Research ArticleCONSERVATION ECOLOGY

# Cost-effective conservation of amphibian ecology and evolution

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Vol. 3, no. 6, e1602929

## Abstract

Habitat loss is the most important threat to species survival, and the efficient selection of priority areas is fundamental 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 diversity can include cost-effectiveness–based assessments of land values. We report new key conservation sites within the Brazilian Atlantic Forest hot spot, revealing a congruence of ecological and evolutionary patterns. We suggest payment for ecosystem services through environmental set-asides on private land, establishing potential trade-offs for ecological and evolutionary processes. Our findings introduce additional effective area-based conservation parameters that set new priorities for biodiversity assessment in the Atlantic Forest, 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 assessment
• Atlantic Forest hotspot
• Amphibians

## INTRODUCTION

Ecosystem functioning and evolutionary processes are usually linked, carrying a series of short-term implications for ecological and human well-being (1). The consequences of human activities go beyond species loss, with various studies also reporting losses of functional traits and evolutionary history in various human-influenced landscapes (2). These losses are increasing demands for effective strategies on biodiversity conservation (3), which have been also subject to the incorporation of economic costs with the objective of providing more feasible conservation strategies on the ground (4). Given that habitat loss is the most important threat to species survival, the protected sites chosen by decision makers determine what species and how many of these will be able to survive in nature (5). The effectiveness of these selected sites in achieving conservation goals depends on how well the ecological diversity is represented in a given area (6). Several studies have focused on spatial prioritization to represent taxonomic diversity (TD), not highlighting the importance of capturing other biodiversity components, such as functional diversity (FD) and phylogenetic diversity (PD) (7). Moreover, to date, their conservation strategies have been blind to the functions these other components perform in a cost-effective conservation policy.

FD is a biodiversity dimension that represents the extent of functional differences among species based on the distinction of their morphological, physiological, and ecological traits (8). PD adds value to theoretical and applied ecology studies by distinguishing species according to their evolutionary histories (9), reflecting the time and mode of divergence across the tree of life (10). In addition, FD and PD can better predict ecosystem function and stability than TD (11, 12). However, using TD, FD, and PD in a simultaneous approach can help predict differential effects of competition and environmental filtering on the community assembly (13). Nonetheless, consistency in the relationships between TD, FD, and PD can provide insights into the extent to which community assembly is driven by deterministic versus stochastic processes (14).

A central question in community ecology and conservation biology is related to determining how biodiversity patterns can influence ecosystem functioning (1517). The key strategy to address this issue is to assess the relationships between functional and phylogenetic biodiversity components of the ecosystem (11, 18). Understanding the associations between ecological similarity and phylogenetic relatedness among species helps in the formulation of a hypothesis about the impact of evolutionary changes on functional ecology (19). Focusing on both functional and phylogenetic traits of a community can improve our understanding of the consequences of biodiversity loss (20). However, 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 still 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 have not yet been implemented in practice and therefore remain as 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 inside PAs but also throughout the biome (24). In this context, environmental set-asides on private land have been shown to be a promising strategy for conservation of species and ecological functions across farmlands (25). Nevertheless, set-asides of private land for conservation generally come with economic costs to the landowners (26). Therefore, environmental strategies that incorporate payment for ecosystem services (PES) can provide an efficient tool for increasing landowner participation in conservation programs (25). This strategy’s feasibility is reflected in the ever-increasing number of PES projects around the world (27, 28). Despite this trend, most PES projects are relatively local initiatives that may not adequately represent the full range of conservation needs and economic issues observed throughout biodiversity hot spots (28). On the other hand, many environmental organizations are developing systematic planning tools to help identify opportunities that offer the greatest return on investment in biodiversity protection (29). In a conservation context, this investment can be indicated by cost-effectiveness–based estimates of land values, that is, the trade-off between biodiversity gains and economic costs of paying landowners to participate in set-aside programs (26).

## SUPPLEMENTARY MATERIALS

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 Forest.

fig. S2. Mismatch maps among FD (Petchey and Gaston’s 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 Forest.

fig. S4. Spatial distribution of the PAs, the forest 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 forest remnants outside of the PAs, and the medium-priority sites covered by the proposed model 3 to amphibian conservation in the Brazilian Atlantic Forest.

fig. S6. Forest remnants and complementary fieldwork areas sampled in the Brazilian Atlantic Forest.

table S1. Results from the PERMANOVA on the land cost-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.

data file S1. Functional traits and references for 453 amphibian species sampled in the Brazilian Atlantic Forest (.xlsx as a separate file).

data file S2. GenBank accession numbers for 207 amphibian species sampled in the Brazilian Atlantic Forest (.xlsx as a separate file).

This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

## REFERENCES AND NOTES

Acknowledgments: We thank L. Rincón for useful comments on the manuscript. We thank A. Rudoy, E. Pujol, and M. Cianciaruso for helpful discussions. We are grateful to S. Naeem, M. Winter, and two anonymous reviewers for the constructive comments and great suggestions on the paper. We thank the Museu de Biologia Professor Mello Leitão and the Spitzkopf Ecological Park for the fieldwork support. We also 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 collection 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.-M. is funded by CNPq (140710/2013-2 and 152303/2016-2). Author contributions: F.S.C. conceived the study and wrote the manuscript with contributions from all coauthors. F.S.C. and R.L.-d.-M. 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 data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Additional data related to this paper may be requested from the authors.
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