The interplay of natural variability, productivity and management of the benthic ecosystem in the Humboldt Current System: Twenty years of assessment of Concholepas concholepas fishery under a TURF management system

Highlights

• A long-term analysis based in four trophic models was done in order to compare benthic ecosystems.

• The interanual dynamics of loco resource is coupled with fluctuations in the associated communities.

• Fishing not only impacts the exploited species but also the entire ecosystem.

• Environmental variability is suggested as an important driver of community and loco resource trajectories.

Abstract

Areas with controlled access, as Marine Protected Areas (MPAs) and Territorial Use Rights for Fisheries (TURF), are conceived as tools to contribute to the ecosystem conservation and fisheries sustainability. Management and Exploitation Areas for Benthic Resources (MEABR), a TURF system implemented in Chile, offers the opportunity to test this hypothesis. The management in these areas is based mainly on the assessment of the resources population status, with low or no consideration of the ecological - environmental effects that condition their productivity. In this study, we evaluate ecological trophic dynamics of the rocky subtidal community configuration in four periods along 20 years of the highly productive Choros Island MEABR – MPA, including one pre-implementation period. In this TURF, the carnivore gastropod Concholepas concholepas (locally known as “loco”) is the main targeted resource. The performance of ecosystem indexes of this TURF increased during the MEABR regime as compared with the pre MEABR implementation. Nevertheless, the most conspicuous increase occurred in 2013, primarily in response to changes in environmental conditions and their direct and indirect effects on community interactions. The analysis of interactions between guilds indicated that the main drivers were the interaction between the primary productivity, prey abundance and the top predator loco. This produces a long-term dynamic of the system modulated by the interplay of environmental variability, which at benthic community level increases prey populations thus sustaining increased loco productivity. In turn, intensified predation of loco reduces its prey. This produces natural productivity fluctuations, which counteract the expected outcome of management actions, impeding to achieve stable landings in the long term.

Introduction

The protection of coastal populations and ecosystems, through spatially explicit tools, can promote ecologically and economically sustainable fisheries within or outside their boundaries (Hughes et al., 2005; Sladek-Nowlis and Friedlander, 2005; Claudet et al., 2006; Halpern et al., 2010; McCay and Jones, 2011). Controlling human impact within such spaces is an opportunity to foster our understanding of the ecology of coastal communities, and evaluate their efficiency through resulting changes in the ecosystem (Bohnsack, 1998; Guénette et al., 2014). Chile has implemented this type of tools, with Marine Protected Areas (MPA) and Territorial Use Rights for Fisheries (TURF), with controlled fishing and monitoring, thus offering a unique opportunity (San Martín et al., 2010).

Management of areas with controlled human access (MPAs, TURFs, etc.), but allowing controlled fisheries, could contribute to avoid direct stock overexploitation (Botsford et al., 2003; Denny and Babcock, 2004) as well as indirect negative decreases in fishing yields through ecosystem disturbance (Claudet et al., 2006). Therefore, effectiveness of these type of areas must be assessed not only in regard to fisheries improvements, but also on its ecosystem basis (Pitcher et al., 2002), because among others, the removal of target species that play a keystone role on community structure, may alter the overall community functioning (Botsford et al., 1997; Crain and Bertnes, 2006; González et al., 2016). Studying these areas can be useful to test hypotheses at the ecosystem level, such as trophic relationships (Halpern, 2003). Changes in community structure can emerge due to changes in the food web after MPA or TURF implementation, where trophic cascades may cause decreases in prey abundance after increases in predator abundance (Pinnegar et al., 2000). Changes in community structure could reflect trophic complexity and increased primary and secondary production within these areas (Babcock et al., 1999).

Community models for MPAs based on trophic relationships (Watson et al., 2000; Pitcher et al., 2002) have allowed to study the effects of MPA implementation. Studies have shown how and where primary and secondary production, as well as biomass, are transferred among trophic levels (Watson et al., 2000; González et al., 2016). Nevertheless, these studies generally lack a temporal dimension of analysis, which limits the general conclusions about the functional ecological effects of MPAs that can be drawn out of it (Halpern et al., 2010; Pinnegar et al., 2000). In addition, there is no explicit evaluation of the effects that fishing (as the removal of a particular target species) has on the structure and energy transfer of the supporting coastal benthic communities, when this is permitted within these areas (Riascos et al., 2016); and, whether the implementation of a multispecies management program is required to meet conservation or fisheries objectives (Ortiz et al., 2010; González et al., 2016).

Understanding the flow of matter and energy through any community network allows to assess the influence of each component upon the entire food web (Ulanowicz and Baird, 1999). The Ecopath with Ecosim (EwE) software quantifies ecosystem macroscopic indexes regarding its structure and dynamics. It also estimates the propagation of direct and indirect effects through the networks as response to different management/harvest scenarios within marine ecosystems (Christensen et al., 2005). This analysis can provide vital information for Ecosystem-Based Fisheries Management (EBFM), which aims to maintain ecosystems by conserving ecosystem structure and function (Garcia and Cochrane, 2005). To understand the ecosystem responses to the harvest of a particular species it is necessary to understand its trophic role and the trophic control mechanisms of the community. Bottom up and top down control mechanisms have been widely studied and the effects of removing top predators or low trophic level species in each case can be predicted. Nevertheless, in benthic communities there is compiling evidence that mixed control mechanisms might be more realistic (Ortiz et al., 2013). Thus, to predict and conclude about the efficiency of areas with controlled human activity, it is necessary to conduct an adequate long-term monitoring and scientific study to re-evaluate species-community interactions (García-Charton et al., 2004). Studies based using initial and historical data can allow to question if an apparent increase in the health of an ecosystem is linked to protection from detrimental uses or is better explained by the initial features of the protected area. This type of evaluation must consider that the natural variability can result in biased interpretations (Underwood and Chapman, 2003) as well as the effects of its propagation through trophic and non-trophic interactions across the community structure (Kéfi et al., 2015), when they are not properly taken into account.

Coastal marine areas in the Humboldt System Current (HSC) are one of the most productive around the world (Halpin et al., 2004; Montecino et al., 2004; Thiel et al., 2007). This system is characterized by the upwelling of cold nutrient rich waters responsible for the dramatic increase of biological productivity that exerts a bottom-up effect on the system (Thatje et al., 2008). Upwelling intensity is heterogeneous along the coast, and the relative distance to upwelling centers plays an important role in the succession and structure of hard-bottom communities (Broitman et al., 2001; Narváez et al., 2006). Coastal circulation is strongly influenced by topography, and physical oceanographic processes also affect offshore/onshore and alongshore advection, and therefore impact larval and plankton retention, dispersal and onshore delivery (Marín et al., 2001; Castilla et al., 2002; Wieters et al., 2003; Narváez et al., 2004). Moreover, the Chilean coast presents a strong inter-annual variability in upwelling and hydrographic characteristics associated with El Niño-La Niña periods, which may modulate recruitment variability and community structure (Gaymer et al., 2010; Moreno et al., 1998; Thiel et al., 2007). Therefore, upwelling and ENSO-related conditions affect primary productivity (Iriarte and González, 2004; Wieters et al., 2003), zooplankton community composition (Escribano et al., 2004), fish population dynamics (Halpin et al., 2004), larval dispersal (Poulin et al., 2002a, Poulin et al., 2002b), benthic algal growth (Wieters et al., 2003), benthic-pelagic coupling and population dynamics of benthic organisms (Castilla and Camus, 1992; Thiel et al., 2007; Gaymer et al., 2010).

Management and Exploitation Areas for Benthic Resources (MEABRs, a type of TURF) are spatially explicit conservation and/or management instruments included in Chilean legislation that have been implemented throughout the coast since 1988. MEABRs were not originally intended to protect ecosystem functions and diversity, but to sustainably exploit a few target species. A general management plan applies to these fisheries: 20% of the exploitable target species biomass is extracted annually after direct stock assessment (González et al., 2006). Currently, the MEABRs constitute a network of over 479 discrete areas, covering over 1100 km² spreaded along the coast. Therefore, MEABRs are supposed to give substantial benefits for biodiversity conservation, because they are effective no-take areas for all species, apart from the target species (generally two to five) selected each year for harvesting. This could represent an important ancillary network of add-on effects for species that are not directly connected to the management policies (Gelcich et al., 2008). MPAs and MEABRs might overlap in space, in the example we will analyse the MEABRs extends from the intertidal down to 25 m depth being comprised within a larger MPA.

The main species fished exclusively within the boundaries of MEABRs is the gastropod Concholepas concholepas (loco). Its fishery is regulated by setting each year, and for each MEABR a total allowable catch (TAC) after single-species stock assessment (González et al., 2006). The loco is recognized as a keystone species along the Chilean coast, affecting the community dynamics under top-down control (Duran and Castilla, 1989; Stotz, 1997). However, the management of benthic fisheries in the MEABRs has ignored the processes related to the ecosystem structure and function, despite its stated objective is to contribute to ecosystem-based management (Botsford et al., 1997; Rice, 2011). The aim of this study was to compare the long-term performance of benthic ecosystem of Choros Island MEABR (C–I MEABR), an exploitation area embedded in a wider MPA, using an analytical framework of ecological network, and to assess its impact/dependence on loco fisheries. Ecosystem changes under the present management strategy and environmental conditions were assessed for 4 time-series over a 20-year period.