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Review ARTICLE

Front. Mar. Sci., 07 November 2017 | https://doi.org/10.3389/fmars.2017.00353

Systematic Planning and Ecosystem-Based Management as Strategies to Reconcile Mangrove Conservation with Resource Use

  • 1Resource Management Working Group, Faculty of Biology, University of Bremen, Bremen, Germany
  • 2Leibniz-Centre for Tropical Marine Research (ZMT), Bremen, Germany
  • 3Instituto de Ciências do Mar (LABOMAR), Universidade Federal do Ceará, Fortaleza, Brazil

About 120 million people worldwide live within 10 km of large mangrove forests, and many of them directly depend on the goods and services provided by these ecosystems. However, it remains unclear how to synchronize ecological definitions and legal conservation strategies regarding mangroves, especially in developing countries, such as Brazil. The influence of human populations' socio-economic context in mangrove conservation policies, as well associated challenges in incorporating this influence, are underestimated or, often, largely ignored. Considering the recent threats emerging from changes in legislation and the lack of spatial and social-ecological integrated data to plan mangrove conservation in Brazil, this paper aims to answer the following questions: (1) What suitable measures could managers and other decision makers adopt for efficient mangrove conservation planning?; (2) What are the site-specific, social-ecological aspects that need to be taken into account when deciding on conservation and management strategies?; and (3) How could science contribute to the development of these measures? In order to achieve an ecosystem-based management approach, mangrove ecosystems should not be divided into sub-systems, but instead treated as an integrated system. Furthermore, interconnections with other coastal ecosystems must be assessed and taken into account. This is crucial for effective systematic conservation planning. Also, most of the particular social-ecological aspects in the different types of mangrove ecosystems along the Brazilian coast, and how those differences might be considered while planning for conservation, remain poorly understood. Based on similar drivers of change, geological features, and likely impacts of climate change, a macro-unit approach is proposed to group mangrove systems along the Brazilian coast and guide national policies. This paper draws parallels with management approaches worldwide to find common points and hence lessons to be applied in other regional realms. It considers the issues of legal vulnerability and needs for social-ecological data on mangroves, contributing toward systematic conservation planning and ecosystem-based management for these ecosystems.

Introduction

About 120 million people worldwide live within 10 km of mangrove forests (UNEP, 2014). Many of them largely depend on the goods and services provided by coastal ecosystems, such as food and timber provision, fuel wood and shoreline protection (Spalding et al., 2010; Barbier et al., 2011). Mangroves also indirectly deliver farther-reaching benefits, such as serving as habitat for terrestrial and marine species (Nagelkerken et al., 2008). At least 776 species of birds, fish, mollusks, arthropods and plants are associated with these ecosystems in Brazil (Schaeffer-Novelli, 1999), with even larger numbers in Indo-Pacific mangroves (Latham and Ricklefs, 1993). On a global scale, they function as important carbon-sequestering systems (Donato et al., 2011; Ray et al., 2011; Murdiyarso et al., 2012).

In some developing countries, mangroves are estimated to contribute to national economies with US$33–57 thousand per hectare per year (e.g., Sathirathai and Barbier, 2001). Some coastal human populations are directly dependent on mangroves, such as in north Brazil, where 83% of rural households harvest natural resources from mangroves, which also provide 68% of their cash income (Glaser, 2003). However, mangroves have been largely affected by land conversion, pollution, and overexploitation, leading to a loss 3–5 times faster than that in other forest types (Alongi, 2002). Clearing of these forests is usually due to aquaculture, agriculture, and urban land uses (Spalding et al., 2010). The deforestation of coastal vegetated ecosystems corresponds to up to nearly 20% of total emissions from deforestations on the planet, with economic damages of US$6–42 billion per year (Pendleton et al., 2012).

Brazil has between 75 and 83% of its mangrove coverage within some category of protected area (Magris and Barreto, 2010; Prates et al., 2012). This represents a much larger cover than the global average (~ 28%) (Juffe-Bignoli et al., 2014). The total protected extension of Brazilian mangroves kept increasing in recent years: since 2014, the country holds the largest extent of protected mangrove in the world: 322 thousand hectares inside 11 “extractive reserves”—a sustainable-use category (Plataforma Brasil, 2015). Similar protected area models have been shown to offer good conservation results elsewhere (Aheto et al., 2016). In Brazil, however, these reserves have not yet been systematically assessed. Moreover, around 58% of the total protected mangrove areas are within the category of environmental protection areas, a sustainable-use category of protected areas considered to deliver low levels of protection (Prates et al., 2012).

Despite having already lost 10–20% of its mangroves (FAO, 2007), Brazil still holds a total mangrove area of over one million hectares (Magris and Barreto, 2010), spread out along 6,786 km of coastline (Schaeffer-Novelli et al., 2000). Contrary to the trend in other countries, the total mangrove area in Brazil even increased in the first decade of the millennium (Aide et al., 2013).

Recent changes in conservation policy in Brazil, however, such as the new Brazilian Forest Code (BRASIL, 2012), will likely have negative impacts on mangroves and other vegetation types (Silva et al., 2011; Medeiros et al., 2015; Ferreira and Lacerda, 2016b; Oliveira-Filho et al., 2016). This federal law, strongly biased toward agribusiness interest (Oliveira-Filho et al., 2016), disaggregates from the mangrove the salt flats (“apicuns”), which are of special interest to shrimp farming, but also an important component of the mangrove ecosystem (Schmidt et al., 2013). The new law admits the “sustainable use” of these areas, including aquaculture and salt production ponds.

Negative impacts on coastal and marine processes and on social-economic activities are predicted consequences of this change in legislation (Rovai et al., 2012) because it fails to adopt an ecosystem-based approach when defining mangroves and the interactions between its components. Ecosystem-based management is here understood as “an integrated approach to management that considers the entire ecosystem, including humans” (McLeod et al., 2005), where the complexity and relationship within close ecological systems are acknowledged, together with social and governance objectives of mangrove management (Barbier, 2006; Aswani et al., 2012; Carter et al., 2015; Long et al., 2015). The ecosystem-based management approach is an opportunity to maximize ecosystem services while promoting ecological resilience and appropriate productive activities (Lithgow et al., in press).

The recent developments and discussions on sub-systems, such as the salt flats, and the uniqueness of mangroves as ecosystems illustrate the discussion that directly affects mangrove conservation. It remains unclear how to synchronize the ecological definitions and legal conservation strategies regarding mangroves. As observed for other countries where mangrove forests are found, laws and policies in Brazil are rarely designed for the specific management requirements of mangroves. As illustrated by the Forest Code, mangroves are usually regulated under legal frameworks created originally for forests in general, environment, water, land, or marine fisheries (Rotich et al., 2016).

Mangrove management requires attention to the multidimensional benefits they provide, both ecologically and socially (Rotich et al., 2016). However, incorporation of social-ecological aspects, such as people's perception and traditional uses in conservation policies, is deficient (McConney and Charles, 2008). As pointed out by Benessaiah and Sengupta (2014), one challenge is that many ecologists and managers tend to define ecosystems in a localized sense, rather than adopting a broader understanding of ecosystems as self-organizing units comprised of interacting ecological and social components operating at different scales. Adopting a social–ecological system approach explicitly defines issues as an integrated system of people and environment (Benessaiah and Sengupta, 2014; Nayak and Berkes, 2014). The term social–ecological is used throughout this paper in the sense of the integration of humans and nature in complex, adaptive systems (Berkes and Folke, 1998).

Systematic conservation planning requires explicit goals and criteria for implementing conservation action, besides mechanisms for maintaining the conditions within reserves that are required to foster the persistence of key natural features (Margules and Pressey, 2000). It is based on the extent to which conservation goals have already been met in existing reserves and clear methods to locate and design new reserves to complement existing ones (Margules and Pressey, 2000).

Considering the recent threats from changes in legislation and the lack of spatial, social-ecological data integration to plan for conservation of mangrove systems, this paper aims to answer the following questions: (1) What suitable measures could managers and other decision makers adopt for efficient mangrove conservation planning?; (2) What are the site-specific, social-ecological aspects that need to be taken into account when deciding on conservation and management strategies?; and (3) How could science contribute to the development of these measures?

This is the first review to consider the issues of legal vulnerability and lack of integrated social-ecological data, using Brazil as a study case and systematic planning and ecosystem-based management as backbones to discuss the following suggested approaches to tackle the apparent paradox of reconciling mangrove conservation and sustainable use: (1) mangrove as a social-ecological system; (2) mangrove as an integrated system; (3) multi-scale planning; (4) standardized, GIS-based information and synthesis work; and (5) assessment of the protected area system.

Linking Systematic Planning and Ecosystem-Based Management to Guide Further Strategies

The Mangrove as a Social-Ecological System

The involvement of stakeholders in environmental management, when underpinned by a focus on empowerment, equity, trust and learning, can (1) improve environmental decision making by considering more comprehensive information inputs (Reed, 2008) and (2) increase public trust in decisions and civil society, if participatory processes are perceived to be transparent and consider conflicting claims and views (Richards et al., 2004). Stakeholder participation can increase the likelihood that environmental decisions are perceived to be holistic and fair, accounting for a diversity of values and needs and recognizing the complexity of human-environmental interactions (Richards et al., 2004). It can also empower stakeholders through the co-generation of knowledge with researchers and through increased participants' capacity to use this knowledge (Stephenson et al., 2016). To be successful, the involvement of actors must be institutionalized, creating organizational cultures that can facilitate processes where goals are negotiated and outcomes are uncertain (Reed, 2008).

Scientific research can indicate concrete measures to enhance stakeholder participation and develop strategies to help involve local actors in a more efficient way. As emphasized by Ferreira and Lacerda (2016a), in order to promote mangrove conservation, besides government enforcement of the protection legislation, people need to be aware of the goods and services provided by mangroves. Unfortunately, population awareness usually only arises after the consequences of mangrove degradation (Barbier, 2006), so providing people with information about similar cases and the consequences of mangrove degradation elsewhere through experience exchange could be a shortcut to avoid human-promoted mangrove degradation by lack of knowledge. However, science often fails to translate knowledge to decision makers and the general public (Granek et al., 2010).

In the case of fisheries, which is an important human activity developed in mangrove areas (UNEP, 2014), engaging community leaders has been shown to be essential to achieve successful co-management (Gutiérrez et al., 2011). Native populations, especially those directly dependent on mangrove goods and services, as well as other societal sectors, need to be integrated through community-based management (Ferreira and Lacerda, 2016a). In addition, when considering the effectiveness of protected areas, besides creating more and larger reserves, it is important to concomitantly invest in education, economic incentives, and community-based enforcement (Rife et al., 2013).

Regarding fisheries management, successful outcomes of community-based initiatives benefit from (1) effective information sharing, (2) harvesting rules that merge traditional and contemporary practices, (3) strong leadership, and (4) resource monitoring (Blythe et al., 2017). There is, though, a deficiency of information on the social dimensions of mangrove management (Rotich et al., 2016), necessary to promote these aspects. Local and scientific knowledge can be integrated to provide a more comprehensive understanding of complex and dynamic socio-ecological systems and processes (Reed, 2008).

Local people often have a symbolic relationship with the mangrove forest, so the socio-cultural dimension of mangrove services needs to be considered by policy makers to tackle challenges in coastal ecosystems conservation (Queiroz et al., 2017). To tackle the financial dependency on mangroves it is vital to provide all stakeholders with the capability to influence the political aspects of governance, support institutions which foster accountability, encourage civil society to participate in decision making processes, and ensure that views from the local level feed into the multi-level governance process (Orchard et al., 2015).

Partnerships with mangrove research groups need to be created and strengthened (Ferreira and Lacerda, 2016a). Scientific research can contribute, for example, with the development of methods to incorporate local ecological knowledge, through bottom-up social studies that shed light on how to apply this knowledge to the development of conservation strategies for mangroves. This is especially relevant to assess monetary and non-monetary values of ecosystem goods and services. With such a valuation at the local level, policy makers can be made aware that the profit coming from the shrimp market, for example, is considerably smaller than the environmental damage caused, as exposed in the case of some intensive shrimp farms in NE Brazil (Ferreira and Lacerda, 2016a). {One exception could be, for example, organic farms in NE Brazil and traditional “tambacs” in Asia, which may have a mutual benefit for adjacent mangrove forests (Lacerda et al., 2002).}

A lack of understanding of the values associated with wetlands is largely due to the complexity and “invisibility” of spatial relationships between groundwater, surface water, and wetland vegetation (Turner et al., 2000). Following a global pattern (Walters et al., 2008), the values associated with Brazilian mangrove ecosystems are not taken into account by policy makers, when, for example, shrimp farming is considered more valuable than mangrove preservation. Despite pressure and consequent damages over mangroves, little is known about their unique value in terms of ecosystem services, since local variation can be high due to site specificities along the Brazilian coast (Souza and Ramos e Silva, 2010; Estrada et al., 2015; Ferreira and Lacerda, 2016a). But even these few accurate studies are not taken into consideration by decision makers or environmental authorities. The largest mangroves in the world, the Sundarbans, for example, lack a specific protection agenda or policy (Roy and Alam, 2012).

More integrated studies to assess ecosystem services and vulnerability to environmental impacts have to be conducted for Brazilian mangroves. Integrated wetland research combining social and natural sciences can help to partly solve the information problem and provide consistency among various government policies (Turner et al., 2000). While global (Martínez et al., 2007) and local scale (Saint-Paul and Schneider, 2016) integrated approaches have been applied, the regional level might be the best starting point to identify cross-scale interactions which shape coastal and marine social-ecological dynamics and outcomes (Glaser and Glaeser, 2014).

In order to make progress, further and intensified co-operation is needed between social and natural scientists (Turner et al., 2000). It is also imperative to collect and integrate data from different disciplines, which are essential for sustainable development and management, particularly in developing countries (Dahdouh-Guebas, 2002). Including models and values of ecosystem services and vulnerability in marine spatial planning, for example, can help achieve multiple benefits for nature and people (Arkema et al., 2015). Böhnke-Henrichs et al. (2013) provide a framework for such an ecosystem service approach in marine spatial planning. Given the peculiarities of transitional ecosystems such as mangroves, however, an even more specific typology and sets of indicators for coastal areas could be useful to assess ecosystem services. Additionally, stakeholders at different spatial scales can have very different interests in ecosystem services (Hein et al., 2006), so it is important to consider the scales of these services when valuation is applied to support the formulation or implementation of spatial plans.

In fisheries, for example, management systems are starting to value fishers' knowledge, considered part of the “best available information.” Fishermen are able to provide information that can integrate ecological, economic, social, and institutional considerations of future management. Fishers' knowledge can be added to traditional assessment with appropriate analysis and explicit recognition of the intended use of the information and, if implemented in a participatory process designed to receive and use it, this knowledge can facilitate the participation of fishers in assessment and management, considered as best practice in fisheries governance (Stephenson et al., 2016).

The view of mangroves and contiguous coastal ecosystems as an assembly of interconnected exchanging matter and energy flux means that the conservation and use of such ecosystems requires integrated management (Ferreira and Lacerda, 2016a). Indeed, countless fishery resources recruit and grow in different coastal ecosystems, which also share mutual buffer effects (Walters et al., 2008; PEDRR, 2010). An integrated, ecosystem-based management should account for the complexity and relationship within close ecological systems (Macintosh and Ashton, 2005; Long et al., 2015; Lithgow et al., in press). It should also account for social and governance objectives of mangrove ecosystem management, like community-based management and social decisions, effective use of scientific knowledge, stakeholder involvement, appropriate monitoring, applying of precautionary approach and others (Macintosh and Ashton, 2005; Walters et al., 2008; Granek et al., 2010; Aswani et al., 2012; Carter et al., 2015; Long et al., 2015; Schmitt and Duke, 2015). Such an approach has been rarely applied worldwide, mainly due to land tenure issues, lack of interdisciplinary research and of incorporation of native populations' knowledge, weak law compliance, and ineffective governance structures (Aswani et al., 2012; Carter et al., 2015; de Almeida et al., 2016; Ferreira and Lacerda, 2016a).

Standardized, GIS-Based Information and Synthesis Work

Brazil holds the world's largest nearly uninterrupted mangrove belt, between the cities of Belém and São Luís: a 6,516-km2 tract that, as a unitary system, corresponds to 4.3% of the total global mangrove area and over 80% of Brazilian mangroves (Spalding et al., 2010). The Bragança peninsula is the data-richest area in this mangrove belt, due to intensive research work developed through the MADAM Project and subsequent projects (Saint-Paul and Schneider, 2016). Geomorphological and hydrographic conditions (Souza Filho and Paradella, 2002) as well as vegetation patterns (Menezes et al., 2008), are likely similar throughout the northern mangrove region. Research gaps remain, however, as to whether data and assessment applied to the local level could be scaled up to support a regional approach to management.

Such a vast area of populated coast calls for a conservation strategy consonant with community-based management (Ferreira and Lacerda, 2016a), which could be capable of safeguarding the interests of local communities while taking into consideration the already existing protected areas and indigenous territories. In co-management arrangements, for example, priorities of the various local stakeholder groups are assessed throughout the planning and management processes. In the case of an extractive reserve in North Brazil, interests of local communities have been assessed and incorporated into formal management instruments using, at least, three different strategies: (1) by researchers (Glaser, 2003; Glaser and Da Silva Oliveira, 2004), generating valuable knowledge which later on was applied by decision makers (Abdala et al., 2012); (2) by planners and managers directly (Abdala et al., 2012); or (3) as an action-research approach, where scientists facilitated co-management processes, such as participatory coastal planning (Saint-Paul and Schneider, 2016).

Additionally, the monitoring of fisheries and aquaculture activities, which varies among the different mangroves on the Brazilian coast, could contribute to the assessment of ecosystem services in mangroves. Shrimp farming as the main activity in mangrove areas can be more easily monitored, while crab catching, for instance, is not detectable by GIS imagery analyses, what makes the latter more challenging to monitor (Santos et al., 2014).

Moreover, Walters et al. (2008) emphasize how important the availability of these data to the general public is. Satellite imagery, although in a limited format, are available on the internet at no or little cost through virtual globe programs (even though some areas of the world's surface remain poorly covered by the most easily accessible tools). In the hands of the public, these new tools could significantly change the socio-economic dynamics associated with these forests (Walters et al., 2008). Stakeholders should therefore have further and broader access to accurate and cost-effective techniques for mapping and monitoring, in order to develop and implement effective policy for the socio-economic use of mangroves (Walters et al., 2008).

Magris and Barreto (2010) highlight the need to map and make available GIS-based databases to monitor environmental changes in mangroves and, therefore, allow for efficient conservation actions. National-level organizations in Brazil need to take more serious steps toward a GIS-based databank for coastal and marine ecosystems.

Researchers in Brazil have to report their results to the federal biodiversity conservation agency for a range of field work projects. Having such results as a starting point, this agency could synthesize data produced and evaluate what information is missing, which could then be used in conservation studies. Plus, systemic and interdisciplinary studies, which include not only ecological, but also social, political and economic aspects, can provide the solution to complex problems faced by Brazilian marine protected areas (Gerhardinger et al., 2011).

Putting together pieces of information that might point to generalizations is also vital to conservation research, yet this task seems to have been left to reports and plans developed by practitioners, or are limited to a few literature reviews or meta-analyses. Research gaps do not necessarily mean lack of primary data, but spatial planning methods and case studies in similar social-ecological contexts to guide on-the-ground application can be rare. A few initiatives worldwide constitute a step-forward on the road to experience exchange, such as the Panorama platform, as an assemblage of successful examples for protected areas1. Regarding the ecosystem service approach, groups such as the Ecosystem Service Partnership (ESP)2 and The Economics of Ecosystems and Biodiversity (TEEB)3 provide case studies, which focus on the terrestrial environment, such as in the Amazon region (Rodrigo Cassola, 2010). Projects that directly apply the ecosystem service approach to spatial planning in Brazilian coastal and marine environments are rare.4

Compared to fully terrestrial vegetation ecosystems, such as the Amazon rainforest, and fully marine ecosystems, like coral reefs, mangroves receive little attention from mass media (Valiela et al., 2001). But contrary to the image of mangroves as smelly swamps, charismatic species are often found in many nursing and feeding grounds offered by mangroves {a list is compiled by UNEP (2014)}, which could be used to enhance support for the conservation of these ecosystems. Indeed, important species for mangrove ecology, such as the crab Ucides cordatus, face overfishing and decreasing population levels in some Brazilian mangroves. This can lead to overfishing of alternative stocks, for example, the red mangrove crab Goniopsis cruentata, which is also a key species (Ferreira et al., 2013). Consequences of these changes for mangrove functioning remain uncertain.

Furthermore, moving from policy toward action is important to improve the protection of mangroves and of the livelihoods that depend on these ecosystems (Friess et al., 2016). Ferreira and Lacerda (2016a) urge for restoration of deforested mangroves. An inexpensive and time-saving solution would be to map and protect mangrove areas with a potential for self-recovery (Ferreira et al., 2015). Beyond specific purposes, mapping is an important tool for systematic conservation planning and ecosystem-based management (Maia et al., 2006). The zoning of protected areas in Brazil, for example, is an essential part of their management plan (BRASIL, 2000), which again highlights the importance of spatial data for mangrove management.

More Than the Sum of Its Parts: The Mangrove as an Integrated Ecosystem

In 2012 the Brazilian National Congress passed the controversial Forest Code (BRASIL, 2012). While not being the main focus of most discussions about the new law, the changes on the legal framework for mangrove protection did not go unnoticed: an important sub-system, the “apicum” {escape valve for inland migration of mangroves as an adaptive response to sea level rise (Godoy and Lacerda, 2015)}, was removed from the concept of mangrove ecosystem, being now separately attended to by this new law in a less strict level of protection. These salt flats are non-vegetated areas, essential for the maintenance of the forested area in the mangrove systems (Schmidt et al., 2013) and are the ecosystem's last resource in terms of space to persist transitional periods and sea level rise (Oliveira-Filho et al., 2016). The most protective legislation only covers the wooded component (mangrove forests) (Oliveira-Filho et al., 2016). This measure makes a large area (over 600,000 hectares) available for aquaculture development (Ferreira and Lacerda, 2016b). Making salt flats available for occupation squeezes mangroves between open waters and human activity in these salt flats, hindering them from migrating inland following sea level rise. Without these buffer areas vulnerability to climate change will be increased, and mangrove forests will be doomed in the long run.

The current legislation for mangroves in Brazil therefore ignores the correlate features and interdependencies between these habitat types (Moura-Fé et al., 2015). Furthermore, the total mangrove extent safeguarded in permanent protection areas, which represent another important protection instrument in Brazilian legislation, will be reduced, showing how some governmental authorities and policies purposely ignore scientific warnings about necessity and even economic advantages of mangrove conservation to favor agribusiness lobbies (Ferreira and Lacerda, 2016b).

While the new law has been contested by the Brazilian Academy of Sciences (Silva et al., 2011), there is no unanimity about the features that constitute mangroves in Brazil, and how these ecosystems should be managed for conservation and sustainable development. Oliveira-Filho et al. (2016), for example, adopt the definition of mangrove ecosystem as “a tidally influenced wetland complex including progradational sand or mud flats, mangrove forests and salt marshes, hypersaline lagoons, intertidal flats, including salt flats, salt pans, salinas, salt barrens, apicuns, tannes and coastal sabkhas.” The different elements would, therefore, represent alternate states of the mangrove ecosystem (Woodroffe et al., 2016). The legislators in Brazil opted, however, for a different view of this ecosystem, assigning, through the new Forest Code, different levels of protection to the different components, and, therefore, ignoring their interdependency and interconnectedness.

In terms of applicability and monitoring, this new Forest Code also faces the issue that salt flats are not separately identified and mapped in Brazil, which leaves space for arbitrary identification of these areas during the planning and management actions at medium and large scales, moving in the opposite direction of what is required to safeguard biodiversity and the services provided by these ecosystems. Adopting such a measure reveals a national environmental policy that is dissonant with the country's intended goals to reduce carbon emissions, which were presented just before the last United Nations Framework Convention on Climate Change—COP 21 in Paris and the zero-illegal-deforestation target for the Brazilian terrestrial Amazon by 2030 (Paulo Moutinho, 2015).

This legal backstep against mangroves in Brazil reflects how complex and dynamic features of systems allow for the emergence not only of a variety of ecological functions, but also of a diversity of social-political perspectives on these systems. While researchers see them as an integrated ecosystem, formed by sub-systems with distinct but intertwined functions, some decision makers perceive the different vegetation types as a justification to assign different degrees of protection for areas within a highly interconnected system. Interconnectivity and interdependency, of course, do not automatically translate into uniform usage of the areas. However, such fragmentation through a national regulation might set the stage for local claims for controversial use, especially by the powerful aquaculture and salt production industries.

Worldwide, authority over mangrove forest management is overwhelmingly vested in state institutions and mangrove protection is a central objective. Within the forest sector, however, mangroves normally occupy a relatively marginal role with few policies or regulations tailored to the unique needs of mangrove forests (Rotich et al., 2016).

Mangrove ecosystems in Brazil could also profit from a unifying legal instrument, which brings together a body of regulations on mangrove use and conservation, while also recognizing the uniqueness, importance, and interconnectedness of mangroves and their sub-systems. The Amazon and Atlantic Forests, for example, have national laws as specific protection instruments (BRASIL, 1953, 2006), being also recognized as biomes by both the national authority responsible for the federal protected areas and the Ministry of Environment. A possible solution to the mangrove legal tangle would be, therefore, a unifying, national-level legislative framework for the conservation and sustainable use of mangroves in Brazil. A framework alone, however, would not be able to tackle all the legal issues regarding mangrove conservation and, if not followed by enforcement, would eventually become a useless instrument, like many other environmental laws at municipal, state, and federal levels.

Multi-Scale Mangrove Planning

In mangroves around the world, frameworks and mechanisms to enable multi-sectoral coordination across agencies and governance levels are uncommon, and where they exist, they are difficult to put into practice (Rotich et al., 2016). At the federal government scale, it is important to recognize mangroves and its subsystems as one integrated ecosystem. Concurrently, legislation needs to take into consideration regional aspects and allow for flexible management strategies related to regional or local specificities. At the municipality or state level, for instance, part of the wrongs of the new Forest Code could be at least partially overcome.

Schaeffer-Novelli et al. (1990) identified eight mangrove segments along the Brazilian coastline, according to climatic and physiographic characteristics of the mapping units. A unique combination of mangrove structure, beach characteristics, tidal regime and species composition, among others, distinguishes each of those segments. Recent studies and management plans have approached mangroves according to macro-, meso- and microtidal regimes (Magris and Barreto, 2010; MMA, 2015); creating a simpler grouping that still considers major differences among the Brazilian mangrove types, while being possibly more applicable in terms of policy-making at a national level.

Following a simplified approach, but also considering regional peculiarities relevant for management, four major mangrove regions are here proposed: North, Northeast, East, and Southeast. Such a division is based on Knoppers et al. (1999) and Godoy and Lacerda (2015), as well as on the approaches mentioned in the previous paragraphs (Figure 1).

FIGURE 1
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Figure 1. Brazilian mangroves and formal protection level for each proposed macro-unit. Based on Knoppers et al. (1999), Godoy and Lacerda (2015). The mangrove distribution data derive from Giri et al. (2011), and the protected area data from (IUCN UNEP-WCMC., 2017). “Unknown protection” was assigned to categories whose level of protection was not declared in the UNEP-WCMC dataset. *“only forest component protected” refers to mangrove areas that are not inside a protected area or indigenous area, but are, like all forest components of mangroves in Brazil, protected under the Forest Code (BRASIL, 2012) as “permanent protection areas.” Considering the states in Brazil, the division goes as follows: AP, PA, and MA (North); PI, CE, and RN (Northeast); PB, PE, AL, SE, and BA (East); ES, RJ, SP, PR, and SC (Southeast).

Macro-units are thus illustrated (Figure 1 and Table 1) to guide a unified, national-level policy framework for spatial planning of mangroves. Distinctions between the macro-units are manifold (Table 1). A steep coastline in the southeast and semiarid conditions in the northeast limit a possible landward refuge of forests facing sea level increase, hence restricting them to a narrow fringe along these coasts (Ferreira and Lacerda, 2016a). These traits, summed up with strong human-use pressures (Godoy and Lacerda, 2015), might hinder mangrove survival in the face of climate change. On the other hand, mangrove areas have the chance to expand in the northern part of the coastline, following predictions related to sea-level rise, because here mangroves find landward areas for expansion, such as in the Amazon estuary (Cohen and Lara, 2003; Cohen et al., 2008; Ward et al., 2016). Along the eastern and southeastern coasts, estuaries and coastlines have suffered severe damage (Magris and Barreto, 2010; Prates et al., 2012). In southeastern mangroves, main drivers of degradation are coastal development, urbanization, and pollution, mostly from inadequate solid waste disposal and oil spills (Ferreira and Lacerda, 2016a). In the Northeast macro-unit, mangrove loss of up to 10% is large compared to the other segments, corresponding to at least twice the country's average deforested area (Ferreira and Lacerda, 2016a). Northern mangroves, despite being relatively pristine and proportionally better included in protected areas, need to be made more resilient as social-ecological systems, in order to face severe impacts that might reach these ecosystems, as it has happened in the other segments.

TABLE 1
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Table 1. Distinct traits about each proposed mangrove macro-unit.

Differences in anthropogenic impacts on mangroves ecosystems and resulting impacts are also shown for the four macro-units proposed (Table 1). A large national coverage under the denomination of protected area alone does not systematically safeguard the various mangroves segments along the coast: the extent of mangroves inside the various categories of protected areas in Brazil varies considerably among the different macro-units, showing that the distinct mangrove systems in Brazil are unevenly protected (Figure 1).

In terms of social-economic activities developed, there is a considerable difference among these mangrove macro-units. While saltwater aquaculture is being intensively practiced in eastern (Godoy and Lacerda, 2015) and northeastern Brazil (Santos et al., 2014), artisanal fisheries and crabbing as well as harvesting of other natural resources prevail in northern mangroves (Tenório et al., 2015). Northeastern mangroves suffer from severe habitat loss due to the advance of shrimp farming (Meireles et al., 2008) and other activities such as agriculture, urban expansion, and tourism (Guimarães et al., 2010). Saltpans were also a major economic activity in northeastern mangroves, and one single state in this region reached the production of approximately 95% of the country's national consumption (Bezerra and Brito, 2001). In the eastern mangrove coastline, local shell fishing activity is now being devastated by port pollution in Pernambuco (Zoe Sullivan, 2014). Due to the variety of habitats and anthropogenic pressures, changes in coverage and distribution of mangroves in this macro-unit should be more carefully assessed at the local level (Godoy and Lacerda, 2015).

Local peculiarities are also important while determining which benefits derive from mangroves in each region. Lee et al. (2014), for example, point out that effective coastal protection provided by mangroves depends on factors at landscape/geomorphic to community scales and local/species scales. It is therefore important to approach and include knowledge on local settings for mangrove management (Lee et al., 2014). Similarly, in the case of climate adaptation for protected areas, the process should be area-specific and consider ecological and social-economic conditions within and beyond the protected areas' boundaries (Rannow et al., 2014). Management strategies for mangrove conservation in Brazil, including designation and management of protected areas, and other protection instruments should therefore consider regional social-ecological peculiarities.

Assessment of the Protected Area System

In Brazil, protected areas have been shown to play a role in maintaining mangrove forest structure (Cavalcanti et al., 2009). In Indonesia, Miteva et al. (2015) concluded that protected areas reduced mangrove loss by about 14,000 hectares and avoided blue carbon emissions of approximately 13 million metric tons (CO2-equivalent). These results were significant only for a stricter category of protected area, which does not allow for resource extraction. This highlights the importance of knowing not only if mangroves are under some sort of legal protection, but also how, i.e., what the specific regulations for protection are—not to mention whether these mechanisms are actually applied on the ground, or are just “paper rules.”

Mangroves clearly have a high value for conservation and are largely threatened ecosystems. Despite this, conservation planning for ecosystem services provided by mangroves, as well as its tradeoffs with biodiversity, remains an incipient research field. The challenges of integrating methods that are currently applied to land and marine environments into the management of transitional and highly dynamic regions such as mangroves are minimally approached by the literature. Furthermore, it remains unknown to which extent decision makers apply modeling and decision-support tools, such as InVEST and Marxan (for more information on these tools, see Ball et al., 2009; Guerry et al., 2012, respectively).

A gap analysis to evaluate how well marine protected areas in Brazil meet conservation objectives for representation, connectivity, and risk-spreading revealed that objectives were far from fully attained (Magris et al., 2013). The protection of the marine environment was considered poor, with less than 1.9% of Brazil's marine jurisdiction within protected areas, from which only 0.14% within no-take areas. Only 23% of the ecosystems met the minimal number of replicates required by the risk-spreading objective. More positively, just over half (51%) of the no-take areas are a desirable distance apart. A systematic expansion is therefore needed to move toward an ecologically representative and functioning system of marine protected areas in Brazil. (Magris et al., 2013).

Brazil has a 10%-target for the protection of its marine territory, which should be implemented based on a central management strategy that takes into consideration the distinct regions and local specificities. However, while the need for more protected areas is comprehensible, some questions should be considered: Are there other categories of protected areas, currently not included in the Brazilian national reserves system, which represent possible good solutions for Brazilian conflicts in the conservation of mangroves? Why is it that so many protected areas do not have a management plan yet?

Instead of addressing existing issues in the network system, the designation of more marine protected areas, in the way it is currently taking place in Brazil, could actually decrease implementation capacity and effectiveness, not achieving much beyond the fulfillment of the country's internationally established marine biodiversity targets (Gerhardinger et al., 2011). Plus, a national effectiveness monitoring scheme still lacks for marine protected areas, even though Brazil has a large number of scientists and other professional capable of performing or assisting with such a task.

The previously mentioned data banks and the national-level macro-units proposed in this paper could be used to support the development of a national spatial plan that takes into consideration existing coastal marine protected areas, while also indicating conservation priorities outside these reserves, allowing for their expansion, the creation of corridors and of new areas.

Even if salt lands were to be considered an alternative for the allocation of economic activities inside mangrove areas, some questions would have to be addressed before allowing for this type of use: How to assign activities to the different habitats inside mangroves without negatively impacting the maintenance of interconnected systems? For example, if mangroves are valued, under an ecosystem service approach, for carbon storage, and the aquaculture performed in these areas is of high economic importance, how to balance these uses, without implying that salt flats are capable of absorbing any damaging activities as a trade-off to preserve the more highly appreciated mangrove forests?

Conclusions

Using systematic planning and ecosystem-based management as guiding strategies, we discussed the following approaches: (1) mangrove as a social-ecological system; (2) mangrove as an integrated system; (3) multi-scale planning; (4) standardized, GIS-based information and synthesis work; and (5) assessment of the protected area system. This is, to our knowledge, the first review that shows why and how these approaches can be used to tackle the apparent paradox of reconciling mangrove conservation and sustainable use.

Complexity and extremely high economic pressure on areas such as mangroves pose a proportionally large challenge to the conservation of these ecosystems. Thorough assessment and political recognition of their social-ecological importance can greatly contribute to a larger effort in working toward its conservation.

While environmental impacts associated with global climate change are generally expected to occur sometime in the future, many mangrove areas along the Brazilian coastline are already witnessing these impacts, and possible, future impacts have already been shown (Godoy and Lacerda, 2015). However, this is not taken into consideration in conservation strategies and legislation in Brazil, as can be easily concluded from the new Forest Code and the exclusion of salt flats from mangrove protection areas - this urgently calls for a revision of this legal instrument.

At the national level, policy-making lacks comprehensive understanding of how the various types of mangrove ecosystems along the coast function, in what social-ecological aspects they differ, and how those differences might be taken into account while planning for conservation. To support systematic conservation analyses and policy-making, mangrove ecosystems along the Brazilian coast could be grouped into planning macro-units, according to social-ecological features, geological traits and expected effects of climate change (Figure 1 and Table 1). While accounting for local peculiarities, it is important to also try and draw parallels to other mangrove ecosystems and try to learn from experiences from these ecosystems (successful restoration initiatives, co-management approaches, etc.).

Despite the widespread, mandatory reporting back of research, mangrove policy making lacks synthesized data to underpin management and conservation planning. Also, based on the deficiencies registered in the literature and the lessons learned from nearly 20 years of successes and challenges of the law that created the current national system of protected areas (BRASIL, 2000), the set of protected areas requires not only expansion but also re-structuring. Across the different countries where mangroves occur, there is a lack of evidence for the success of responses (as well as analysis of the interactions and feedbacks between different responses) in terms of their effects on declining ecological states of these ecosystems and on the services they provide.

While the need remains for more robust, unified legislation for mangrove conservation, the Brazilian experience shows that legal instruments are not enough for the effective protection of these ecosystems. Due to lack of proper evaluation of mangrove functioning, as in the case of the new Forest Code mentioned above, anthropogenic drivers have the potential to increase threats and reduce the effectiveness of conservation legislation and possible following actions. Permanent periodical assessment of mangrove conservation status and sustainable use, long-term monitoring of rehabilitation experiments, community-based management and continuous adaptation of legislation are required to curb drivers of change and their negative impacts on mangroves.

Developing and applying methods for an ecosystem-based management that deals with and helps overcome the complexity and pressure faced by mangroves is by definition an intricate and challenging task. Needless to emphasize, though, is the urgency to address these research gaps, in hopes that filling them up will contribute to the protection of one of our most valuable and most threatened ecosystems.

Author Contributions

RB designed the work, compiled literature sources, drafted, and wrote the manuscript. AF and LL helped compile literature sources, wrote parts of the manuscript, checked references, and critically revised the content of the paper. RB, AF, and LL approved the final version of the manuscript to be submitted.

Funding

This work was supported by the Brazilian Council for Scientific and Technological Development—CNPq (Process 290055/2014-8).

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

Special thanks to Prof. Dr. Matthias Wolff, for discussing and revising the manuscript. We thank Prof. Dr. Rebecca Rendle-Bühring and Dr. Aline Quadros for kindly revising and helping improve the manuscript. We are grateful to CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior/MEC, Brazil) for providing post-doctoral grant (AF). We also thank GLOMAR—Bremen International Graduate School for Marine Sciences, University of Bremen, for supporting the research and the University of Bremen for proving financial means for the publication of the manuscript.

Footnotes

1. ^http://panorama.solutions/en

2. ^http://es-partnership.org/

3. ^http://www.teebweb.org/

4. ^One example is the Babitonga Ativa Project, in southern Brazil (http://www.babitongaativa.com/).

References

Abdala, G., Saraiva, N., and Wesley, F. (2012). Plano de Manejo da Reserva Extrativista Caeté-Taperaçu - Volume I - Diagnóstico da Unidade de Conservação. Brasília: ICMBio.

Aheto, D. W., Kankam, S., Okyere, I., Mensah, E., Osman, A., Jonah, F. E., et al. (2016). Community-based mangrove forest management: implications for local livelihoods and coastal resource conservation along the Volta estuary catchment area of Ghana. Ocean Coastal Manage. 127, 43–54. doi: 10.1016/j.ocecoaman.2016.04.006

CrossRef Full Text | Google Scholar

Aide, T. M., Clark, M. L., Grau, H. R., López-Carr, D., Levy, M. A., Redo, D., et al. (2013). Deforestation and reforestation of Latin America and the Caribbean (2001–2010). Biotropica 45, 262–271. doi: 10.1111/j.1744-7429.2012.00908.x

CrossRef Full Text | Google Scholar

Alongi, D. M. (2002). Present state and future of the world's mangrove forests. Environ. Conserv. 29, 331–349. doi: 10.1017/S0376892902000231

CrossRef Full Text | Google Scholar

Arkema, K. K., Verutes, G. M., Wood, S. A., Clarke-Samuels, C., Rosado, S., Canto, M., et al. (2015). Embedding ecosystem services in coastal planning leads to better outcomes for people and nature. Proc. Natl. Acad. Sci. U.S.A. 112, 7390–7395. doi: 10.1073/pnas.1406483112

PubMed Abstract | CrossRef Full Text | Google Scholar

Aswani, S., Christie, P., Muthiga, N. A., Mahon, R., Primavera, J. H., Cramer, L. A., et al. (2012). The way forward with ecosystem-based management in tropical contexts: reconciling with existing management systems. Mar. Policy 36, 1–10. doi: 10.1016/j.marpol.2011.02.014

CrossRef Full Text | Google Scholar

Ball, I. R., Possingham, H. P., and Watts, M. (2009). “Marxan and relatives: software for spatial conservation prioritisation,” in Spatial Conservation Prioritisation: Quantitative Methods and Computational Tools, eds A. Moilanen, K. A. Wilson, and H. Possingham (Oxford: Oxford University Press), 185–195.

Google Scholar

Barbier, E. B. (2006). Natural barriers to natural disasters: replanting mangroves after the tsunami. Front. Ecol. Environ. 4, 124–131. doi: 10.1890/1540-9295(2006)004[0124:NBTNDR]2.0.CO;2

CrossRef Full Text | Google Scholar

Barbier, E. B., Hacker, S. D., Kennedy, C., Koch, E. W., Stier, A. C., and Silliman, B. R. (2011). The value of estuarine and coastal ecosystem services. Ecol. Monogr. 81, 169–193. doi: 10.1890/10-1510.1

CrossRef Full Text | Google Scholar

Benessaiah, K., and Sengupta, R. (2014). How is shrimp aquaculture transforming coastal livelihoods and lagoons in estero real, nicaragua? The need to integrate social–ecological research and ecosystem-based approaches. Environ. Manage. 54, 162–179. doi: 10.1007/s00267-014-0295-x

PubMed Abstract | CrossRef Full Text | Google Scholar

BRASIL (1953). Lei 1.806. Plano de Valorização Econômica da Amazônia. Available online at: http://www2.camara.leg.br/legin/fed/lei/1950-1959/lei-1806-6-janeiro-1953-367342-publicacaooriginal-1-pl.html

BRASIL (2000). Lei 9.985. Sistema Nacional de Unidades de Conservação da Natureza - SNUC. Available online at: http://www.mma.gov.br/port/conama/legiabre.cfm?codlegi=322

BRASIL (2006). Lei 11.428. Utilização e Proteção da Vegetação Nativa do Bioma Mata Atlântica. Available online at: http://www.planalto.gov.br/ccivil_03/_ato2004-2006/2006/lei/l11428.htm

BRASIL (2012). Lei 12.651. Código Florestal Brasileiro. Available online at: http://www.planalto.gov.br/ccivil_03/_ato2011-2014/2012/lei/l12651.htm

Berkes, F., and Folke, C. (1998). Linking Social and Ecological Systems: Management Practices and Social Mechanisms for Building Resilience. Cambridge: Cambridge University Press.

Google Scholar

Bezerra, D. B., and Brito, L. P. (2001). “Avaliação dos impactos ambientais produzidos pela Indústria Salineira do Rio Grande do Norte,” in 21o Congresso Brasileiro de Engenharia Sanitária e Ambiental, 4a Feira Internacional de Tecnologias de Saneamento Ambiental (João Pessoa: ABES), 1–47.

Google Scholar

Blythe, J., Cohen, P., Eriksson, H., Cinner, J., Boso, D., Schwarz, A.-M., et al. (2017). Strengthening post-hoc analysis of community-based fisheries management through the social-ecological systems framework. Mar. Policy 82, 50–58. doi: 10.1016/j.marpol.2017.05.008

CrossRef Full Text | Google Scholar

Böhnke-Henrichs, A., Baulcomb, C., Koss, R., Hussain, S. S., and de Groot, R. S. (2013). Typology and indicators of ecosystem services for marine spatial planning and management. J. Environ. Manage. 130, 135–145. doi: 10.1016/j.jenvman.2013.08.027

PubMed Abstract | CrossRef Full Text | Google Scholar

Carter, H., Schmidt, S., and Hirons, A. (2015). An international assessment of mangrove management: incorporation in integrated coastal zone management. Diversity 7:74. doi: 10.3390/d7020074

CrossRef Full Text | Google Scholar

Cavalcanti, V. F., Soares, M. L. G., Estrada, G. C. D., and Chaves, F. O. (2009). Evaluating mangrove conservation through the analysis of forest structure data. J. Coastal Res. 390–394.

Google Scholar

Cohen, M. C., and Lara, R. J. (2003). Temporal changes of mangrove vegetation boundaries in Amazonia: application of GIS and remote sensing techniques. Wetlands Ecol. Manage. 11, 223–231. doi: 10.1023/A:1025007331075

CrossRef Full Text | Google Scholar

Cohen, M. C. L., Lara, R. J., Smith, C. B., Angélica, R. S., Dias, B. S., and Pequeno, T. (2008). Wetland dynamics of Marajó Island, northern Brazil, during the last 1000 years. CATENA 76, 70–77. doi: 10.1016/j.catena.2008.09.009

CrossRef Full Text | Google Scholar

Cunha, I. A. (2006). Fronteiras da gestão: os conflitos ambientais das atividades portuárias. Rev. Adm. Públ. 40, 1019–1040. doi: 10.1590/S0034-76122006000600005

CrossRef Full Text | Google Scholar

Dahdouh-Guebas, F. (2002). The use of remote sensing and GIS in the sustainable management of tropical coastal ecosystems. Environ. Dev. Sustain. 4, 93–112. doi: 10.1023/A:1020887204285

CrossRef Full Text | Google Scholar

de Almeida, L. T., Olímpio, J. L. S., Pantalena, A. F., de Almeida, B. S., and de Oliveira Soares, M. (2016). Evaluating ten years of management effectiveness in a mangrove protected area. Ocean Coastal Manage. 125, 29–37. doi: 10.1016/j.ocecoaman.2016.03.008

CrossRef Full Text | Google Scholar

Donato, D. C., Kauffman, J. B., Murdiyarso, D., Kurnianto, S., Stidham, M., and Kanninen, M. (2011). Mangroves among the most carbon-rich forests in the tropics. Nat. Geosci. 4, 293–297. doi: 10.1038/ngeo1123

CrossRef Full Text | Google Scholar

Estrada, G. C. D., Soares, M. L. G., Fernadez, V., and de Almeida, P. M. M. (2015). The economic evaluation of carbon storage and sequestration as ecosystem services of mangroves: a case study from southeastern Brazil. Int. J. Bioivers. Sci. Ecosyst. Serv. Manage. 11, 29–35. doi: 10.1080/21513732.2014.963676

CrossRef Full Text | Google Scholar

FAO (2007). The World's Mangroves, 1980–2005: A Thematic Study in the Framework of the Global Forest Resources Assessment 2005. FAO Rome.

Ferreira, A. C., Ganade, G., and de Attayde, J. L. (2015). Restoration versus natural regeneration in a neotropical mangrove: effects on plant biomass and crab communities. Ocean Coastal Manage. 110, 38–45. doi: 10.1016/j.ocecoaman.2015.03.006

CrossRef Full Text | Google Scholar

Ferreira, A. C., Ganade, G., Morais Freire, F. A., and Attayde, J. L. (2013). Propagule predation in a Neotropical mangrove: the role of the Grapsid crab Goniopsis cruentata. Hydrobiologia 707, 135–146. doi: 10.1007/s10750-012-1416-2

CrossRef Full Text | Google Scholar

Ferreira, A. C., and Lacerda, L. D. (2016a). Degradation and conservation of Brazilian mangroves, status and perspectives. Ocean Coastal Manage. 125, 38–46. doi: 10.1016/j.ocecoaman.2016.03.011

CrossRef Full Text | Google Scholar

Ferreira, A. C., and Lacerda, L. D. (2016b). Reply to “On the impact of the Brazilian forest code on mangroves: a comment to Ferreira and Lacerda (2016)” by Ronaldo Ruy Oliveira-Filho et al. Ocean Coastal Manage. 132, 170–171. doi: 10.1016/j.ocecoaman.2016.08.003

CrossRef Full Text | Google Scholar

Friess, D. A., Thompson, B. S., Brown, B., Amir, A. A., Cameron, C., Koldewey, H. J., et al. (2016). Policy challenges and approaches for the conservation of mangrove forests in Southeast Asia. Conserv. Biol. 30, 933–949. doi: 10.1111/cobi.12784

PubMed Abstract | CrossRef Full Text | Google Scholar

Gerhardinger, L., Godoy, E. S., Jones, P. S., Sales, G., and Ferreira, B. (2011). Marine protected dramas: the flaws of the brazilian national system of marine protected areas. Environ. Manage. 47, 630–643. doi: 10.1007/s00267-010-9554-7

PubMed Abstract | CrossRef Full Text | Google Scholar

Giri, C., Ochieng, E., Tieszen, L. L., Zhu, Z., Singh, A., Loveland, T., et al. (2011). Status and distribution of mangrove forests of the world using earth observation satellite data. Global Ecol. Biogeogr. 20, 154–159. doi: 10.1111/j.1466-8238.2010.00584.x

CrossRef Full Text | Google Scholar

Glaser, M. (2003). Interrelations between mangrove ecosystem, local economy and social sustainability in Caeté Estuary, North Brazil. Wetlands Ecol. Manage. 11, 265–272. doi: 10.1023/A

CrossRef Full Text | Google Scholar

Glaser, M., and Da Silva Oliveira, R. (2004). Prospects for the co-management of mangrove ecosystems on the North Brazilian coast: whose rights, whose duties and whose priorities? Nat. Resour. Forum 28, 224–233. doi: 10.1111/j.1477-8947.2004.00092.x

CrossRef Full Text | Google Scholar

Glaser, M., and Glaeser, B. (2014). Towards a framework for cross-scale and multi-level analysis of coastal and marine social-ecological systems dynamics. Reg. Environ. Change 14, 2039–2052. doi: 10.1007/s10113-014-0637-5

CrossRef Full Text | Google Scholar

Godoy, M. D., and Lacerda, L. D. (2015). Mangroves response to climate change: a review of recent findings on mangrove extension and distribution. Anais Acad. Bras. Ciências 87, 651–667. doi: 10.1590/0001-3765201520150055

PubMed Abstract | CrossRef Full Text | Google Scholar

Granek, E. F., Polasky, S., Kappel, C. V., Reed, D. J., Stoms, D. M., Koch, E. W., et al. (2010). Ecosystem services as a common language for coastal ecosystem-based management. Conserv. Biol. 24, 207–216. doi: 10.1111/j.1523-1739.2009.01355.x

PubMed Abstract | CrossRef Full Text | Google Scholar

Guerry, A. D., Ruckelshaus, M. H., Arkema, K. K., Bernhardt, J. R., Guannel, G., Kim, C.-K., et al. (2012). Modeling benefits from nature: using ecosystem services to inform coastal and marine spatial planning. Int. J. Biodivers. Sci. Ecosystem Serv. Manage. 8, 107–121. doi: 10.1080/21513732.2011.647835

CrossRef Full Text | Google Scholar

Guimarães, A. S., Travassos, P., Souza Filho, P. W. M., Gonçalves, F. D., and Costa, F. (2010). Impact of aquaculture on mangrove areas in the northern Pernambuco Coast (Brazil) using remote sensing and geographic information system. Aquac. Res. 41, 828–838. doi: 10.1111/j.1365-2109.2009.02360.x

CrossRef Full Text | Google Scholar

Gutiérrez, N. L., Hilborn, R., and Defeo, O. (2011). Leadership, social capital and incentives promote successful fisheries. Nature 470, 386–389. doi: 10.1038/nature09689

PubMed Abstract | CrossRef Full Text | Google Scholar

Hein, L., van Koppen, K., de Groot, R. S., and van Ierland, E. C. (2006). Spatial scales, stakeholders and the valuation of ecosystem services. Ecol. Econ. 57, 209–228. doi: 10.1016/j.ecolecon.2005.04.005

CrossRef Full Text | Google Scholar

IUCN and UNEP-WCMC. (2017). The World Database on Protected Areas (WDPA) [On-line]. Available online at: www.protectedplanet.net

Juffe-Bignoli, D., Burgess, N. D., Belle, E., de Lima, M. G., Deguignet, M., Bertzky, B., et al. (2014). Protected Planet Report 2014.

Knoppers, B., Ekau, W., and Figueiredo, A. G. (1999). The coast and shelf of east and northeast Brazil and material transport. Geo Mar. Lett. 19, 171–178. doi: 10.1007/s003670050106

CrossRef Full Text | Google Scholar

Lacerda, L., Conde, J., Kjerfve, B., Alvarez-León, R., Alarcón, C., and Polanía, J. (2002). “American mangroves,” in Mangrove Ecosystems, ed L. D. D. Lacerda (New York, NY: Springer Berlin Heidelberg), 1–62.

Google Scholar

Latham, R., and Ricklefs, R. (1993). “Global patterns in diversity in mangrove floras. Species diversity in ecological communities,” in Historical and Geographical Perspectives, eds R. E. Ricklefs and D. Schluter (Chicago, IL: University of Chicago Press), 294–314.

Lee, S. Y., Primavera, J. H., Dahdouh-Guebas, F., McKee, K., Bosire, J. O., Cannicci, S., et al. (2014). Ecological role and services of tropical mangrove ecosystems: a reassessment. Global Ecol. Biogeogr. 23, 726–743. doi: 10.1111/geb.12155

CrossRef Full Text | Google Scholar

Lithgow, D., de la Lanza, G., and Silva, R. (in press). Ecosystem-based management strategies to improve aquaculture in developing countries: case study of marismas nacionales. Ecol. Eng. doi: 10.1016/j.ecoleng.2017.06.039

CrossRef Full Text | Google Scholar

Long, R. D., Charles, A., and Stephenson, R. L. (2015). Key principles of marine ecosystem-based management. Mar. Policy 57, 53–60. doi: 10.1016/j.marpol.2015.01.013

CrossRef Full Text | Google Scholar

Macintosh, D. J., and Ashton, E. C. (2005). Principles for a Code of Conduct for the Management and Sustainable Use of Mangrove Ecosystems. Aarhus: World Bank/ISME/cenTER.

Google Scholar

Magris, R. A., and Barreto, R. (2010). Mapping and assessment of protection of mangrove habitats in Brazil. Pan Am. J. Aquat. Sci. 5, 546–556.

Google Scholar

Magris, R., Mills, M., Fuentes, M., and Pressey, R. (2013). Analysis of progress towards a comprehensive system of marine protected areas in Brazil. Nat. Conserv. 11, 81–97. doi: 10.4322/natcon.2013.013

CrossRef Full Text | Google Scholar

Maia, L., Lacerda, L., Monteiro, L., and Souza, G. (2006). Atlas dos manguezais do nordeste do Brasil. Fortaleza: SEMACE 1:125.

Margules, C. R., and Pressey, R. L. (2000). Systematic conservation planning. Nature 405, 243–253. doi: 10.1038/35012251

PubMed Abstract | CrossRef Full Text | Google Scholar

Martínez, M. L., Intralawan, A., Vázquez, G., Pérez-Maqueo, O., Sutton, P., and Landgrave, R. (2007). The coasts of our world: ecological, economic and social importance. Ecol. Econ. 63, 254–272. doi: 10.1016/j.ecolecon.2006.10.022

CrossRef Full Text | Google Scholar

McConney, P., and Charles, A. (2008). “Managing small-scale fisheries: moving towards people-centred perspectives,” in Handbook of Marine Fisheries Conservation and Management, eds R. Q. Grafton, R. Hilborn, D. Squires, M. Tait, and M. Williams (New York NY: Oxford University Press), 532–545.

Google Scholar

McLeod, K. L., Lubchenco, J., Palumbi, S. R., and Rosenberg, A. A. (2005). Scientific Consensus Statement on Marine Ecosystem-Based Management Prepared by Scientists and Policy Experts to Provide Information About Coasts and Oceans to U.S. Policy-Makers. Available online at: http://www.marineplanning.org/pdf/Consensusstatement.pdf (Accessed August 04, 2017).

Medeiros, S. R. M., Carvalho, R. G., and Pimenta, M. R. C. (2015). A proteção do ecossistema manguezal à luz da lei 12.651/2012: novos desafios para a sustentabilidade dos manguezais do Rio Grande do Norte. Geotemas 4, 59–78.

Google Scholar

Menezes, M. P. M. d., Berger, U., and Mehlig, U. (2008). Mangrove vegetation in Amazonia: a review of studies from the coast of Pará and Maranhão States, north Brazil. Acta Amazonica 38, 403–420. doi: 10.1590/S0044-59672008000300004

CrossRef Full Text | Google Scholar

Meireles, A. J. A., Cassola, R. S., Tupinambá, S. V., and Queiroz, L. S. (2008). Impactos ambientais decorrentes das atividades da carcinicultura ao longo do litoral cearense, nordeste do Brasil. Revista Mercator 6, 83–106.

Miteva, D. A., Murray, B. C., and Pattanayak, S. K. (2015). Do protected areas reduce blue carbon emissions? A quasi-experimental evaluation of mangroves in Indonesia. Ecol. Econ. 119, 127–135. doi: 10.1016/j.ecolecon.2015.08.005

CrossRef Full Text | Google Scholar

MMA (2015). Resolução No. 9. Plano de Ação Nacional para Conservação das Espécies Ameaçadas e de Importância Socioeconômica do Ecossistema Manguezal - PAN Manguezal. Available online at: http://www.icmbio.gov.br/portal/images/stories/docs-plano-de-acao/pan-manguezais/retificada_-_portaria-aprovacao-pan-manguezais.pdf

Moura-Fé, M. M., Albuquerque, A. G. B. M., Freitas, E. M. N., and Barbosa, W. R. (2015). A Proteção do Ecossistema Manguezal pela Legislação Ambiental Brasileira. GEOgraphia 17, 126–153.

Google Scholar

Murdiyarso, D., Kauffman, J., Warren, M., Pramova, E., and Hergoualc'h, K. (2012). Tropical wetlands for climate change adaptation and mitigation science and policy imperatives with special reference to Indonesia. CIFOR Working Paper.

Google Scholar

Nagelkerken, I., Blaber, S., Bouillon, S., Green, P., Haywood, M., Kirton, L., et al. (2008). The habitat function of mangroves for terrestrial and marine fauna: a review. Aquat. Bot. 89, 155–185. doi: 10.1016/j.aquabot.2007.12.007

CrossRef Full Text | Google Scholar

Nayak, P. K., and Berkes, F. (2014). Linking global drivers with local and regional change: a social-ecological system approach in Chilika Lagoon, Bay of Bengal. Reg. Environ. Change 14, 2067–2078. doi: 10.1007/s10113-012-0369-3

CrossRef Full Text | Google Scholar

Oliveira-Filho, R. R., Rovai, A. S., Menghini, R. P., Coelho Júnior, C., Schaeffer Novelli, Y., and Cintrón, G. (2016). On the impact of the Brazilian Forest Code on mangroves: a comment to Ferreira and Lacerda (2016). Ocean Coast. Manage. 132, 36–37. doi: 10.1016/j.ocecoaman.2016.08.002

CrossRef Full Text

Orchard, S. E., Stringer, L. C., and Quinn, C. H. (2015). Environmental entitlements: institutional influence on mangrove social-ecological systems in Northern Vietnam. Resources 4, 903–938. doi: 10.3390/resources4040903

CrossRef Full Text | Google Scholar

Paulo Moutinho. (2015). Is zero deforestation possible for the Brazilian Amazon? Available online at: https://ensia.com/voices/is-zero-deforestation-possiblefor-the-brazilian-amazon/ [Accessed 19.04 2016].

PEDRR (2010). Demonstrating the role of ecosystem-based management for disaster risk reduction. Partnership for Environment and Disaster Risk Reduction (PEDRR), 113.

Pendleton, L., Donato, D. C., Murray, B. C., Crooks, S., Jenkins, W. A., Sifleet, S., et al. (2012). Estimating global “Blue Carbon” emissions from conversion and degradation of vegetated coastal ecosystems. PLoS ONE 7:e43542. doi: 10.1371/journal.pone.0043542

PubMed Abstract | CrossRef Full Text | Google Scholar

Plataforma Brasil. (2015). Brasil agora possui a maior faixa protegida de manguezais do mundo. Available online at: http://www.brasil.gov.br/meio-ambiente/2015/01/brasil-cria-maior-faixa-protegida-de-manguezais-do-mundo [Accessed 19.09.2016].

Prates, A. P. L., Gonçalves, M. A., and Rosa, M. R. (2012). Panorama da Conservação dos Ecossistemas Costeiros e Marinhos no Brasil. Brasília: MMA, 152.

Queiroz, L. S., Rossi, S., Calvet-Mir, L., Ruiz-Mallén, I., García-Betorz, S., Meireles, A.J.d.A., et al. (2017). Neglected ecosystem services: highlighting the socio-cultural perception of mangroves in decision-making processes. Ecosyst. Serv. 26, 137–145. doi: 10.1016/j.ecoser.2017.06.013

CrossRef Full Text | Google Scholar

Rannow, S., Macgregor, N. A., Albrecht, J., Crick, H. Q., Förster, M., Heiland, S., Salvà-Prat, J., et al. (2014). Managing protected areas under climate change: challenges and priorities. Environ. Manage. 54, 732–743. doi: 10.1007/s00267-014-0271-5

PubMed Abstract | CrossRef Full Text | Google Scholar

Ray, R., Ganguly, D., Chowdhury, C., Dey, M., Das, S., Dutta, M. K., et al. (2011). Carbon sequestration and annual increase of carbon stock in a mangrove forest. Atmospheric Environ. 45, 5016–5024. doi: 10.1016/j.atmosenv.2011.04.074

CrossRef Full Text | Google Scholar

Reed, M. S. (2008). Stakeholder participation for environmental management: a literature review. Biol. Conserv. 141, 2417–2431. doi: 10.1016/j.biocon.2008.07.014

CrossRef Full Text | Google Scholar

Richards, C., Blackstock, K., and Carter, C. (2004). Practical Approaches to Participation, SERG Policy Brief No. 1, eds C. E. Carter and C. L. Spash Aberdeen: Macaulay Institute.

Google Scholar

Rife, A. N., Erisman, B., Sanchez, A., and Aburto-Oropeza, O. (2013). When good intentions are not enough… Insights on networks of “paper park” marine protected areas. Conserv. Lett. 6, 200–212. doi: 10.1111/j.1755-263X.2012.00303.x

CrossRef Full Text | Google Scholar

Rodrigo Cassola. (2010). TEEB case: Conserving forests through grants, Brazil. Available online at: http://doc.teebweb.org/wp-content/uploads/2013/01/Conserving-forests-through-grants-Brazil.pdf [Accessed 19.04 2017].

Rotich, B., Mwangi, E., and Lawry, S. (2016). Where Land Meets the Sea: A Global Review of the Governance and Tenure Dimensions of Coastal Mangrove Forests. Bogor; Washington, DC: CIFOR and USAID Tenure and Global Climate Change Program.

Google Scholar

Rovai, A. S., Menghini, R. P., Schaeffer-Novelli, Y., Molero, G. C., and Coelho, C. (2012). Protecting Brazil's coastal wetlands. Science 335, 1571–1572. doi: 10.1126/science.335.6076.1571

CrossRef Full Text | Google Scholar

Roy, A. K. D., and Alam, K. (2012). Participatory forest management for the sustainable management of the Sundarbans mangrove forest. Am. J. Environ. Sci. 8, 549–555. doi: 10.3844/ajessp.2012.549.555

CrossRef Full Text | Google Scholar

Saint-Paul, U., and Schneider, H. (2016). The need for a holistic approach in mangrove-related fisheries research: a specific review of the German and Brazilian research project MADAM. J. Fish Biol. 89, 601–618. doi: 10.1111/jfb.12880

PubMed Abstract | CrossRef Full Text | Google Scholar

Santos, L. C. M., Gasalla, M. A., Dahdouh-Guebas, F., and Bitencourt, M. D. (2017). Socio-ecological assessment for environmental planning in coastal fishery areas: a case study in Brazilian mangroves. Ocean Coast. Manage. 138, 60–69. doi: 10.1016/j.ocecoaman.2017.01.009

CrossRef Full Text | Google Scholar

Santos, L. C. M., Matos, H. R., Schaeffer-Novelli, Y., Cunha-Lignon, M., Bitencourt, M. D., Koedam, N., et al. (2014). Anthropogenic activities on mangrove areas (São Francisco River Estuary, Brazil Northeast): a GIS-based analysis of CBERS and SPOT images to aid in local management. Ocean Coast. Manage. 89, 39–50. doi: 10.1016/j.ocecoaman.2013.12.010

CrossRef Full Text | Google Scholar

Sathirathai, S., and Barbier, E. B. (2001). Valuing mangrove conservation in Southern Thailand. Contemp. Econ. Policy 19, 109–122. doi: 10.1111/j.1465-7287.2001.tb00054.x

CrossRef Full Text | Google Scholar

Schaeffer-Novelli, Y. (1999). Grupo de Ecossistemas: Manguezal, Marisma e Apicum. São Paulo: Programa Nacional da Diversidade Biológica–Pronabio. Projeto de Conservação e Utilização Sustentável da Diversidade Biológica Brasileira–Probio. Subprojeto Avaliação e Ações Prioritárias para a Conservação da Biodiversidade da Zona Costeira e Marinha.

Google Scholar

Schaeffer-Novelli, Y., Cintrón-Molero, G., Adaime, R. R., and de Camargo, T. M. (1990). Variability of mangrove ecosystems along the Brazilian coast. Estuaries 13, 204–218. doi: 10.2307/1351590

CrossRef Full Text | Google Scholar

Schaeffer-Novelli, Y., Cintrón-Molero, G., Soares, M. L. G., and De-Rosa, T. (2000). Brazilian mangroves. Aquat. Ecosyst. Health Manage. 3, 561–570. doi: 10.1016/S1463-4988(00)00052-X

CrossRef Full Text | Google Scholar

Schmidt, A. J., Bemvenuti, C. E., and Diele, K. (2013). Sobre a definição da zona de apicum e a sua importância ecológica para populações de caranguejo-uçá, Ucides cordatus (Linnaeus, 1763). Boletim Tecnico Cientifico do CEPENE 19, 9–25.

Google Scholar

Schmitt, K., and Duke, N. C. (2015). “Mangrove management, assessment and monitoring,” in Tropical Forestry Handbook, eds L. Pancel and M. Köhl (Berlin; Heidelberg: Springer-Verlag), 30.

Google Scholar

Silva, J., Nobre, A., Manzatto, C., Joly, C., Rodrigues, R., Skorupa, L., et al. (2011). O Código Florestal e a Ciência: Contribuição para o Diálogo. São Paulo: Sociedade Brasileira para o Progresso da Ciência, SBPC.

Sobrinho, M., and Andrade, A. (2009). O desafio da conservação de manguezais em áreas urbanas: identificação e análise de conflitos socioambientais no Manguezal do Pina-Recife-PE-Brasil. Unimontes Científica 11, 8–16.

Souza, F. E. S., and Ramos e Silva, C. A. (2010). Ecological and economic valuation of the Potengi estuary mangrove wetlands (NE, Brazil) using ancillary spatial data. J. Coast. Conserv. 15, 195–206. doi: 10.1007/s11852-010-0133-0

CrossRef Full Text | Google Scholar

Souza Filho, P. W. M., and Paradella, W. R. (2002). Recognition of the main geobotanical features along the Bragança mangrove coast (Brazilian Amazon Region) from Landsat TM and RADARSAT-1 data. Wetlands Ecol. Manag. 10, 121–130. doi: 10.1023/A:1016527528919

CrossRef Full Text | Google Scholar

Spalding, M., Kainuma, M., and Collins, L. (2010). World atlas of mangroves. A collaborative project of ITTO, ISME, FAO, UNEP-WCMC. UNESCO-MAB, UNU-INWEH and TNC. London: Earthscan.

Stephenson, R. L., Paul, S., Pastoors, M. A., Kraan, M., Holm, P., Wiber, M., et al. (2016). Integrating fishers' knowledge research in science and management. ICES J. Mar. Sci. 73, 1459–1465. doi: 10.1093/icesjms/fsw025

CrossRef Full Text | Google Scholar

Tenório, G. S., Souza-Filho, P. W. M., Ramos, E. M., and Alves, P. J. O. (2015). Mangrove shrimp farm mapping and productivity on the Brazilian Amazon coast: environmental and economic reasons for coastal conservation. Ocean Coast. Manage. 104, 65–77. doi: 10.1016/j.ocecoaman.2014.12.006

CrossRef Full Text | Google Scholar

Turner, R. K., van den Bergh, J. C. J. M., Söderqvist, T., Barendregt, A., van der Straaten, J., Maltby, E., et al. (2000). Ecological-economic analysis of wetlands: scientific integration for management and policy. Ecol. Econ. 35, 7–23. doi: 10.1016/S0921-8009(00)00164-6

CrossRef Full Text | Google Scholar

UNEP (2014). The Importance of Mangroves to People: A Call to Action. Cambridge: United Nations Environment Programme World Conservation Monitoring Centre.

Valiela, I., Bowen, J. L., and York, J. K. (2001). Mangrove forests: one of the world's threatened major tropical environments. Bioscience 51, 807–815. doi: 10.1641/0006-3568(2001)051[0807:MFOOTW]2.0.CO;2

CrossRef Full Text | Google Scholar

Vasconcellos, M., and Diegues, A. C., and Kalikoski, D. C. (2011). “Coastal fisheries of Brazil,” in Coastal Fisheries of Latin America and the Caribbean, eds S. Salas, R. Chuenpagdee, A. Charles, and J. C. Seijo (Rome: FAO), 73–116. FAO Fisheries and Aquaculture Technical Paper. No. 544.

Google Scholar

Walters, B. B., Rönnbäck, P., Kovacs, J. M., Crona, B., Hussain, S. A., Badola, R., et al. (2008). Ethnobiology, socio-economics and management of mangrove forests: a review. Aquat. Bot. 89, 220–236. doi: 10.1016/j.aquabot.2008.02.009

CrossRef Full Text | Google Scholar

Ward, R. D., Friess, D. A., Day, R. H., and MacKenzie, R. A. (2016). Impacts of climate change on mangrove ecosystems: a region by region overview. Ecosyst. Health Sustainab. 2:e01211. doi: 10.1002/ehs2.1211

CrossRef Full Text | Google Scholar

Woodroffe, C. D., Rogers, K., McKee, K. L., Lovelock, C. E., Mendelssohn, I. A., and Saintilan, N. (2016). Mangrove sedimentation and response to relative sea-level rise. Ann. Rev. Mar. Sci. 8, 243–266. doi: 10.1146/annurev-marine-122414-034025

PubMed Abstract | CrossRef Full Text | Google Scholar

Zoe Sullivan (2014). Brazil's shellfishing communities blighted by industrial pollution. Available online at: https://www.theguardian.com/global-development/2014/mar/04/brazil-shellfishing-communities-pernambuco-industrial-pollution [Accessed 19.09 2016].

Keywords: coastal-marine spatial planning, social-ecological system, marine protected area, ecosystem service, GIS-based data, Brazil

Citation: Borges R, Ferreira AC and Lacerda LD (2017) Systematic Planning and Ecosystem-Based Management as Strategies to Reconcile Mangrove Conservation with Resource Use. Front. Mar. Sci. 4:353. doi: 10.3389/fmars.2017.00353

Received: 28 April 2017; Accepted: 18 October 2017;
Published: 07 November 2017.

Edited by:

Lyne Morissette, M—Expertise Marine, Canada

Reviewed by:

Daniel Pinero, Universidad Nacional Autónoma de México, Mexico
Andrew M. Fischer, University of Tasmania, Australia

Copyright © 2017 Borges, Ferreira and Lacerda. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Rebecca Borges, rebecca.borges@uni-bremen.de