The role of estuarine macrofaunal patterns for the management of marine protected areas in a changing world

Highlights

• Integrate science and management is a challenge to improve conservation strategies.

• Macrofaunal patterns were assessed and further discussed with local stakeholders.

• High mud content in the sediment were correlated with reduced macrofaunal richness.

• Taxa richness can be an indicator related to initial ecosystem changes.

• These indicators are useful to implementing an adaptive ecosystem-based management.

Abstract

The integration of biodiversity knowledge with management needs in coastal protected ecosystems is a current challenge that requires a social-ecological perspective, especially in view of the current scenario regarding climate changes. At the southeastern Brazil, estuaries inside protected areas highlight as a great source of ecosystem services connected to the biodiversity, such as the food provisioning for local communities (i.e. fishery supply). However, climate change models considering the last four decades alert to an annual rainfall increase in the region, threatening the estuarine biodiversity and its associated ecosystem services. Here, we evaluated how estuarine macrofaunal distribution could be used as ecological indicators to support the stakeholders management needs in subtropical Marine Protected Areas (MPAs). The intertidal macrofauna distribution was assessed along physical gradients in estuaries within MPAs of the southeastern Brazil, testing the effects of salinity and sediment properties on taxa richness. Then, implications of these ecological findings were discussed with the local users and managers of the MPAs, aiming to stipulate indicators and management proposals considering the rainfall increase predicted for the region. We found that macrofauna community varied between estuarine zones along the physical gradients. High values of mud and organic content in the sediment were correlated with reduced taxa richness in the upper estuarine zone, indicating high vulnerability of biodiversity to a possible estuarine mud input connected to the expected rainfall increase. Stakeholders noted that this knowledge could assist with spatial planning for an adaptive management of the biodiversity use rules on the MPAs, with focus on the ecosystem services conservation (ecosystem-based management). Stakeholders suggested using biodiversity hotspots to guide estuarine areas classification (no-take zones and sustainable use zones), maintaining the resources use rules adaptable according to the biodiversity changes. In this regard, our data revealed important bioindicators, such as the macrofaunal richness, which can be monitored as “early signals” to assess eventual ecosystem alterations related to the climate changes. These signals can include loss in taxa richness, extirpation of species exclusively found on the lower estuarine zone (sensitives to mud input) and changes in the distribution or abundance of dominant taxa. We suggest that understanding the relationships between macrofaunal indicators and ecosystems services, associated with continuous monitoring, are the key steps to implementing an adaptive ecosystem-based management of these protected estuaries in the current changing scenario, contributing to decision making at local scale that respond to global challenges, as the UN Ocean Decade.

Introduction

Improvement of decision-making by the integration of scientific knowledge with the management needs in marine systems is a current challenge, mainly in front of the ongoing climate changes, that are threatening all ecosystems around the world. Groundbreaker integrated approaches are necessary to understand changes in social systems caused by ecological conditions and changes in ecological systems associated with social practices (Vieira, Berkes, & Seixas, 2005). In this way, humans are considered part of the process (i.e., human-in-ecosystem) as opposed to an external disturbance to ecological systems (Davidson-Hunt and Berkes, 2003, Gunderson and Allen, 2010). Considering this perspective, obtaining knowledge of biodiversity patterns summed to the understanding of multiple stakeholders about the ecosystem management needs are important elements in the creation of appropriate strategies for natural resource use and conservation (Turra et al., 2013).

Among the coastal social-ecological systems, the estuaries integrate terrestrial, marine and freshwater environments and provide a range of ecosystem services that benefit local communities and large human activities, such as fisheries, ports and tourism (Lana & Bernardino, 2018). Estuaries display high levels of dynamism and a complex physical environment that create important physical gradients (Attrill & Rundle, 2002). These gradients influence the distribution of estuarine biodiversity, ecosystem services and resources (Aura et al., 2017, Whitfield et al., 2012) and, consequently, the human communities dependent on the resources. Understanding these relationships can improve management strategies, aiming the conservation of ecosystem services and estuarine resources connected to biodiversity patterns and processes (Sheng et al., 2019, Turra et al., 2013).

Benthic macrofauna is a significant component of estuarine biomass connected to fundamental ecosystem services. For instance, macrobenthic communities serve in the roles of biological production (Bissoli & Bernardino, 2018), encompassing species of direct importance for human consumption (Ellison, 2008). Furthermore, macrofaunal species are key elements on the diet of fishes (Contente et al., 2009, Wakabara et al., 1993), also implying an indirect importance of macrofauna for the fishery resources supply. Other ecosystem services are also regulated by macrofaunal species, such as the sediment bioturbation and the estuarine cycling of nutrients and organic matter (Murray et al., 2017, Natálio et al., 2017). Based on these connections, patterns of macrofaunal richness and community composition can signal the state of vulnerability of specific estuarine services and functions, guiding decision-making to control the associated pressures (Dolbeth et al., 2007, Gomes and Bernardino, 2020, Palmer et al., 2015). Therefore, estuarine macrobenthic communities could be important bioindicators for monitoring ecosystem changes and improving management and adaptation strategies.

In fact, the use of macrofauna as bioindicators to improve coastal management is not new and has historically been applied to assess and control pressures in the context of marine pollution (e.g. Pearson & Rosenberg, 1978). Nevertheless, this tool can also be a key element in the current climate change scenario, considering the close relationship between macrofauna and the estuarine physical drivers (Bernardino et al., 2016). For instance, data regarding macrofauna distribution reflect that salinity is the key driver regulating species richness along the estuarine gradient (Attrill and Rundle, 2002, Whitfield et al., 2012). Similarly, evidences from many estuaries revealed that zones with great salinity values present great species richness (Giménez et al., 2005, Josefson and Hansen, 2004, Lana et al., 1997, Pollack et al., 2011, Ysebaert et al., 1993). Other findings showed that sediment properties along this gradient (e.g., grain size and organic content) could be important factors influencing macrofauna richness and abundance (Ellis et al., 2006, Thrush et al., 2003, Thrush et al., 2004). At the current climate change context, previsions point out that rainfall patterns will change around the world, changing the freshwater input on estuarine systems (e.g. Marengo et al., 2010). Rainfall changes can modify the gradients of salinity and sediments across the estuarine zones (Palmer et al., 2015, Thrush et al., 2004), ultimately changing the macrofaunal patterns and their ecosystem services associated. In this context, the changes in macrofaunal patterns along estuarine gradients have a potential usage as signals to detect ecosystem changes connected to climate drivers.

However, despite these investigations, many gaps in the knowledge of macrofaunal distribution along estuarine gradients persist and the potential bioindicators that could be used to support management and adaptations strategies are still not clear. Most of the studies regarding this topic were performed at estuaries located in temperate regions (e.g., Attrill and Rundle, 2002, Giménez et al., 2005, Ysebaert et al., 1993). Studies performed on tropical and subtropical estuaries usually present no clear spatial relationship between salinity and intertidal macrofauna richness (Ferreira et al., 2020, Mariano and Barros, 2015, Morais et al., 2016). In addition, the tropical estuaries studied are primarily located in urban or polluted areas (Barros et al., 2014, Barros et al., 2012, Barros et al., 2008, Ourives et al., 2011). These gaps highlight a scarcity of scientific support for the management of conserved estuaries in tropical and subtropical important sites, such as the Marine Protected Areas (MPAs), for instance. MPAs encompass estuaries with great importance for coastal traditional communities dependent on different ecosystem services and resources which could be vulnerable to the expected changes (McLeod, Salm, Green, & Almany, 2009). Therefore, beyond the scientific gaps to be filled, it is also important to understand the viewpoints of MPAs stakeholders (Mills et al., 2020), mainly regarding how these ecological data can serve to support management strategies to conserve their practices.

Based on that, our goal was to assess how macrofaunal distribution could be used as ecological indicators to support management strategies of subtropical estuaries, within MPAs, in a climate change context. To fill this goal in a holist way, we search connections between the distributional patterns of intertidal macrofauna across physical gradients and the management needs of the MPA stakeholders. First, two questions were investigated to evaluate macrofaunal ecological gradients: (1) How does the intertidal macrofauna community change among different zones along the estuarine gradient? (2) Is the richness of those macrofaunal communities connected with spatial changes in salinity and sediment properties? Second, we assessed the understanding of MPAs stakeholders (i.e. local users and managers) regarding the implications of these ecological gradients for ecosystem management at the MPAs. On this step, we aimed to find possible indicators based on macrofaunal gradients that could be useful to evaluate future impacts, related to the expected climate changes, on the ecosystem services of interest to the stakeholders. Therefore, we stimulated the integration of our scientific finds with the stakeholders management needs aiming to discuss proposals for decision-making. In the context of our study area, this integration still remains a barrier to management of MPAs (Ranzani & Serafini, 2020).