
Considered every bit the most threatened biodiversity hot spots on Earth (34), the Atlantic Woods had an original of area around i,500,000 km2, of which only nigh 12.nine% (~194,500 kmtwo) still remains in Brazil, Paraguay, and Argentine republic (53), corresponding to about 100,000 km2 of Brazilian forest remnants (63). The large fragments are located in hilly terrain, which hinder human occupation (64). Moreover, the ranges of different altitudinal and latitudinal gradients where these remnants were found have favored high biodiversity and owned species compared to other biomes in Brazil (53).
Although having a high rate of habitat loss (65), which is one of the main risk factors for amphibian extinction (35), the Atlantic Forest is the leader biome in amphibian diversity in Brazil, with 543 described species, comprising ~90% endemics and corresponding to more than 50% of all amphibian species of the entire state (66). However, despite the legal restrictions on deforestation in the Brazilian Atlantic Forest, vegetation is nonetheless extracted illegally, representing a mean rate of forest loss of effectually 0.15%/yr (67). Hither, nosotros used the term Brazilian Atlantic Forest with regard to the vegetation remnant map reported by the SOS Mata Atlântica/Instituto Nacional de Pesquisas Espaciais in 2015 (67).
Data acquisition
We obtained spatial data on amphibian species with three procedural approaches. Offset, nosotros built a data set up with all the species distributed in the Atlantic Woods co-ordinate to Haddad et al. (66); second, we included maps of geographical ranges for each species from the International Union for Conservation of Nature (IUCN) Red List of Threatened Species database (68); and third, we conducted complementary fieldwork comprising the major Atlantic Woods remnants of Brazil, to supplement the data set with additional data on distribution and observed functional traits (body size, reproductive mode, habitat, activity, toxicant patterns, habit, and calling site).
We led the survey in seven Brazilian PAs located in the fundamental corridor of the Atlantic Forest and the Serra exercise Mar coastal forests, stretching from the south to the northeast of the country (fig. S6). We sampled each surface area for 10 days between Jan and March 2015 (wet season), which are the months of highest activity of amphibians in the Atlantic Woods (69). In all localities, we conducted the survey using acoustic and visual nocturnal/diurnal assessments (70, 71), through an active search around h2o bodies, streams, and along 2000 1000 of woods transects for each assessed PA.
Next, we used ArcGIS 10.1 software (72) to build presence/absence matrices from the species distribution data past superimposing a filigree organisation with cells of 0.1° latitude/longitude, creating a network with 10,359 grid cells for the Brazilian Atlantic Forest. Nosotros also used spatial data on the Atlantic Forest PAs through the Brazil's Ministry of Environment database (73), including their categories (IUCN categories I to Iv) and land coverage.
Data analyses
We characterized 453 amphibian species through eight functional traits from 56 categories that determine different dimensions of the amphibians' ecological niches regarding morphology, life history, and beliefs. We used the trait categories reported past Haddad et al. (66), with some additional complementary data obtained in our fieldwork (see data file S1). Data file S1 describes the functional traits and their references for 453 amphibian species sampled in the Brazilian Atlantic Forest: (i) body size (millimeter), (2) members (apodal and tetrapod), (iii) activity (nocturnal, diurnal, and both), (iv) toxicity (toxic, nontoxic, unpalatable, or bad odor), (v) habitat (forested area, open up area, and both), (six) habit (arboreal, phytotelmate, terrestrial, cryptozoic, fossorial, rheophilic, semiaquatic, and aquatic), (vii) calling site (bamboo grove, swamp or lake, bromeliad, forest floor, tree awning, caves or burrows, rock wall, backwater river, stream, river, shrubs, grasslands, and not sings), and (viii) reproductive manner [1 to 39 modes; see the report of Haddad and Prado (74)]. These functional traits primarily contribute to ecosystem-supporting services through directly and indirect changes on ecosystem functions and processes (46). These functions tin be structural (habitat and habit) and ecological (body size, members, activity, poisonous, calling site, and reproductive style). For farther details, encounter the Supplementary Materials (table S2), where we show the specific functions and the ecosystem-supporting services of each one of the functional traits assessed (46, 66, 74–77).
To calculate the FD, we followed the protocol proposed by Petchey and Gaston (8): (i) structure of a species-trait matrix, (ii) conversion of species-trait matrix into a distance matrix, (iii) clustering distance matrix into a UPGMA (Unweighted Pair-Group Method with Arithmetics Average) dendrogram, and (4) computing FD by summing dendrogram branch lengths of species community. According Petchey and Gaston (8), FD is the functional metric that best relates to the performance of communities. To create the distance matrices, we used the method proposed by Pavoine et al. (78), through the Gower distance. Nosotros constructed the dendrograms using a hierarchical clustering, where only the species found in both the functional trait data set up and the amphibian occurrence database were considered. To verify whether FD was influenced past species richness, we used contained bandy null models (79), according to the protocol proposed by Swenson (80). The values provided by these models are more sensitive in preserving both site multifariousness and species frequency of occurrence while randomizing the pairs of species/sites, which ensure that patterns of trait assembly do non simply reflect differential occurrence of particular species (80, 81). We tested whether the observed FD was higher, equal, or lower than that expected by chance for each grid prison cell, assuming a random distribution in which every species could occupy whatsoever grid cell in the biome. For this, nosotros computed 1000 random replicates of the remaining FD, assuasive us to obtain a P value of FD as compared to the distribution of the random replicates. Although observed and null FD metrics indicate very similar responses (43, 80), the values generated by these metrics do not necessarily represent redundant data. Observed FD is highly correlated with species richness, whereas its nil model is totally independent of the species richness of an assemblage (80), which provides expected values at different species richness levels (43). In addition, we compared relative changes of observed and null FD distributions using paired t test. Given their different ability to discriminate community assembly rules, where the predictive accuracy of zippo FD is clearly better than the observed FD (43, eighty), nosotros used the goose egg model approach to detecting patterns in the overlap amid species in functional character space. Therefore, nosotros used the term FD with regard to the nada FD distributions in all further comparisons. We performed all analyses using the packages "ade4," "picante," "FD," and "vegan" through the R software (82).
For PD, we used the Faith's PD index (83), comprising the sum of the lengths of the branches from the phylogenetic tree of all species assessed. We based the phylogenetic distance on 207 species nucleotide sequences obtained from GenBank (data file S2) [come across the report of Benson et al. (84)], provided by the National Heart for Biotechnology Information. Post-obit the protocol proposed by Pyron and Wiens (85) in an extant amphibian phylogeny, nosotros used 12 genes to produce a novel phylogeny guess for the Atlantic Wood amphibians (eleven,906 base pairs for each species), through three mitochondrial (Cyt-b, 12s, and 16s) and 9 nuclear (CXCR4, H3A, NCX1, POMC, RAG1, ROHD, SIA, SLC8A3, and TYR) genes. For length-variable regions, we performed multiple pairwise comparisons using the online version of MAFFT half-dozen.8 with the M-INS-i algorithm (86). Next, we put together alignments of all genes in the aforementioned alignment, using the software Sequence Matrix 1.7.7 (87) to concatenate the supermatrix previously produced.
Nosotros reconstructed phylogenetic relationships with Bayesian analyses using BEAST one.8 (88). We performed the phylogenetic assay based on the combined information matrix through the Hasegawa, Kishino, and Yano (HKY) model of sequence evolution for ane division for all genes, using a Yule speciation process as the tree prior under an uncorrelated relaxed clock. Nosotros ran the Yule process for 100 million generations, ensuring that the number of generations convergence was sufficiently assessed with Tracer ane.vi (88), removing a conservative x% burn down-in fraction for the final tree. We combined these results with the utilize of LogCombiner 1.8.1 and TreeAnnotator 1.8.1 (88). We considered the nodes strongly supported if they received a posterior probability of ≥0.95. To edit the new phylogenetic tree, we used R software (82), from the package "ape" (89), using the Mesquite software 3.04 (xc) every bit an additional viewing tool. As provided on the functional metrics, we also built naught models to PD according to the same protocol used to obtain the cipher FD expectations (fourscore). Therefore, nosotros computed 1000 random replicates of remaining PD, obtaining a P value of PD as compared to the distribution of the random replicates. Nosotros also compared relative changes of observed and zilch PD distributions using paired t test. As proposed in the FD analyses and considering the predictive accuracy of the null PD compared with the observed PD, nosotros used the term PD with regard to the nada PD distributions in all farther comparisons. We performed the null model analyses using the packages ade4, picante, and vegan through the R software (82).
In addition, we calculated the TD and the number of TS present in each filigree jail cell, correlating with the values obtained by the FD and PD indices through uncomplicated linear regression models. Nosotros besides plotted the mismatches amid the relative values of these biodiversity components in a spatial representation to show where the greatest disparity might be would be, which is besides of interest. We classified TS according to the National Red List categories, using the official list of TS of the Brazilian fauna (91). We calculated the price-effectiveness values according to the expanse required to correspond each biodiversity component assessed (FD, PD, TD, and TS). Following Banks-Leite et al. (26), we based our toll-effectiveness analyses on the boilerplate value of PES across the Brazilian Atlantic Forest remnants, which corresponds to $13,273 for each square kilometer given annually to the individual wood landowners (28). In addition, to provide a comparative guess of cost-effectiveness–based land values of PAs and non-PAs, we performed a gap assay (92), measuring the corporeality of FD, PD, TD, and TS covered both by PAs and non-PAs. Thus, to assess the response of cost-effectiveness confronting the predicted variables FD, PD, TD, and TS, we used PERMANOVA, with thousand permutations based on a Euclidean distance matrix, through the "adonis" office in the vegan R package (93). Finally, we provide iii prioritization models based on different levels of complementary scenarios calculated as
where model i refers to very high priority, and values of FD, PD, and TD are ≥90% of the total observed (North); model two refers to high priority, where values of FD, PD, and TD are ≥seventy% of the total observed (North); and model iii refers to a medium priority, where values of FD, PD, and TD are ≥l% of the total observed (N). We did non consider areas with FD, PD, and TD values lower than the boilerplate conservation targets assessed (FD, PD, and TD, <50% of the total observed). The principal reason for this arroyo was to establish prioritization models that indicate areas from medium to very high priority, leaving out areas with low priority. In these three models, we considered but areas containing at least ane TS (TS, ≥ane) and excluded all the PAs available, analyzing only non-PAs (areas under no protection). Under our prioritization arroyo, we assumed that areas that are already protected, such every bit PAs, do not have priority for additional conservation efforts.
Supplementary Fabric
http://advances.sciencemag.org/cgi/content/full/3/6/e1602929/DC1:
Acknowledgments
We give thanks L. Rincón for useful comments on the manuscript. We thank A. Rudoy, Eastward. Pujol, and Chiliad. Cianciaruso for helpful discussions. Nosotros are grateful to S. Naeem, K. Winter, and two anonymous reviewers for the effective comments and great suggestions on the paper. We thank the Museu de Biologia Professor Mello Leitão and the Spitzkopf Ecological Park for the fieldwork back up. Nosotros too thank the Technical and Scientific Committee of the Forest Institute of São Paulo (COTEC), Environmental Institute of Paraná (IAP), and the Chico Mendes Institute for logistical support and drove licenses (ICMBio 30344 and 44755). Funding: This work was supported by the CAPES Foundation, Ministry of Education of Brazil (99999.001180/2013-04). R.L.-d.-Grand. is funded by CNPq (140710/2013-2 and 152303/2016-2). Author contributions: F.S.C. conceived the written report and wrote the manuscript with contributions from all coauthors. F.S.C. and R.50.-d.-K. designed the analyses, collected the data, and created the figures. All authors discussed the results and edited the manuscript. Competing interests: The authors declare that they have no competing interests. Data and materials availability: All information needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Boosted information related to this newspaper may be requested from the authors.
SUPPLEMENTARY MATERIALS
Supplementary cloth for this article is available at http://advances.sciencemag.org/cgi/content/full/3/half-dozen/e1602929/DC1
fig. S1. Plots of the relationships between FD (Petchey and Gaston's FD), PD (Faith's PD), TD, and TS of amphibians in the Brazilian Atlantic Wood.
fig. S2. Mismatch maps amongst FD (Petchey and Gaston's FD), PD (Faith'southward PD), TD, and TS of amphibians in the Brazilian Atlantic Forest.
fig. S3. Spatial distribution of the PAs, the forest remnants outside of the PAs, and the very loftier priority sites covered by the proposed model 1 to amphibian conservation in the Brazilian Atlantic Woods.
fig. S4. Spatial distribution of the PAs, the forest remnants outside of the PAs, and the high-priority sites covered by the proposed model ii to amphibian conservation in the Brazilian Atlantic Wood.
fig. S5. Spatial distribution of the PAs, the woods remnants outside of the PAs, and the medium-priority sites covered past the proposed model 3 to amphibian conservation in the Brazilian Atlantic Forest.
fig. S6. Wood remnants and complementary fieldwork areas sampled in the Brazilian Atlantic Forest.
tabular array S1. Results from the PERMANOVA on the land price-effectiveness by the FD (Petchey and Gaston's FD), PD (Faith's PD), TD, and TS of amphibians in the Brazilian Atlantic Forest.
table S2. Specific functions, ecosystem-supporting services, and references related to the amphibian functional traits assessed in the Brazilian Atlantic Forest.
information file S1. Functional traits and references for 453 amphibian species sampled in the Brazilian Atlantic Forest (.xlsx as a dissever file).
information file S2. GenBank accretion numbers for 207 amphibian species sampled in the Brazilian Atlantic Forest (.xlsx equally a separate file).
REFERENCES AND NOTES
i. Alberti G., Eco-evolutionary dynamics in an urbanizing planet. Trends Ecol. Evol. 30, 114–126 (2015). [PubMed] [Google Scholar]
2. Mayfield M. Thousand., Bonser Southward. P., Morgan J. W., Aubin I., McNamara Due south., Vesk P. A., What does species richness tell united states of america nearly functional trait diversity? Predictions and evidence for responses of species and functional trait diversity to state-apply modify. Global Ecol. Biogeogr. 19, 423–431 (2010). [Google Scholar]
3. Diniz-Filho J. A. F., Bini Fifty. Yard., Vieira C. M., Blamires D., Terribile L. C., Bastos R. P., de Oliveira G., de Souza Barreto B., Spatial patterns of terrestrial vertebrate species richness in the Brazilian Cerrado. Zool. Stud. 47, 146–157 (2008). [Google Scholar]
four. Naidoo R., Balmford A., Costanza R., Fisher B., Greenish R. E., Lehner B., Malcolm T. R., Ricketts T. H., Global mapping of ecosystem services and conservation priorities. Proc. Natl. Acad. Sci. U.S.A. 105, 9495–9500 (2008). [PMC free article] [PubMed] [Google Scholar]
5. Jenkins C. N., Van Houtan M. S., Pimm S. L., Sextond J. O., Us protected lands mismatch biodiversity priorities. Proc. Natl. Acad. Sci. UsaA. 112, 5081–5086 (2015). [PMC free article] [PubMed] [Google Scholar]
6. Dietz M. S., Belote R. T., Aplet G. H., Aycrigg J. L., The world's largest wilderness protection network after 50 years: An assessment of ecological system representation in the U.S. National Wilderness Preservation Arrangement. Biol. Conserv. 184, 431–438 (2015). [Google Scholar]
7. Devictor V., Mouillot D., Meynard C., Jiguet F., Thuiller W., Mouquet N., Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: The need for integrative conservation strategies in a irresolute earth. Ecol. Lett. 13, 1030–1040 (2010). [PubMed] [Google Scholar]
eight. Petchey O. L., Gaston Thousand. J., Functional diversity: Back to basics and looking forward. Ecol. Lett. 9, 741–758 (2006). [PubMed] [Google Scholar]
9. Schweiger O., Klotz Southward., Walter D., Kühn I., A comparative examination of phylogenetic diversity indices. Oecologia 157, 485–495 (2008). [PubMed] [Google Scholar]
ten. Webb C. O., Ackerly D. D., McPeek Chiliad. A., Donoghue Thousand. J., Phylogenies and community environmental. Annu. Rev. Ecol. Syst. 33, 475–505 (2002). [Google Scholar]
11. Cadotte M. W., Cavender-Baresn J., Tilman D., Oakley T. H., Using phylogenetic, functional and trait multifariousness to understand patterns of establish customs productivity. PLOS I 4, e5695 (2009). [PMC costless article] [PubMed] [Google Scholar]
12. Cadotte M. Due west., Dinnage R., Tilman D., Phylogenetic diversity promotes ecosystem stability. Ecology 93, S223–S233 (2012). [Google Scholar]
13. Arnan 10., Cerdá X., Retana J., Relationships among taxonomic, functional, and phylogenetic pismire diversity across the biogeographic regions of Europe. Ecography 40, 448–457 (2017). [Google Scholar]
14. Purschke O., Schmid B. C., Sykes M. T., Poschlod P., Michalski Due south. G., Durka W., Kühn I., Winter M., Prentice H. C., Contrasting changes in taxonomic, phylogenetic and functional variety during a long-term succession: Insights into assembly processes. J. Ecol. 101, 857–866 (2013). [Google Scholar]
15. Loreau M., Naeem South., Inchausti P., Bengtsson J., Crud J. P., Hector A., Hooper D. U., Huston 1000. A., Raffaelli D., Schmid B., Tilman D., Wardle D. A., Biodiversity and ecosystem functioning: Current knowledge and future challenges. Science 294, 804–808 (2001). [PubMed] [Google Scholar]
16. Hooper D. U., Chapin F. South. III, Ewel J. J., Hector A., Inchausti P., Lavorel S., Lawton J. H., Gild D. K., Loreau 1000., Naeem S., Schmid B., Setälä H., Symstad A. J., Vandermeer J., Wardle D. A., Effects of biodiversity on ecosystem operation: A consensus of current cognition. Ecol. Monogr. 75, three–35 (2005). [Google Scholar]
17. Naeem S., Duffy J. E., Zavaleta E., The functions of biological diversity in an age of extinction. Science 336, 1401–1406 (2012). [PubMed] [Google Scholar]
xviii. Gravel D., Bell T., Barbera C., Bouvier T., Pommier T., Venail P., Mouquet N., Experimental niche evolution alters the forcefulness of the diversity–productivity relationship. Nature 469, 89–92 (2011). [PubMed] [Google Scholar]
19. Hof C., Rahbek C., Araújo 1000. B., Phylogenetic signals in the climatic niches of the globe'south amphibians. Ecography 33, 242–250 (2010). [Google Scholar]
20. Flynn D. F. B., Mirotchnick Due north., Jain M., Palmer Chiliad. I., Naeem S., Functional and phylogenetic diversity as predictors of biodiversity–ecosystem-role relationships. Ecology 92, 1573–1581 (2011). [PubMed] [Google Scholar]
21. Joseph L. N., Maloney R. F., Possingham H. P., Optimal allotment of resources among threatened species: A project prioritization protocol. Conserv. Biol. 23, 328–338 (2009). [PubMed] [Google Scholar]
22. Naidoo R., Balmford A., Ferraro P. J., Polasky S., Ricketts T. H., Rouget Thou., Integrating economical costs into conservation planning. Trends Ecol. Evol. 21, 681–687 (2006). [PubMed] [Google Scholar]
23. Naughton-Treves Fifty., Kingdom of the netherlands Thou. B., Brandon K., The part of protected areas in conserving biodiversity and sustaining local livelihoods. Annu. Rev. Environ. Resour. 30, 219–252 (2005). [Google Scholar]
24. Gardner T. A., Barlow J., Chazdon R., Ewers R. M., Harvey C. A., Peres C. A., Sodhi Due north. S., Prospects for tropical forest biodiversity in a human-modified globe. Ecol. Lett. 12, 561–582 (2009). [PubMed] [Google Scholar]
25. Dobson A., Club D., Alder J., Cumming G. S., Keymer J., Mcglade J., Mooney H., Rusak J. A., Sala O., Wolters V., Wall D., Winfree R., Xenopoulos M. A., Habitat loss, trophic plummet, and the decline of ecosystem services. Environmental 87, 1915–1924 (2006). [PubMed] [Google Scholar]
26. Banks-Leite C., Pardini R., Tambosi L. R., Pearse Westward. D., Bueno A. A., Bruscagin R. T., Condez T. H., Dixo M., Igari A. T., Martensen A. C., Metzger J. P., Using ecological thresholds to evaluate the costs and benefits of ready-asides in a biodiversity hotspot. Scientific discipline 345, 1041–1045 (2014). [PubMed] [Google Scholar]
27. Van Buskirk J., Willi Y., Enhancement of farmland biodiversity within set-aside land. Conserv. Biol. 18, 987–994 (2004). [Google Scholar]
28. F. B. Guedes, S. E. Seehusen, Pagamentos por Serviços Ambientais na Mata Atlânica: Lições aprendidas e desafios (Ministério do Meio Ambiente, 2011). [Google Scholar]
29. Sutton Northward. J., Choc South., Armsworth P. R., A reliance on agricultural land values in conservation planning alters the spatial distribution of priorities and overestimates the acquisition costs of protected areas. Biol. Conserv. 194, ii–10 (2016). [Google Scholar]
30. Petersen A. H., Strange N., Anthon S., Bjørnerd T. B., Rahbek C., Conserving what, where and how? Cost-efficient measures to conserve biodiversity in Kingdom of denmark. J. Nat. Conserv. 29, 33–44 (2016). [Google Scholar]
31. Gering J. C., Crist T. O., Veech J. A., Additive partitioning of species diverseness beyond multiple spatial scales: Implications for regional conservation of biodiversity. Conserv. Biol. 17, 488–499 (2003). [Google Scholar]
32. Brooks T. M., Mittermeier R. A., da Fonseca Chiliad. A. B., Gerlach J., Hoffmann G., Lamoreux J. F., Mittermeier C. G., Pilgrim J. D., Rodrigues A. S. L., Global biodiversity conservation priorities. Science 313, 58–61 (2006). [PubMed] [Google Scholar]
33. Lee T. Grand., Jetz W., Time to come battlegrounds for conservation nether global alter. Proc. R. Soc. Lond. B Biol. Sci. 275, 1261–1270 (2008). [PMC costless commodity] [PubMed] [Google Scholar]
34. Myers North., Mittermeier R. A., Mittermeier C. G., da Fonseca G. A. B., Kent J., Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000). [PubMed] [Google Scholar]
35. Stuart S. N., Chanson J. S., Cox Due north. A., Young B. E., Rodrigues A. South. L., Fischman D. Fifty., Waller R. W., Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786 (2004). [PubMed] [Google Scholar]
36. Pyron R. A., Wiens J. J., Large-scale phylogenetic analyses reveal the causes of high tropical amphibian diverseness. Proc. Biol. Sci. 280, 20131622 (2013). [PMC free article] [PubMed] [Google Scholar]
37. Carnaval A. C., Hickerson Chiliad. J., Haddad C. F. B., Rodrigues K. T., Moritz C., Stability predicts genetic diverseness in the Brazilian Atlantic forest hotspot. Science 323, 785–789 (2009). [PubMed] [Google Scholar]
38. Mouillot D., Graham Northward. A. J., Villéger Due south., Mason N. Westward. H., Bellwood D. R., A functional approach reveals community responses to disturbances. Trends Ecol. Evol. 28, 167–177 (2013). [PubMed] [Google Scholar]
39. Safi M., Cianciaruso G. V., Loyola R. D., Brito D., Armour-Marshall K., Diniz-Filho J. A. F., Understanding global patterns of mammalian functional and phylogenetic multifariousness. Philos. Trans. R. Soc. Lond. B 366, 2536–2544 (2011). [PMC free article] [PubMed] [Google Scholar]
twoscore. Wiens J. J., Graham C. H., Niche conservatism: Integrating evolution, ecology, and conservation biology. Annu. Rev. Ecol. Evol. Syst. 36, 519–539 (2005). [Google Scholar]
41. Mace Thousand. One thousand., Gittleman J. L., Purvis A., Preserving the tree of life. Science 300, 1707–1709 (2003). [PubMed] [Google Scholar]
42. Mason Northward. W. H., Irz P., Lanoiselée C., Mouillot D., Argillier C., Bear witness that niche specialization explains species-energy relationships in lake fish communities. J. Anim. Ecol. 77, 285–296 (2008). [PubMed] [Google Scholar]
43. Mouchet Thou. A., Villéger Southward., Mason N. W. H., Mouillot D., Functional diversity measures: An overview of their redundancy and their ability to discriminate customs associates rules. Funct. Ecol. 24, 867–876 (2010). [Google Scholar]
44. Stubbs W. J., Wilson J. B., Evidence for limiting similarity in a sand dune community. J. Ecol. 92, 557–567 (2004). [Google Scholar]
45. Whiles Grand. R., Lips Yard. R., Pringle C. M., Kilham S. South., Bixby R. J., Brenes R., Connelly South., Colon-Gaud J. C., Hunte-Brown M., Huryn A. D., Montgomery C., Peterson S., The effects of amphibian population declines on the structure and function of neotropical stream ecosystems. Forepart. Ecol. Environ. 4, 27–34 (2006). [Google Scholar]
46. Hocking D. J., Babbitt K. J., Amphibian contributions to ecosystem services. Herpetol. Conserv. Biol. 9, ane–17 (2014). [Google Scholar]
47. Meredith H. M. R., Buren C. V., Antwis R. Due east., Making amphibian conservation more than effective. Conserv. Evidence 13, 1–v (2016). [Google Scholar]
48. Blaustein A. R., Wake D. B., The puzzle of failing amphibian populations. Sci. Am. 272, 52–57 (1995). [Google Scholar]
49. DeGarady C. J., Halbrook R. S., Using anurans every bit bioindicators of PCB contaminated streams. J. Herpetol. twoscore, 127–130 (2006). [Google Scholar]
50. Lebboroni M., Ricchiardino G., Bellavita M., Chelazzi 1000., Potential use of anurans as indicators of biological quality in upstreams of central Italy. Amphibia-Reptilia 27, 73–79 (2006). [Google Scholar]
51. Hopkins W. A., Amphibians equally models for studying environmental alter. ILAR J. 48, 270–277 (2007). [PubMed] [Google Scholar]
52. Campos F. S., Trindade-Filho J., Brito D., Llorente K. A., Solé M., The efficiency of indicator groups for the conservation of amphibians in the Brazilian Atlantic Forest. Ecol. Evol. 4, 2505–2514 (2014). [PMC free article] [PubMed] [Google Scholar]
53. Ribeiro Yard. C., Metzger J. P., Martensen A. C., Ponzoni F. J., Hirota Yard. Chiliad., The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 142, 1141–1153 (2009). [Google Scholar]
54. Lawler J. J., White D., Assessing the mechanisms backside successful surrogates for biodiversity in conservation planning. Anim. Conserv. eleven, 270–280 (2008). [Google Scholar]
55. Rodrigues A. South. L., Andelman S. J., Bakarr Chiliad. I., Boitani L., Brooks T. Yard., Cowling R. G., Fishpool L. D. C., da Fonseca G. A. B., Gaston G. J., Hoffmann M., Long J. South., Marquet P. A., Pilgrim J. D., Pressey R. L., Schipper J., Sechrest W., Stuart Southward. North., Underhill Fifty. Thousand., Waller R. W., Watts M. E. J., Yan 10., Effectiveness of the global protected area network in representing species diversity. Nature 428, 640–643 (2004). [PubMed] [Google Scholar]
56. Campos F. S., Brito D., Solé M., Threatened amphibians and their conservation status within the protected area network in Northeastern Brazil. J. Herpetol. 47, 277–285 (2013). [Google Scholar]
57. Lemes P., Melo A. S., Loyola R. D., Climate change threatens protected areas of the Atlantic Forest.Biodivers. Conserv. 23, 357–368 (2014). [Google Scholar]
58. Tabarelli M., Aguiar A. V., Ribeiro Yard. C., Metzger J. P., Peres C. A., Prospects for biodiversity conservation in the Atlantic Woods: Lessons from aging human-modified landscapes. Biol. Conserv. 143, 2328–2340 (2010). [Google Scholar]
59. Escobar H., Mud tsunami wreaks ecological havoc in Brazil. Science 350, 1138–1139 (2015). [PubMed] [Google Scholar]
60. Melo F. P. L., Pinto S. R. R., Brancalion P. H. S., Castro P. S., Rodrigues R. R., Aronson J., Tabarelli Yard., Priority setting for scaling-up tropical wood restoration projects: Early lessons from the Atlantic Woods Restoration Pact. Environ. Sci. Policy 33, 395–404 (2013). [Google Scholar]
61. Brancalion P. H. Due south., Viani R. A. G., Strassburg B. B. N., Rodrigues R. R., Finding the coin for tropical forest restoration. Unasylva 63, 25–34 (2012). [Google Scholar]
63. Tabarelli G., Pinto 50. P., Silva J. One thousand. C., Hirota M., Bedê L., Challenges and opportunities for biodiversity conservation in the brazilian atlantic forest. Conserv. Biol. xix, 695–700 (2005). [Google Scholar]
64. Silva W. K. S., Metzger J. P., Simões S., Simonetti C., Relief influence on the spatial distribution of the Atlantic Forest embrace on the Ibiúna Plateau, SP. Braz. J. Biol. 67, 403–411 (2007). [PubMed] [Google Scholar]
65. Teixeira A. M. K., Soares B. S., Freitas Due south. R., Metzger J. P., Modeling landscape dynamics in an Atlantic Rainforest region: Implications for conservation. For. Ecol. Manage. 257, 1219–1230 (2009). [Google Scholar]
66. C. F. B. Haddad, L. F. Toledo, C. P. A. Prado, D. Loebmann, J. L. Gasparini, I. Sazima, Guia dos anfíbios da Mata Atlântica—Diversidade east Biologia (Anolis Books, 2013). [Google Scholar]
67. SOS Mata Atlântica, Instituto Nacional de Pesquisas Espaciais (INPE), Atlas dos Remanescentes Florestais da Mata Atlântica Período 2013–2014 (SOS Mata Atlântica/INPE, 2015).
69. L. J. Vitt, J. P. Caldwell, Herpetology: An Introductory Biology of Amphibians and Reptiles (Elsevier, 2013). [Google Scholar]
lxx. M. L. Crump, N. J. Scott Jr., in Visual Encounter Surveys, W. R. Heyer, M. A. Donnelly, R. W. McDiarmid, 50. A. C. Hayek, Yard. S. Foster, Eds. (Smithsonian Institution Printing, 1994), pp. 84–92. [Google Scholar]
71. B. L. Zimmerman, in Audio Strip Transects, W. R. Heyer, Yard. A. Donnelly, R. West. McDiarmid, 50. A. C. Hayek, Thousand. Southward. Foster, Eds. (Smithsonian Institution Press, 1994), pp. 92–97. [Google Scholar]
72. Environmental Systems Research Constitute (ESRI), ArcGIS Software: Version ten.1 (ESRI, 2011).
74. Haddad C. F. B., Prado C. P. A., Reproductive modes in frogs and their unexpected diversity in the Atlantic forest of Brazil. BioScience 55, 207–217 (2005). [Google Scholar]
75. W. E. Duellman, Fifty. Trueb, Biological science of Amphibians (Johns Hopkins Univ. Printing, 1994). [Google Scholar]
76. K. D. Wells, The Ecology and Beliefs of Amphibians (University of Chicago Press, 2007). [Google Scholar]
77. Toledo Fifty. F., Ribeiro R. S., Haddad C. F. B., Anurans equally prey: An exploratory analysis and size relationships betwixt predators and their prey. J. Zool. 271, 170–177 (2007). [Google Scholar]
78. Pavoine Due south., Vallet J., Dufour A. B., Gachet S., Daniel H., On the claiming of treating various types of variables: Application for improving the measurement of functional variety. Oikos 118, 391–402 (2009). [Google Scholar]
79. Gotelli North. J., Entsminger G. L., Swap and fill algorithms in null model analysis: Rethinking the knight'due south tour. Oecologia 129, 281–291 (2001). [PubMed] [Google Scholar]
fourscore. Due north. G. Swenson, Functional and Phylogenetic Ecology in R (Springer, 2014). [Google Scholar]
81. Ackerly D. D., Schwilk D. W., Webb C. O., Niche evolution and adaptive radiation: Testing the guild of trait divergence. Environmental 87, 50–61 (2006). [PubMed] [Google Scholar]
82. R Development Core Squad, R: A Linguistic communication and Environment for Statistical Computing (R Foundation for Statistical Computing, 2008).
83. Faith D. P., Conservation evaluation and phylogenetic diverseness. Biol. Conserv. 61, ane–10 (1992). [Google Scholar]
84. Benson D. A., Cavanaugh M., Clark 1000., Karsch-Mizrachi I., Lipman D. J., Ostell J., Sayers Eastward. Due west., GenBank. Nucleic Acids Res. 41, D36–D42 (2013). [PMC free commodity] [PubMed] [Google Scholar]
85. Pyron R. A., Wiens J. J., A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol. Phylogenet. Evol. 61 543–583 (2011). [PubMed] [Google Scholar]
86. Katoh K., Toh H., Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 9, 286–298 (2008). [PubMed] [Google Scholar]
87. Vaidya G., Lohman D. J., Meier R., SequenceMatrix: Concatenation software for the fast assembly of multi-gene datasets with grapheme set and codon information. Cladistics 27, 171–180 (2011). [Google Scholar]
88. Drummond A. J., Suchard One thousand. A., Xie D., Rambaut A., Bayesian Phylogenetics with BEAUti and the Beast 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012). [PMC free article] [PubMed] [Google Scholar]
89. Paradis Due east., Claude J., Strimmer Grand., APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004). [PubMed] [Google Scholar]
90. W. P. Maddison, D. R. Maddison, Mesquite: A modular system for evolutionary analysis: Version 3.04 (2015); http://mesquiteproject.org.
92. J. M. Scott, J. Schipper, in Gap Analysis: A Spatial Tool for Conservation Planning, M. J. Groom, G. Yard. Meffe, C. Ronald, Eds. (Sinauer, 2006), pp. 518–519. [Google Scholar]
93. J. Oksanen, F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B. O'Hara, Thousand. L. Simpson, P. Solymos, M. H. H. Stevens, H. Wagner, Community ecology package "vegan" 2013 (R Development Core Team, 2013); https://cran.r-project.org/web/packages/vegan/index.html.
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