Marine protected areas for demersal elasmobranchs in highly exploited Mediterranean ecosystems

https://doi.org/10.1016/j.marenvres.2020.105033Get rights and content

Highlights

  • Proactive area-based protection strategy towards elasmobranch conservation is proposed.

  • Elasmobranch conservation priority areas were identified in the southern part of the western Mediterranean Sea.

  • The addition of complex cost layers and zoning strategy did not alter conservation priority areas for elasmobranchs.

Abstract

Marine ecosystems are complex socio-ecological systems where sustainable solutions can be best gained by satisfying both conservation and socioeconomic demands. Concretely, the Mediterranean Sea is facing a huge demand of resources and marine activities while hosting abundant and unique biodiversity. It is considered an important elasmobranch hotspot where seventy-two elasmobranch species are present in the basin. Despite the recognised importance of elasmobranchs as umbrella species, to date only a small number of marine protected areas have been designated towards their protection. The paucity of spatially-explicit abundance data on elasmobranchs often precludes the designation of these areas to protect these marine predators. Here, we aimed to identify marine areas to protect elasmobranch species by means of a systematic spatial planning approach. We first estimated the spatial distribution of five elasmobranch species (three sharks and two rays) in the western Mediterranean Sea and then applied Marxan decision support tools to find priority marine conservation areas. We found that the five elasmobranchs are distributed in coastal and slope areas of the southern waters of the study area while in the northern region they are abundant in the continental slope and towards offshore waters. Conservation priority areas were identified in the southern part of the western Mediterranean. Adding more complex cost layers and zoning to the analysis did not alter conservation priority areas, confirming such areas are highly consistent and highly important for elasmobranch protection. The marine conservation priority areas identified here can contribute to designate a proactive area-based protection strategy towards elasmobranch conservation, related species and the habitats that they depend in the western Mediterranean Sea.

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

References (98)

  • J. Navarro et al.

    The relative roles of the environment, human activities and spatial factors in the spatial distribution of marine biodiversity in the Western Mediterranean Sea

    Prog. Oceanogr.

    (2015)
  • M.G. Pennino et al.

    Modeling sensitive elasmobranch habitats

    J. Sea Res.

    (2013)
  • R.S. Pomeroy et al.

    How is your MPA doing? A methodology for evaluating the management effectiveness of marine protected areas

    Ocean Coast. Manag.

    (2005)
  • C. Rigby et al.

    Patterns in life history traits of deep-water chondrichthyans

    Deep. Res. Part II Top. Stud. Oceanogr.

    (2015)
  • R.a. Ronconi et al.

    The role of seabirds in Marine Protected Area identification, delineation, and monitoring: introduction and synthesis

    Biol. Conserv.

    (2012)
  • D.B. Segan et al.

    An interoperable decision support tool for conservation planning

    Environ. Model. Software

    (2011)
  • M.E. Watts et al.

    Marxan with Zones: software for optimal conservation based land- and sea-use zoning

    Environ. Model. Software

    (2009)
  • B. Worm et al.

    Global catches, exploitation rates, and rebuilding options for sharks

    Marine Policy

    (2013)
  • I. Afán et al.

    An adaptive method for identifying marine areas of high conservation priority

    Conserv. Biol.

    (2018)
  • T. Agardy

    Marine Protected Areas and Ocean Conservation

    (1997)
  • Y. Aldebert

    Demersal resources of the Gulf of Lions (NW Mediterranean). Impact of exploitation on fish diversity

    Vie Milieu

    (1997)
  • J.A. Ardron et al.

    Marxan good practices handbook, version 2. Pacific marine analysis and research association

  • I.R. Ball et al.

    Marxan (V. 1.8.2

  • N.C. Ban et al.

    Promise and problems for estimating management costs of marine protected areas

    Conserv. Lett.

    (2011)
  • C. Barría et al.

    Unraveling the ecological role of uncommon and endangered elasmobranchs in the Mediterranean Sea using a comparative approach

    Mar. Ecol. Prog. Ser.

    (2015)
  • M. Beger et al.

    Incorporating asymmetric connectivity into spatial decision making for conservation

    Conserv. Lett.

    (2010)
  • J. Bertrand et al.

    Contribution on the distribution of elasmobranchs in the Mediterranean (from MEDITS surveys)

    Biol. Mar. Mediterr.

    (2000)
  • J.A. Bertrand et al.

    The general specifications of the MEDITS surveys

    Sci. Mar.

    (2008)
  • M. Bode et al.

    Cost-effective global conservation spending is robust to taxonomic group

    Proc. Natl. Acad. Sci. U.S.A.

    (2008)
  • K.P. Burnham et al.

    Multimodel inference

    Socio. Methods Res.

    (2004)
  • C. Capapé et al.

    Diet of the marbled electric ray Torpedo marmorata (chondrichthyes: Torpedinidae) off the languedocian coast (southern France, northern Mediterranean)

    Ann. Ser. Hist. Nat.

    (2007)
  • C. Capapé et al.

    Torpedinidae

  • S.C. Clarke et al.

    Global estimates of shark catches using trade records from commercial markets

    Ecol. Lett.

    (2006)
  • R. Coelho et al.

    Life history of a wide-ranging deepwater lantern shark in the north-east Atlantic, Etmopterus spinax (Chondrichthyes: Etmopteridae), with implications for conservation

    J. Fish. Biol.

    (2008)
  • M. Coll et al.

    Assessing fishing and marine biodiversity changes using Fishers' perceptions: the Spanish Mediterranean and gulf of Cadiz case study

    PloS One

    (2014)
  • M. Coll et al.

    The Mediterranean Sea under siege: spatial overlap between marine biodiversity, cumulative threats and marine reserves

    Global Ecol. Biogeogr.

    (2012)
  • M. Coll et al.

    The biodiversity of the Mediterranean Sea: estimates, patterns, and threats

    PloS One

    (2010)
  • M. Coll et al.

    “Low-hanging fruit” for conservation of marine vertebrate species at risk in the Mediterranean Sea

    Global Ecol. Biogeogr.

    (2015)
  • R.M. Daigle et al.

    Operationalizing ecological connectivity in spatial conservation planning with Marxan Connect

    Methods Ecol. Evol.

    (2020)
  • R. Daly et al.

    Refuges and risks: evaluating the benefits of an expanded MPA network for mobile apex predators

    Divers. Distrib.

    (2018)
  • L.N.K. Davidson et al.

    Global marine protected areas to prevent extinctions

    Nat. Ecol. Evol.

    (2017)
  • N. Dulvy et al.

    The Conservation Status of Sharks, Rays and in the Mediterranean Sea

    (2016)
  • N.K. Dulvy et al.

    Extinction risk and conservation of the world's sharks and rays

    Elife

    (2014)
  • M. Estrada

    Primary production in the northwestern Mediterranean

    Sci. Mar.

    (1996)
  • EU

    Communication from the Commission to the European Parliament and the Council on a European Community Action Plan for the Conservation and Management of Sharks

    (2009)
  • P.G.H. Evans

    Marine Protected Areas and marine spatial planning for the benefit of marine mammals

    J. Mar. Biol. Assoc. UK

    (2018)
  • FAO

    The State of Mediterranean and Black Sea Fisheries

    (2018)
  • F. Ferretti et al.

    Loss of large predatory sharks from the Mediterranean Sea

    Conserv. Biol.

    (2008)
  • F. Ferretti et al.

    Patterns and ecosystem consequences of shark declines in the ocean

    Ecol. Lett.

    (2010)
  • Cited by (15)

    • Distribution models of deep-sea elasmobranchs in the Azores, Mid-Atlantic Ridge, to inform spatial planning

      2022, Deep-Sea Research Part I: Oceanographic Research Papers
      Citation Excerpt :

      An approach combining depth, area and gear related management measures may therefore reconcile species conservation and the continuation of fishing in the deep-sea. Our study attempts to explore relationships of the occurrence of deep-sea elasmobranchs with environmental variables beyond depth (Martin et al., 2012; Pennino et al., 2013; Lauria et al., 2015; Giménez et al., 2020). In general, the performance of our models was good and comparable with similar studies (Martin et al., 2012; Lauria et al., 2015), although distribution modelling approaches come with several caveats, extensively discussed in Parra et al. (2017).

    • Spatial-temporal variation of the Western Mediterranean Sea biodiversity along a latitudinal gradient

      2022, Ecological Indicators
      Citation Excerpt :

      In this context, a more detailed spatial analysis is also recommended to confirm those areas with high biodiversity change as well as the most vulnerable areas or those that are most impacted (such as the North Catalan Sea) or may be recovering (such as the Alboran Sea o the Channel). This can be a useful information to be considered for the design and the establishment of marine protected areas (MPAs) and other effective area-based conservation measures (OECMs) for the protection of biodiversity and the sustainable use of marine resources (e.g., Coll et al. 2015; Giménez et al., 2020). Our study, however, presented some limitations as some traits like the trophic level or the mean size may not capture real changes in the traits but the relative change in biomasses.

    • Expanding protected areas to encompass the conservation of the endangered common dolphin (Delphinus delphis) in the Alboran Sea

      2021, Marine Environmental Research
      Citation Excerpt :

      Indeed, these methods have the key advantage of maximizing conservation targets, minimizing potential costs, and optimizing the allocation of limited economic resources to define more meaningful and sustainable MPAs. In other words, it minimizes the conflict between wildlife conservation and important environmental services though the spatial redistribution of economic sectors (Afán et al., 2018; Ball et al., 2009; Beyer et al., 2016; Giménez et al., 2020). Area-based approaches in marine conservation have been extensively promoted by several European Union (EU) directives, especially the Habitats Directive [92/43/EEC], which implemented the Natura 2000 network of protected areas as the centerpiece of the EU conservation strategy.

    View all citing articles on Scopus
    View full text