Patterns of variation of intertidal species of commercial interest in the Parque Litoral Norte (north Portugal) MPA: Comparison with three reference shores

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<ul><li><p>sp</p><p>itaBrags/n,</p><p>1 February 2012Accepted 5 February 2012</p><p>Keywords:MPAs</p><p>a consequence, there is an increasing need for effective manage-ment measures aimed at conserving the diversity of species andhabitats and ensuring a sustainable use of living resources(Sherman, 1994). The implementation of marine protected areas(MPAs) is a common tool aimed at achieving these goals (Agardy,1994; Allison et al., 1998; Roberts et al., 2001; Rodrigues et al.,</p><p>Halpern, 2003; Pelletier et al., 2005; Garca-Charton et al., 2008). Inaddition, indirect effects, such as trophic cascades, within or aroundMPAs have been hypothesized and in some cases supported byempirical studies (Lindberg et al., 1998; Castilla, 1999; Pinnegaret al., 2000; Sala et al., 1998a; Shears and Babcock, 2002; Micheliet al., 2005). Such effects depend in complex ways on life-traits,such as dispersal abilities, of species (McClanahan and Mangi,2000) and features of the reserve, including size, age and design(e.g. Botsford et al., 2003; Claudet et al., 2008).</p><p>* Corresponding author. Tel.: 351 223401818; fax: 351 223390608.</p><p>Contents lists available at</p><p>m</p><p>se</p><p>Marine Environmental Research 77 (2012) 60e70E-mail address: ibertocci@ciimar.up.pt (I. Bertocci).1. Introduction</p><p>The impacts of human activities in coastal areas are of increasingconcern for ecologists, policy-makers and the general public(Jackson et al., 2001; Lotze et al., 2006). Anthropogenic distur-bances can modify the physical environment and directly andindirectly affect patterns of distribution, abundance and diversity ofpopulations and assemblages on a global scale (Vitousek et al.,1997). Removing target and non-target species and habitats canalso indirectly alter food webs and biological interactions (Fogartyand Murawski, 1998; Sala et al., 1998a; Guidetti, 2006). As</p><p>2004), through the preservation of stocks of commercial species,the conservation of natural habitats and the protection of speciesconsidered of particular importance due to their functional role(e.g. King and Beazley, 2005 and references therein) or just theircultural or aesthetic value (Palumbi, 2001).</p><p>The effectiveness of marine reserves has been widely assessedmostly by comparing patterns of density or size of exploited shspecies among protected and reference areas (Dayton et al., 2000;Garca-Charton et al., 2000). A number of previous studies havedocumented increases in abundance and/or size of target speciesinside MPAs compared with unprotected areas (for reviews, seeRocky intertidalSpatial and temporal heterogeneityParacentrotus lividusMytilus galloprovincialisManagementPortugal0141-1136/$ e see front matter 2012 Elsevier Ltd.doi:10.1016/j.marenvres.2012.02.003order to support and implement their management, but it is complicated by the large natural variabilityin space and time of distribution and abundance of natural populations. Here, we tested the hypothesisthat patterns of total abundance and size-frequency distribution of two intensively harvested intertidalspecies (the sea urchin Paracentrotus lividus and the mussel Mytilus galloprovincialis) differed betweena protected and three reference shores along the rocky coast of north Portugal. Response variables werein terms of mean values and measures of variance at different spatial scales (from centimetres to metres)and over time (along a period of about 12 months). A further comparison involved the estimation of thereproductive potential of sea urchins, quantied as variations of Gonad Index (GI gonad dry weight/body dry weight 100) at the scale of shore. Results did not generally support a predictable direct effectof protection, as the total abundance and the abundance of larger individuals of both species and GI didnot differ between the MPA and reference shores. However, a considerable temporal and spatial vari-ability at smaller scales was detected for several response variables. Such ndings have implications formanagement of MPAs, highlighting the need for sampling designs properly replicated in space and time,in order to examine their effectiveness, and for considering spatial and temporal heterogeneity of targetpopulations and driving processes as a criterion for their implementation and design.</p><p> 2012 Elsevier Ltd. All rights reserved.Received 20 December 2011Received in revised formMarine Protected Areas (MPAs) are world-wide established with the aim of conserving biodiversity andpreventing overexploitation of marine organisms. Evaluating the effectiveness of MPAs is needed inArticle history:Patterns of variation of intertidal specieLitoral Norte (north Portugal) MPA: Com</p><p>Iacopo Bertocci a,*, Rula Dominguez a, Cristiano FreaCIIMAR/CIMAR, Centro Interdisciplinar de Investigao Marinha e Ambiental, Rua dosbDepartment of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre</p><p>a r t i c l e i n f o a b s t r a c t</p><p>Marine Environ</p><p>journal homepage: www.elAll rights reserved.of commercial interest in the Parquearison with three reference shores</p><p>s a, Isabel Sousa-Pinto a,b</p><p>as, 289, 4050-123 Porto, Portugal4169-007 Porto, Portugal</p><p>SciVerse ScienceDirect</p><p>ental Research</p><p>vier .com/locate /marenvrev</p></li><li><p>nmeIntertidal benthic assemblages on rocky shores are particularlyexposed to human activities, such as harvesting gastropods andalgae for commercial purposes (Hockey and Bosman, 1986; Castillaand Bustamante, 1989; Lasiak, 1998; Castilla, 1999), removingspecies for bait (Kingsford et al., 1991) and collecting shellsaesthetically appealing (Underwood, 1993a), and to the effects oftrampling associated to them (e.g. Brosnan and Crumrine, 1994).Analogously to ndings from subtidal assemblages, it has beendocumented that the removal of predators can drastically affectintertidal interaction webs and thus deeply alter patterns ofbiodiversity of rocky shores (Hockey and Branch, 1984; Lindberget al., 1998; Castilla, 1999). In other cases, however, no signicanteffects of MPAs were indicated on intertidal organisms (e.g. Lasiak,1998). Actually, the effects of MPAs are generally variable indirection and scale, so that examining such heterogeneity and itsbasic mechanisms is key to improve our knowledge of the effec-tiveness of existing MPAs and to implement the design of presentand planned ones (Halpern and Warner, 2002).</p><p>Comparing the mean abundance of populations between pro-tected and reference areas is complicated by the large variability inpatterns of distribution and abundance of natural populations atdifferent spatial and temporal scales, rising a number of issuesconcerning tests of hypotheses about protection (Schneider, 1994;Underwood and Chapman,1996; Benedetti-Cecchi et al., 2003). Thecentral point involves the use of sampling design able to separatethe real effects of protection from other uncontrolled sources ofvariation (e.g. Garca-Charton and Prez-Ruzafa, 1999; Garca-Charton et al., 2000; Fraschetti et al., 2005). In addition, effectivemanagement in terms of number, size and design of MPAs shouldspecically take into account the spatial and temporal variability ofspecies, in order to guarantee the protection of a representativesample of species and assemblages of a region and themaintenanceof the ecological processes that are responsible for such patterns(Horne and Schneider, 1995; Underwood and Chapman, 1996;Schwartz, 1999; Thrush et al., 2000; Benedetti-Cecchi et al., 2003).This requires comparing MPAs and reference areas not only interms of mean density and/or size of populations, but also in termsof patterns of variance at different scales, an approach rarely foundin the ecological literature (but see Benedetti-Cecchi et al., 2003).</p><p>The issues above were addressed in the present study on pop-ulations of two species of commercial interest, the sea urchin Par-acentrotus lividus and the mussel Mytilus galloprovincialis, sampledin an MPA and three reference shores in north Portugal. Bothspecies are among the most exploited animals from rocky coastsand shallow subtidal habitats for commercial and recreationalpurposes. P. lividus is subject to intense harvesting particularly inthe Mediterranean Sea (Guidetti et al., 2004; Ceccherelli et al.,2009, 2011), on Atlantic coasts of France and Iberian peninsula(Barnes and Crook, 2001) and in Ireland (Byrne, 1990) due to itsgonads, that represent an appreciated delicacy of high marketvalue. Analogously, there is a long history of harvesting M. gallo-provincialis for food and bait (e.g. de Lumley, 1975) and this speciesis currently severely exploited, particularly in some periods, incountries such as Italy (Airoldi et al., 2005), Spain (Rius and Zabala,2008) and Portugal (Rius and Cabral, 2004). Effects of harvestrestrictions on populations of P. lividus (Guidetti et al., 2005;Gianguzza et al., 2006; Guidetti, 2007; Pais et al., 2007; Ceccherelliet al., 2009, 2011) and M. galloprovincialis (Rius and Zabala, 2008)have been examined only in recent years, providing contrastingndings. These ranged from increases in total abundance(Gianguzza et al., 2006) or in the abundance of large individuals(Rius and Cabral, 2004; Ceccherelli et al., 2011) of the exploitedspecies in protected compared to reference conditions, to theopposite pattern (Pais et al., 2007), to complex indirect effects</p><p>I. Bertocci et al. / Marine Enviromediated by biological and abiotic factors. These includedpredators (Sala and Zabala, 1996; Sala, 1997; Guidetti et al., 2005),wave exposure (Micheli et al., 2005), the design of the reserve (Riusand Zabala, 2008) and interactions between biological and physicaldrivers (Hereu et al., 2005). Therefore, examining the effects ofprotection on populations of such species in unstudied areas is ofoverwhelming commercial and ecological importance.</p><p>Here, we compared patterns of abundance and distribution ofP. lividus and M. galloprovincialis between the Parque Litoral NorteMPA and reference shores in north Portugal. Although the directionof possible effects of protection was difcult to predict due to therange of contrasting direct and indirect effects of different factorslikely driving such patterns in the studied system, we tested thegeneral hypotheses that patterns of total abundance (number ofindividuals for sea urchins and percentage cover for mussels) and ofdistribution of individuals among size classes of both species at theMPA differed from those at similar rocky shores located in the samegeographical area, but not subject to the same managementmeasures. These hypotheses were examined both in terms of meanvalues of response variables and their temporal and spatial vari-ances (Warwick and Clarke, 1993; Chapman et al., 1995), by meansof a sampling repeated at different times and at a hierarchy ofspatial scales (Underwood, 1992, 1994), from 10 s centimetres(among replicate quadrates) to 10 s metres (between sites in eachshore) at each of the protected and the reference shore (kilometresapart). In addition, we tested the hypothesis that the reproductivepotential of P. lividus differed between the protected and thereference condition at the scale of the shore. This was based on theknowledge that, for instance, reductions of the reproductive outputoccur under large densities, and consequent food limitation, of seaurchins (e.g. Levitan, 1995; Tomas et al., 2005), although fertiliza-tion rates can be positively related with the density of adults (e.g.Whale and Peckham, 1999).</p><p>2. Methods</p><p>2.1. Study site</p><p>The studywas carried out between October 2010 and September2011 in rocky intertidal habitats of a protected and three referenceshores (stretches of coast 100 s m to 1 km long, 5e10 km apart) innorth Portugal. The tidal regime along the Portuguese coast issemidiurnal, with the largest spring tides of 3.5e4 m. The typicalrocky shore is granitic and the coast is exposed to prevailingnorthwest oceanic swells, particularly intense during the winter(Arajo et al., 2005). The protected shore (Mar: 41 340 5800 N, 08</p><p>480 1900 W) is located within Parque Litoral Norte (PLN), an MPAestablished in 1987 on about 18 km of coast and the adjacent sea,between the city of Apulia in the south to the estuary of the Neivariver in the north. The sampled shore is the largest stretch of rockycoast available within PLN, as the rest of the coast includes just verysmall rocky areas, interspersed among large sandy beaches.Although PLN does not include no-take areas (see http://portal.icnb.pt/ICNPortal/vPT2007-AP-LitoralNorte/HomepageAreasProtegidas.htm for detailed information on legislation, organizationandmanagement) all shing and harvesting activities there requirespecial permits, that are provided only to a small number of locallyresident professionals (to our knowledge, only two licences wereprovided to professional harvesters of sea urchins within PLN andthese are represented by small family units; on the contrary, shoresout of PLN are visited also by professional and recreationalharvesters from nearby areas, such as Galicia in Spain) using, due toboth cultural and law constraints, artisanal techniques. Fishing, inparticular, is mostly based on family activities using trammel nets,longlines and traps as typical gear, whose size and number are</p><p>ntal Research 77 (2012) 60e70 61limited by the reduced size of boats and involved people (two</p></li><li><p>nmepersons per boat in most cases). The use of any tool for harvestingintertidal organisms is prohibited by law, making this activity inprinciple limited to removal by hand during daytime and low tideonly. Enforcement is carried out by a special police sections formarine issues (Polcia Maritima) and by local port authorities(Capitanias do Porto) with recurrent visits at sea and along theshore. The artisanal trait of these activities, however, is associatedto a lack of proper records on collected quantities of organisms, as,for instance, no ofcial devices for recording shed quantities arerequired on board of small boats and most sh and intertidalorganisms are directly sold to consumers (i.e. restaurants andprivate citizens without entering large and better ruled markets).The three reference shores (Amorosa: 41 380 3000 N, 08 490 2300 W;Praia Norte: 41 410 5700 N, 08 510 1300 W;Moledo: 41 500 2500 N, 08</p><p>520 2700 W) were randomly selected from those available alongabout 25 km of coast north of PLN. The coast south of PLN is almostexclusively sandy for more than 60 km, preventing to interspersereference shores between both geographic sides of the MPA.Reference shores outside theMPAwere selected as being analogousto the protected one in terms of a number of macroscopic physicaltraits, including spatial extent (i.e.100 sm long), type of substratum(i.e. mostly granite), slope (i.e. almost at), exposure (i.e. at allshores, the coastline was oriented almost exactly form north tosouth, being exposed to the same prevailing westerly swell andwinds) and accessibility (i.e. all shores were located at comparabledistance from the main road and easily accessible walking fromnear parkings). Both the protected and the reference shores aretypically domi...</p></li></ul>

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