Introduction
Only 7% (c. 20,755 species) of known plant species have had their conservation status evaluated, and approximately 54% of these are categorized as threatened on the IUCN Red List (IUCN, 2015). Given the number of plant species that have not yet been evaluated for the Red List, and the estimates of significant numbers of plant species that have not yet been discovered or described by science (Purvis & Hector, Reference Purvis and Hector2000; Scotland & Wortley, Reference Scotland and Wortley2003; Joppa et al., Reference Joppa, Roberts and Pimm2011; Scheffers et al., Reference Scheffers, Joppa, Pimm and Laurance2012), the current estimate of c. 9,000 threatened taxa is an underestimation. The goals of the Global Strategy for Plant Conservation include completing the evaluation of the conservation status of plants by 2020 (target 2) and protecting 75% of all threatened plant species in situ (target 7; SCBD, 2009).
Brazil harbours c. 45,000 plant species (c. 19% of global plant diversity; Giulietti et al., Reference Giulietti, Harley, Queiroz, Wanderley and van Den Berg2005), with c. 19,000 endemics (Forzza et al., Reference Forzza, Leitman, Costa, Carvalho, Peixoto and Walter2010); a new plant species is described there every 2 days (Sobral & Stehmann, Reference Sobral and Stehmann2009). The conservation status of 4,617 plant species have been evaluated and 2,118 (c. 46%) are categorized as threatened and 554 (c. 12%) as Data Deficient (Martinelli & Moraes, Reference Martinelli and Moraes2013).
Conservation efforts are generally targeted to identify and safeguard priority species and sites at various spatial scales: global (e.g. biodiversity hotspots; Mittermeier et al., Reference Mittermeier, Gil, Hoffmann, Pilgrim, Brooks, Mittermeier and da Fonseca2005), regional (e.g. key biodiversity areas; Eken et al., Reference Eken, Bennun, Brooks, Darwall, Fishpool and Foster2004; Langhammer et al., Reference Langhammer, Bakarr, Bennun, Brooks, Clay and Darwall2007) and local (e.g. Alliance for Zero Extinction; Ricketts et al., Reference Ricketts, Dinerstein, Boucher, Brooks, Butchart and Hoffmann2005). The Alliance for Zero Extinction, an international initiative to identify and protect sites of global relevance to biodiversity conservation, suggests that threatened species that are restricted to a single site or population should be a priority for conservation (Ricketts et al., Reference Ricketts, Dinerstein, Boucher, Brooks, Butchart and Hoffmann2005), based on the concepts of irreplaceability and vulnerability (Pressey, Reference Pressey1994; Margules & Pressey, Reference Margules and Pressey2000; Pressey & Taffs, Reference Pressey and Taffs2001).
The identification and protection of Alliance for Zero Extinction sites is among the metrics used to evaluate ongoing efforts to achieve the Convention on Biological Diversity targets for 2020 (as a subindicator for target 11). The Convention also recommends the implementation of national-level initiatives to identify priority species and sites (CBD, 2015). This is a critical time for conservation in Brazil, and the importance of leading by example has been highlighted on a number of occasions (Scarano et al., Reference Scarano, Guimarães and Silva2012; Ferreira et al., Reference Ferreira, Aragão, Barlow, Barreto, Berenguer and Bustamante2014; Loyola, Reference Loyola2014). Because of its rich biodiversity Brazil is at the forefront of the global conservation agenda, and actions taken at the national level will influence global decision making. Our objective was to identify and map Alliance for Zero Extinction species and sites for the Brazilian flora.
Methods
The methodology used to identify priority species and sites for the Brazilian flora is similar to that used globally (Ricketts et al., Reference Ricketts, Dinerstein, Boucher, Brooks, Butchart and Hoffmann2005). A shortlist of candidate species was obtained from Brazil's national red list of threatened flora (Martinelli & Moraes, Reference Martinelli and Moraes2013). To qualify for Brazilian Alliance for Zero Extinction status a species must be categorized as Endangered or Critically Endangered on this list (Martinelli & Moraes, Reference Martinelli and Moraes2013), with a majority of the population or distribution (c. 95%) confined to a single site with a definable boundary (Ricketts et al., Reference Ricketts, Dinerstein, Boucher, Brooks, Butchart and Hoffmann2005). Distribution and population data were obtained from published databases (Giulietti et al., Reference Giulietti, Rapini, Andrade, Queiroz and Silva2009; Plantas Raras do Brasil, 2009; Martinelli & Moraes, Reference Martinelli and Moraes2013; Biodiversitas Foundation, 2015; List of Species of the Brazilian Flora, 2015; speciesLink, 2015). We also consulted the Catalogue of Plants and Fungi of Brazil (Forzza et al., Reference Forzza, Leitman, Costa, Carvalho, Peixoto and Walter2010).
To evaluate the protection status of sites we overlaid them with the World Database on Protected Areas (Protected Planet, 2015). Sites were defined as protected if they overlapped with an existing protected area; otherwise they were defined as unprotected. To evaluate human pressure on sites, we obtained human density and gross domestic product data for the municipalities where the sites are located (IBGE, 2010). Statistical analyses were performed in R v. 2.15.2 (R Development Core Team, 2012). Brazil has identified priority areas and conservation actions to protect its biodiversity (Ministério do Meio Ambiente, 2007). To evaluate the congruence between these priority areas and the Alliance for Zero Extinction sites for the Brazilian flora, we estimated the overlap between the existing conservation agenda and the newly identified Alliance for Zero Extinction sites.
Results
We identified a total of 234 trigger species located in 140 Alliance for Zero Extinction sites (Fig. 1). The Atlantic Forest hosts the largest number of such sites for the Brazilian flora (78), and two oceanic sites are particularly important: Fernando de Noronha and Trindade (Figs 1 & 2). Most trigger species belong to the families Asteraceae (38 species), Bromeliaceae (24) and Cactaceae (16; Supplementary Table S1).
Fig. 1 Protected (n = 21; black filled circles) and unprotected (n = 119; grey filled circles) Alliance for Zero Extinction sites for the Brazilian flora.
Fig. 2 Number of Alliance for Zero Extinction sites for the Brazilian flora, by biome.
The status of the sites is a cause for concern as only 21 are located within protected areas (Figs 1 & 3); of these only eight are in strictly protected areas and 13 are in sustainable-use protected areas. Most of the protected sites are in the Atlantic Forest (10 sites, or 13% of the Alliance for Zero Extinction flora sites in the Atlantic Forest), whereas the Pampa and the Pantanal do not have a single protected site within their boundaries (Fig. 1; Supplementary Table S2).
Fig. 3 Number of Alliance for Zero Extinction sites for the Brazilian flora in each category of protected area.
Neither human density (t = −1.020, df = 22.347, P = 0.31) nor annual gross domestic product per capita (t = −1.239, df = 22.319, P = 0.22) has a relationship with the level of protection of the sites analysed. Unprotected sites had a mean human population density of 181 inhabitants per km2 and a mean annual gross domestic product per capita of USD 6,363.80, whereas protected sites had a mean human population density of 489 inhabitants per km2 and a mean annual gross domestic product per capita of USD 9,314.50 (Supplementary Table S2).
Only 74 (53%) of the identified Alliance for Zero Extinction sites for flora were located within an official priority area identified by the Brazilian government (Fig. 4). Of these, 56 (76%) were categorized as extremely high priority, three (4%) as very high priority, 11 (15%) as high priority and four (5%) sites were included within the Data Deficient category (Fig. 5). It is important to note the large number of single-site species categorized as Vulnerable on the Brazilian Red List (285 species, 108 sites; Supplementary Table S3); although they do not trigger the designation of Alliance for Zero Extinction sites (Ricketts et al., Reference Ricketts, Dinerstein, Boucher, Brooks, Butchart and Hoffmann2005; Alliance for Zero Extinction, 2010), changes in their conservation status could dramatically increase the number of such sites for the Brazilian flora.
Fig. 4 Alliance for Zero Extinction sites for the Brazilian flora in government-defined priority areas for conservation action (n = 74; black filled circles) and non-priority areas (n = 66; grey filled circles).
Fig. 5 Number of Alliance for Zero Extinction sites for the Brazilian flora in each priority category.
Discussion
National-level analyses may speed up the identification and protection of globally sensitive species and sites, particularly in the case of endemics. Mexico has the highest number of sites in the global Alliance for Zero Extinction scheme, with 151 trigger species and 68 sites (Alliance for Zero Extinction, 2010). Currently, Brazil has 28 trigger species and 27 sites overall (Alliance for Zero Extinction, 2010), substantially fewer than our calculations of 234 trigger species in 140 sites. Our calculations are, however, significant underestimations, as only 15% of the Brazilian flora has been assessed (Martinelli & Moraes, Reference Martinelli and Moraes2013), and do not take into account the 12,000 animal species recently assessed in Brazil, of which 1,173 are categorized as threatened (Ministério do Meio Ambiente, 2014).
The high number of Alliance for Zero Extinction sites in the Atlantic Forest and in the Cerrado may be attributable to the high levels of habitat destruction and endemism in these regions (Myers et al., Reference Myers, Mittermeier, Mittermeier, da Fonseca and Kent2000; Mittermeier et al., Reference Mittermeier, Gil, Hoffmann, Pilgrim, Brooks, Mittermeier and da Fonseca2005), suggesting urgent reactive conservation strategies are needed to safeguard such sites (Brooks et al., Reference Brooks, Mittermeier, da Fonseca, Gerlach, Hoffmann and Lamoreux2006). The trends in the policy of protected area creation in Brazil (Cabral & Brito, Reference Cabral and Brito2013) and the low human occupation of the Amazon should facilitate the adoption of a proactive conservation strategy to safeguard Alliance for Zero Extinction sites in the Amazon (Brooks et al., Reference Brooks, Mittermeier, da Fonseca, Gerlach, Hoffmann and Lamoreux2006).
Our results highlight the need for protection of currently unprotected sites. At the global level, 22% of Alliance for Zero Extinction sites are protected (Butchart et al., Reference Butchart, Scharlemann, Evans, Quader, Aricò and Arinaitwe2012), whereas only 15% of the sites designated for the Brazilian flora are protected, and thus Brazil is lagging behind the global efforts to protect such sites (CBD target 11). Although protected areas have been created in the Atlantic Forest and in the Cerrado they are small, and therefore the increase in the total area protected within these biomes is insignificant (Cabral & Brito, Reference Cabral and Brito2013). The present political scenario for improving and expanding the national protected area network is not promising (Bernard et al., Reference Bernard, Penna and Araújo2014; Marques & Peres, Reference Marques and Peres2015). None of the sites identified here, however, overlap with protected areas that were recently downgraded, downsized or degazetted (Bernard et al., Reference Bernard, Penna and Araújo2014; Marques & Peres, Reference Marques and Peres2015); the Alliance for Zero Extinction sites are the top candidates for complementing Brazil's existing protected area network. It has been noted that species occurring within Alliance for Zero Extinction sites have had less deterioration of their conservation status than species outside these sites (Butchart et al., Reference Butchart, Scharlemann, Evans, Quader, Aricò and Arinaitwe2012). The protection of priority sites for biodiversity also provides significant benefits for people, and improvements in ecosystem services (Larsen et al., Reference Larsen, Turner and Brooks2012). However, given the high number of Alliance for Zero Extinction sites in Brazil, and the country's unstable protected area policy (Bernard et al., Reference Bernard, Penna and Araújo2014; Marques & Peres, Reference Marques and Peres2015), legally protecting all of the sites is not feasible.
Implementation of strategies to protect biodiversity on private lands, complementing the existing protected area networks, is therefore required (Norton, Reference Norton2000; Jenkins et al., Reference Jenkins, Van Houtan, Pimm and Sexton2015; Kamal et al., Reference Kamal, Grodzińska-Jurczak and Brown2015). In Brazil, Private Natural Heritage Reserves (Reservas Particulares do Patrimônio Natural) are a successful strategy, with landowners receiving economic incentives from the government if they create a private protected area. The coverage of protected land is increased at only a small cost to the government (Rambaldi et al., Reference Rambaldi, Fernandes and Schmidt2005; Crouzeilles et al., Reference Crouzeilles, Vale, Cerqueira and Grelle2013). Incentives to create Private Natural Heritage Reserves could support short-term biodiversity conservation while new strategies are tested and implemented to ensure long-term efficiency and stability of conservation outside governmental protected areas (Young, Reference Young2005; Kamal et al., Reference Kamal, Grodzińska-Jurczak and Brown2015). In situ and ex situ population management could also complement the strategy of protecting sites (e.g. Hoffmann et al., Reference Hoffmann, Blum, Velazco, Gill and Borgo2015), and the role of herbaria and botanical gardens in conservation should be promoted (Wyse Jackson & Sutherland, Reference Wyse Jackson and Sutherland2000; Maunder et al., Reference Maunder, Higgens and Culham2001a,Reference Maunder, Lyte, Dransfield and Bakerb; Schatz, Reference Schatz2002; Callmander et al., Reference Callmander, Schatz and Lowry2005).
Our results represent an underestimation of the number of Alliance for Zero Extinction sites for the Brazilian flora, for four main reasons: (1) Brazil's red list includes many Data Deficient species (Martinelli & Moraes, Reference Martinelli and Moraes2013), some of which may be threatened (Sousa-Baena et al., Reference Sousa-Baena, Garcia and Peterson2014); (2) the Linnean shortfall (Whittaker et al., Reference Whittaker, Araújo, Jepson, Ladle, Watson and Willis2005; Possingham et al., Reference Possingham, Grantham and Rondinini2007), where species that are not yet formally described by science are overlooked in strategies devised to safeguard biodiversity; (3) there are many single-site species categorized as Vulnerable whose conservation status may worsen, triggering new Alliance for Zero Extinction sites for the Brazilian flora (Supplementary Table S3); and (4) our analysis is based on only a partial assessment of the conservation status of Brazilian plants, as Martinelli & Moraes (Reference Martinelli and Moraes2013) provided assessments for only 4,617 of c. 45,000 species. The number of species that trigger Alliance for Zero Extinction sites is likely to increase substantially when the assessment of all Brazilian endemics is completed.
This work is an example of how science can help inform public policies, using the national plant red list as a scientific guide for the development and allocation of scarce conservation resources (Scarano & Martinelli, Reference Scarano and Martinelli2010). The use of red lists as a conservation tool in Brazil is gaining momentum (e.g. Morais et al., Reference Morais, Braga, Bastos and Brito2012, Reference Morais, Siqueira, Lemes, Maciel, De Marco and Brito2013; Moraes et al., Reference Moraes, Borges, Martins, Fernandes, Messina and Martinelli2014). In the national flag the green colour symbolizes the country's forests and abundant biodiversity but it will fade if the native flora is not effectively protected.
Acknowledgements
We are grateful for the comments and suggestions received from two anonymous reviewers and from Martin Fisher, which greatly improved the manuscript. We thank Kelly Souza for providing support with ArcGIS. MFD and TVG thank CAPES for their graduate scholarships. DB is grateful for the continuous support of CNPq (#305446/2012-6).
Biographical sketches
Milena Diniz's main research interests are in evaluating the effectiveness of protected area networks in Brazil, and prioritizing areas for conservation. Tatiel Gonçalves’ interests lie in the use of Red Lists as conservation tools to advance the protection of biodiversity and in the influence of conservation policies on conservation actions. Daniel Brito's research focus is on comprehending the extinction process, identifying conservation priorities, advancing Red Lists as conservation tools, and estimating the consequences of knowledge gaps in conservation.
