Marine protected areas for demersal elasmobranchs in highly exploited Mediterranean ecosystems
Introduction
Several human activities, such as fishing, industrial activity, energy production between others, take place in natural environments worldwide with significant deleterious effects on ecosystems, including marine ecosystems (Halpern et al., 2015; Venter et al., 2016). Such effects in the oceans are expected to expand into deeper and more distant marine areas as “blue growth” strategies are promoted (Katsanevakis et al., 2017). Threats imposed by humans are ubiquitous and are causing important changes in marine biodiversity and ecosystems functioning (Halpern et al., 2015; Jackson et al., 2001). Exploitation, pollution, eutrophication and habitat loss are among the most impacting for the survival and conservation of marine species (Halpern et al., 2015). Additionally, other growing impacts such as climate change or the introduction of alien species are of concern (Kelleher, 1999; Korpinen and Andersen, 2016; Pomeroy et al., 2005).
Policymakers face increasing pressure to design and apply effective and robust regulations to preserve marine biodiversity. One common approach is the implementation of Marine Protected Areas (MPAs) - spatially designed and managed to protect marine ecosystems, habitats and species (Agardy, 1997). Site-based approaches, such as MPAs, can enhance biodiversity conservation if they are designed with a science-based approach, accounting for areas of high abundance of species of conservation concern or focal biodiversity targets as well as the distribution of their main threats (Davidson and Dulvy, 2017) and with an effective enforcement regime (Horta e Costa et al., 2016).
Predators and other marine megafauna have been proposed as useful organisms to define and identify MPAs because their spatial distribution and population parameters integrate seasonal spatial and abundance variation of lower trophic levels and on broad areas (Hooker and Gerber, 2004; Ronconi et al., 2012, but see Sergio et al., 2008). They can act as a biodiversity surrogates when other biodiversity data is not available. In some cases, imperilled species lack spatial-explicit abundance data because they are rare and thus difficult to track and, so relying in species that are more abundant but with similar ecological requirement may serve as a good surrogate to use in marine spatial planning. Marine predators have been, in turn, strongly impacted by human activities, and several species and taxa are currently considered of immediate conservation concern (Hooker et al., 2011; Daly et al., 2018). Top consumers such as some marine mammals and seabirds are commonly used as focal species to designate MPAs (e.g., Afán et al., 2018; Arcos et al., 2012; Evans, 2018; Gormley et al., 2012). In comparison, sharks and rays have been overlooked (Davidson and Dulvy, 2017; MPAtlas, 2016) but they also need spatial-explicit protection. Their life-history characteristics such as low fecundity, slow growth and late reproductive maturity make them highly vulnerable to human activities (Coelho and Erzini, 2008; Frisk et al., 2005; García et al., 2008; Rigby and Simpfendorfer, 2015). As well as the fact that they are targeted for food and medicinal use (unlike seabirds and marine mammals), and suffer high mortality due to fishery by-catch (Clarke et al., 2006). The depletion of the populations of sharks and rays can lead, in turn, to important cascading effects on lower trophic levels (Ferretti et al., 2010; Myers et al., 2007) so their protection can serve as a proactive strategy (i.e. before the species or habitats become threatened) to conserve the whole marine food web.
Awareness of the vulnerability and ecological role of elasmobranchs is leading to increased conservation attention (Barría et al., 2015; Davidson and Dulvy, 2017; Gallagher et al., 2012). The European Commission, in particular, adopted in 2009 the first Action Plan for the conservation and management of elasmobranchs to reverse the impacts of shark depletions and rebuild stocks under threat (EU, 2009). This plan considers the implementation of management actions to protect priority elasmobranch habitats, the reduction of fisheries by-catch, and the study of current and expected impacts to design efficient strategies for the preservation of elasmobranch biodiversity (Katsanevakis et al., 2009). Even so, in some geographic areas such as the Mediterranean Sea, which is considered an important elasmobranch hotspot of extinction risk at global scale (Dulvy et al., 2014), existing marine protected areas do not guarantee current European species targets (Micheli et al., 2013a, Micheli et al., 2013b; Coll et al., 2015). Declines of both medium- and large-size elasmobranchs have been observed in the last decades (Ferretti et al., 2008; IUCN, 2019) and only few species still remain in highly impacted sites (Aldebert, 1997; Coll et al., 2013; Ferretti et al., 2008; Malak et al., 2011). These negative trends could reflect a lack of representation of elasmobranchs species in existing marine protected areas, as they were not explicitly accounted for in current MPA design (MPAtlas, 2016).
In this study, we aimed for first time to identify priority areas for protecting the demersal elasmobranch community in the western Mediterranean Sea. We applied a systematic conservation planning approach comparing identifyed priorities with the current MPA network to evaluate its usefulness in relation to the management of demersal elasmobranchs. Due to the scarce information regarding the spatial distribution of demersal sharks and rays, here we focused on five species of elasmobranch (three sharks and two rays), for which accurate abundance and distribution data is available from a long-term systematic survey conducted in the Mediterranean Sea (Bertrand et al., 2000). These species encompass a wide range of ecological requirements and their well-documented distribution can be informative of ecologically relevant areas for the wider demersal elasmobranch community, formerly more diverse and nowadays much degraded (Aldebert, 1997; García et al., 2008; Rigby and Simpfendorfer, 2015; Simpfendorfer and Kyne, 2009).
As a first step, we identified areas of high ecological value by analysing the spatial distribution of abundances of the five selected species and their relationships with main environmental variables. We then explored different conservation planning alternatives by considering both the distribution and their main threat (i.e. fishing activity) and also including other potential threats (surface temperature anomalies, concentration of pesticides and fertilizers, ocean pollution, and inorganic pollution) in a cost-effectiveness framework (Watts et al., 2017). Increased levels of complexity were considered in the analyses by accounting separately for single or multiple threats combinations as well as by considering different zonation plans limiting local human use (fisheries) at different levels in different parts of the protected areas.
Section snippets
Study area
The study area included the Spanish continental shelf and upper slope (up to 800 m depth) of the western Mediterranean Sea, from the “Cap de Creus” in the north to the “Cabo de Palos” in the south (Fig. 1). This area has been identified as a highly impacted marine area within the Mediterranean Sea, where multiple threats operate simultaneously (Coll et al., 2012; Micheli et al., 2013a; Ramírez et al., 2018). Despite these impacts, the area still hosts relative high levels of marine diversity
Elasmobranch distributions
In total, 143 of 169 sampled 0.1°grid cells were occupied at least once during the study period by one of the study species, 83 by two, 32 by three, 7 by four and none by all of them. S. canicula showed the highest abundance values (mean ± SD: 364 ± 954 ind·km−2), followed by G. melastomus (81 ± 217 ind·km−2), R. asterias (4 ± 12 ind·km−2), T. marmorata (4 ± 12 ind·km−2) and E. spinax (3 ± 12 ind·km−2). The spatial distribution of the five species also differed between them. S. canicula was
Discussion
In this study, we applied for the first time a systematic spatial planning approach focused on elasmobranch species in the western and, in general, in the Mediterranean Sea. Our results can be used to inform proactive area-based protection for the demersal elasmobranch community inhabiting the Mediterranean waters under Spanish jurisdiction, to avoid a further decrease in their conservation status as it has been already documented in several areas of the basin (Aldebert, 1997; Ferretti et al.,
Declaration of competing interest
We declare no conflict of interest.
Acknowledgements
The authors also express their gratitude to all the people incolved in the MEDITS surveys. Thanks to Isabel Afán from the Laboratorio de SIG y Teledetección (LAST) of the Estación Biológica de Doñana – CSIC and Francisco Ramírez from ICM-CSIC for their useful discussions and help with spatial data analysis. JG partially carried out the analysis of the present study during his research internship at the Centre for Biodiversity and Conservation Science (School of Biological Sciences, University
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