Artificial Marine Micro-Reserves Networks (AMMRNs): an innovative approach to conserve marine littoral biodiversity and protect endangered species

Depósito de investigación de la Universidad de Sevilla https://idus.us.es/ “This is an Accepted Manuscript of an article published in Marine Ecology on May 2014 available at ttps://doi.org/10.1111/maec.12167.” Artificial Marine Micro-Reserves Networks (AMMRNs): an innovative approach to conserve marine littoral biodiversity and protect endangered species Jos e ´ C. García- G o ´ mez 1 , Jos e ´ M. Guerra-García1, Free Espinosa1, Manuel J. Maestre1, Georgina Rivera- Ingraham1,2, Darren Fa3, Alexander R. Gonz a ´ lez 1 , Aurora Ruiz-Tabares1 & Carlos M. L o ´ pez -F e ´ 1 1 Laboratorio de Biología Marina, Facultad de Biología, Universidad de Sevilla, Seville, Spain 2 Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany 3 The Gibraltar Museum, Gibraltar, UK Keywords Artificial Marine Reserve Networks; breakwaters; coastal engineering; endangered and invasive species; harbours and ports; reserve effect. Correspondence José M. Guerra-García, Laboratorio de Biología Marina, Facultad de Biología, Universidad de Sevilla, Avenida Reina Mercedes 6, 41012 Seville, Spain. E-mail: [email protected] Accepted: 8 February 2014 doi: 10.1111/maec.12167 Abstract Coastal engineering works, especially the outer breakwaters of ports where environmental conditions are usually good, often constitute new habitats for marine littoral species. Their potential indirect contribution to the regeneration and conservation of protected species opens up a new perspective in protection of marine biodiversity. This is particularly true when these works harbour, as we show here, important reproductive populations of species that are threatened or even in danger of extinction. We provide integrated data on protected marine species in Southern Iberia established on different substrata (quarried dolomitic rocks, concrete cubic blocks, concrete tetrapods and vertical concrete walls) that are used in the construction of artificial levees that could potentially be Artificial Marine Micro-Reserves (AMMRs). We also present the first evidence of the ‘reserve effect’ in potential AMMRs and we discuss the need for the creation of AMMRs including their effective networking (AMMRNs), supporting data for which has been observed by studying coastal facilities subjected to strict access restrictions (for security reasons, not conservation). These facilities have acted as valuable proxies and, in reality, potentially act as AMMRs, as well as having a role in helping to detect and control invasive species. We discuss the ecological engineering aspects related to the design and type of materials used in coastal constructions with a view to aiding the integration of these into existing coastal ecosystems as well as promoting greater settlement of species and therefore increases in biodiversity. Finally, the environmental implications of AMMRNs within the future implementation strategy of the Water Framework Directive 2000/60 EC are also discussed. Introduction Many authors have reported on the increased rates of extinction and depletion of many of the world’s species in historical times (Terborgh 1974; Primack & Ros 2002). The marine sphere, particularly coastal environments, is an area where human impacts are particularly keenly felt, given that a significant proportion of the world’s population live by, and actively use and exploit, the coast (Jackson et al. 2001). There is a growing need for innovative approaches to environmental conservation that integrate the various stakeholders in a synergistic manner to the benefit of all concerned. Such approaches are urgently needed given that anthropic demands on coastlines are expected to increase in the future (Airoldi et al. 2005). Many reasons are given for the conservation of species and habitats (Balmford et al. 2002) involving modern developments in systematic conservation planning and design of Marine Protected Areas (MPAs) (Beger et al. 2010; Mills et al. 2010; Carvalho et al. 2011; Lester et al. 2013; Portman et al. 2013), considering the connectivity among them (Almany et al. 2009; Beger et al. 2010; Kininmonth et al. 2011; Olds et al. 2012). Even though many strategies have been proposed for the protection of marine populations (improving of water quality, preventing of overexploitation and spread of exotic species), reserves offer a different type of protection: a spatially explicit form, often permanent, that permits a degree of restriction of human activities (Allison et al. 1998). MPAs represent an efficient way of conserving marine fishing resources, as well as protecting ecosystems from human disturbances (García-Charton et al. 2008). Reserves by themselves cannot guarantee the replenishment of populations of many species. Some authors have argued that there are classes of species for which reserves are of little use, specifically those with planktonic larvae or adults (Kenchington 1990). However, other species with planktonic larvae or large adult ranges may have a stage that is dependent on nursery areas, spawning sites or calving sites. Such species may be protected by reserves if the critical areas can be identified (Allison et al. 1998). In this context, breeding populations of many threatened invertebrates have been detected on artificial substrates in marine environment. They could be effectively protected using different approaches in marine conservation planning. Many artificial coastal structures such as breakwaters, piers and protective armoury (often referred to as ‘riprap’) can provide habitats for many marine littoral species, particularly along areas exposed to the open sea or otherwise exposed to elevated levels of hydrodynamism (Davis et al. 2002). However, this has usually been considered habitat of secondary importance when compared with natural coastlines and as such has received less attention. García- G ó mez et al. (2011) illustrated how such engineering works can benefit conservation efforts indirectly by acting as important smallscale repositories of breeding populations of endangered species, opening up a novel and innovative perspective to the management of these protected species. The importance of coastal harbour works in the protection, monitoring and conservation of endangered species was initially highlighted for one endangered species, Patella ferruginea (Guerra- García et al. 2004a) and subsequently for other protected species (García-Gómez et al. 2011, 2012). This led to the proposal for a new form of environmental protection, the ‘Artificial Marine Micro- Reserve’ (AMMR), defined as an artificial coastal construction which, by mutual agreement between owners and government, is protected due to the environmental value of species or ecosystems that it hosts (García- Gómez et al. 2011). One of the main determinants in the development of the proposal was the massive presence of more than 14,000 specimens of P. ferruginea on artificial substrata of port of Ceuta (4000 specimens inside, 10,000 outside) (Rivera-Ingraham et al. 2011a), almost eight times more than the total number (around 1800) recorded for the entirety of the Southern Iberian Peninsula (Arroyo et al. 2011). García- G ó mez et al. (2011) pointed out that due to its intertidal habit, P. ferruginea is vulnerable not only to negative impacts such as pollutant spills but also to direct collection by humans as well as other anthropic impacts. Given that natural coastlines are usually publicly accessible, this species cannot be as effectively protected as in artificial habitats, which can be literally fenced off and/or kept under strict surveillance. Moreover, it is easier to develop contingency measures and effective protection of endangered species along artificial coastal facilities, among several other significant benefits of AMMRs which are highlighted by these authors. In addition, the management of individuals in artificial areas could be facilitated by AMMRs with strictly protected zones (e.g. for programmes to reintroduce the species in areas where it is extinct locally, where new recruits could be installed on artificial plates). In this regard, some experiments have been successfully carried out in the port of Ceuta (Rivera-Ingraham et al. 2011b). The concept of AMMR exceeds the geographical area of Europe and can be extended to other continents in countries with a coastline where protected species exist (or may need protection in the future), which have a tendency to naturally settle on artificial coastal installations, thus establishing reproductive foci, especially on breakwaters and storm protection jetties. To date there have been no studies focused on the protection of protected species diversity on artificial substrates in order to assess their possible role in conservation. Networks of reserves have been advocated by numerous researchers (Salm & Clark 1989; Ballantine 1991; Dyer & Holland 1991; Bohnsack 1992; Quinn et al. 1993; Castilla & Fern´andez 1996) as a potentially effective solution to large-scale reserve coverage while applying restrictions to only a small fraction of exploited areas. Researchers propose that such networks, properly designed, could provide several replicate source populations, reduce region-wide risk of anomalous effects on a single reserve and increase the potential benefits to nonreserve areas by increasing the connectance between protected and nonprotected areas (Allison et al. 1998). Our proposal for the creation of AMMRs and AMMRNs (Artificial Marine Micro-Reserve Networks) strictly follows the philosophy that to protect species, habitats must be protected (OOPEU 2004). In the present case, P. ferruginea occur naturally and as effective breeding populations on artificial coastal installations that come under different forms of ownership. On a larger scale the creation of AMMRNs should also be supported, as these, properly monitored and managed, would not only aid the conservation of protected species but by safeguarding larger individuals (which contribute disproportionately to fecundity), would facilitate, a priori, gene flow between sub-populations and encourage settlement and colonization of new sites (Alexander & Gladstone 2013). Established networks would aid conservation efforts not only by extending the distribution of these species but also by buffering the effects of any isolated negative impacts to network nodes (such as a localized oil spill at a port) and enhancing the capacity for subsequent recovery. Finally, AMMRNs can play a particularly important role in the conservation of marine invertebrates, and aid in further research on these, especially as invertebrates are the least protected marine organisms, as shown in the IUCN Red List categories and also CITES. In fact, the number of scientific papers on invertebrate families listed by IUCN is extremely low (e.g. 1000 times lower than for sea turtles) compared with those published for bony fishes, elasmobranchs, reptiles and seabirds (McClenachan et al. 2012). AMMRNs could play an active role in the systematic conservation planning process tailored to complex environments (see Giakoumi et al. 2012). Hence, the main objective of the present study is to analyse and discuss the need for the creation of AMMRNs, based on integrative data. Methods The in situ observations of protected species located on jetties and breakwaters reported in Table 1 were made during monitoring programmes conducted in the Strait of Gibraltar and the Mediterranean coast of Andalucía and Gibraltar (Southern Iberian Peninsula), specifically in Ceuta (35°53'25.07″ N, 5°18'45.90″ W, July–August, 1997–1998), Tarifa (36°00'29.05″ N, 5°36'03.64″ W, July 2009) Algeciras (36°08'25.58″ N, 5°25'48.35″ W; July–September 1996), La Línea (36°09'20.70″ N, 5°21'51.17″ W; July–September 1996), Gibraltar (36°07'56.61″ N, 5°21'47.27″ W; June– August 2005), La Mamola (36°44'45.20″ N, 3°16'42.12″ W; December, 2007) and Motril (36°43'04.51″ N, 3°31'23.15 W; October, 2011). We identified four types of artificial substrates: quarried dolomite/limestone boulders, often referred to as ‘riprap’, cubic concrete blocks, concrete tetrapods and vertical concrete walls. Detailed surveys were carried out both along the intertidal and the subtidal (down to 20 m depth) of these four substrate types. We report on the presence or absence of species that are presently under some form of statutory protection (international, national and/or regional). We have avoided in this case any form of quantification given the different characteristics of the various species, with some being strictly sessile in their adult stage (macrophytes, sponges, anthozoans, colonial vermetids, gastropods and bivalve molluscs), partially sessile during low tide (patellids) and vagile (decapod crustaceans, ranellid gastropods and cipreids, echinoid and asteroid echinoderms, and bony fishes). In the case of P. ferruginea, one of the protected species identified as endangered, all breakwaters in the South Bay of Ceuta were surveyed in their entirety between 2006 and 2008. To have a spatial reference for the position of individuals in different areas of the docks, P. ferruginea individuals were counted in 10-m-long transects of coastline, measured parallel to the waterline. Each specimen was measured using a vernier calliper. After calculating the density of individuals within each of the transects, we compared the density of individuals between the sides facing the channel exit (see Fig. 1) and those oriented in the opposite direction, using a nonparametric Kruskal–Wallis test. However, to compare the mean sizes of individuals on both sides, every specimen was considered individually. To establish whether there exists a density decrease at the large biogeographical scale away from the Strait of Gibraltar towards the northeast along the Southern Iberian Peninsula, the breakwaters of the port of Estepona (36°24'44.94″ N, 5°09'24.30″ W, July–August 2009), Marbella-La Bajadilla (36°30'20.28″ N, 4°52'31.00″ W, July–August 2010) and Torremolinos (36°35'38.28″ N, 4°30'39.49″ W; August–September 2011) were surveyed in their entirety. All the breakwaters surveyed were very similar in construction and orientation, which made them readily comparable. Results Protected species observed in different types of potential AMMRs substrates The protected species observed to be associated with artificial coastal breakwaters and harbour facilities along the south of the Iberian Peninsula and Ceuta in North Africa are detailed in Table 1, specifying the common location of each species on each of the four types of substrates sampled: dolomite rock quarry, cubic blocks of concrete, concrete tetrapods and vertical concrete walls. The majority of intertidal and subtidal protected species referred to in the text are illustrated in Figs 2 and 3. Intertidal species and forms of protection 1 Lithophyllum byssoides (Lamarck) Foslie: Berne Convention (Annex II: strictly protected fauna species) and the Barcelona Convention (Annex II marine species endangered or threatened). 2 Patella ferruginea Gmelin, 1791: Berne Convention (Annex II: strictly protected fauna species), the Barcelona Convention (Annex II: endangered marine species or threatened), Habitats Directive (Annex IV: animal and plant species of Community interest need of strict protection), Spanish Catalogue of Threatened Species (category ‘endangered’), Andalusian Endangered Species Catalogue (category ‘endangered’), Data Book of the Invertebrates of Andalusia (category ‘critically endangered’) and Government of Gibraltar Nature Protection Ordinance 1991, (category ‘strictly protected’). 3 Cymbula nigra (Da Costa, 1771): Berne Convention (Annex II: strictly protected fauna species), the Barcelona Convention (Annex II: endangered marine species or threatened species) and Data Book of the Invertebrates of Andalusia (category ‘vulnerable ‘). 4 Dendropoma petraeum (Monterosato, 1884): Berne Convention (Annex II: strictly protected fauna species), the Barcelona Convention (Annex II: endangered marine species or threatened), Spanish Catalogue of Threatened Species (category ‘vulnerable’), Andalusian Catalogue of Endangered Species (category ‘vulnerable’) and Red Data Book of the Invertebrates of Andalusia (category ‘vulnerable’). Sublittoral species and forms of protection 1 Tethya aurantium (Pallas, 1766): Berne Convention (Annex II: strictly protected fauna species), the Barcelona Convention (Annex II: endangered marine species or threatened as Tethya sp. Plur.) and Red Data Book of the Invertebrates of Andalusia (category ‘vulnerable’). Astroides calycularis (Pallas, 1766): Berne Convention (Annex II: strictly protected fauna species), the Barcelona Convention (Annex II marine species endangered or threatened), CITES (Appendix II species are not necessarily endangered, but in which trade must be controlled to avoid utilization incompatible with their survival), Spanish Catalogue of Threatened Species (category ‘vulnerable’), Andalusian Endangered Species Catalogue (category ‘vulnerable’), Red Data Book of the Invertebrates of Andalusia (category ‘vulnerable’) and Government of Gibraltar Nature Protection Ordinance 1991, (category ‘strictly protected’). 2 Lithophaga lithophaga (Linnaeus, 1758): Berne Convention (Annex II: strictly protected fauna species), the Barcelona Convention (Annex II: endangered marine species or threatened), Habitats Directive (Annex V: animal and plant species of interest whose taking in the wild and exploitation may be subject to management measures), CITES (Appendix II species not necessarily threatened with extinction, but in which trade must be controlled to avoid utilization incompatible with their survival), Red Data Book of the Invertebrates of Andalusia (category ‘vulnerable’) and Government of Gibraltar Nature Protection Ordinance 1991 (category ‘strictly protected’). 3 Pinna nobilis Linnaeus, 1758: Berne Convention (Annex II: strictly protected fauna species), the Barcelona Convention (Annex II: endangered marine species or threatened), Habitats Directive (Annex V: animal and plant species of Community interest whose taking in the wild and exploitation may be subject to management measures), Spanish Catalogue of Threatened Species (category ‘vulnerable’), Andalusian Endangered Species Catalogue (category ‘vulnerable’), Red Data Book of Invertebrates of Andalusia (category ‘ vulnerable ‘) and Government of Gibraltar Nature Protection Ordinance 1991 (category ‘strictly protected’). 4 Pinna rudis Linnaeus, 1758: Berne Convention (Annex II: strictly protected fauna species), the Barcelona Convention (Annex II: endangered marine species or threatened species), Red Data Book of the Invertebrates of Andalusia (category ‘vulnerable’) and Government of Gibraltar Nature Protection Ordinance 1991 (category ‘strictly protected’). 5 Charonia lampas (Linnaeus, 1758): Berne Convention (Annex II: strictly protected fauna species), the Barcelona Convention (Annex II: endangered marine species or threatened), Spanish Catalogue of Threatened Species (category ‘vulnerable’), Andalusian Endangered Species Catalogue (category ‘vulnerable’), Red Data Book of the Invertebrates of Andalusia (category ‘vulnerable’) and Government of Gibraltar Nature Protection Ordinance 1991 (category ‘strictly protected’). 6 Luria lurida (Linnaeus, 1758): Berne Convention (Annex II: strictly protected fauna species), the Barcelona Convention (Annex II: endangered marine species or threatened species), Red Data Book of the Invertebrates of Andalusia (category ‘vulnerable’) and Government of Gibraltar Nature Protection Ordinance 1991 (category ‘strictly protected’). 7 Centrostephanus longispinus (Philippi, 1845): Berne Convention (Annex II: strictly protected fauna species), the Barcelona Convention (Annex II: endangered marine species or threatened), Spanish Catalogue of Threatened Species (category ‘special interest’), Andalusian Endangered Species Catalogue (category ‘special interest’), Habitats Directive (Annex V: animal and plant species of interest whose taking in the wild and exploitation may be subject to management measures), Red Data Book of the Invertebrates of Andalusia (category ‘vulnerable’) and Government of Gibraltar Nature Protection Ordinance 1991 (category ‘strictly protected’). 8 Ophidiaster ophidianus (Lamarck, 1816): Berne Convention (Annex II: strictly protected fauna species), the Barcelona Convention (Annex II: endangered marine species or threatened species) and Data Book of the Invertebrates of Andalusia (category ‘vulnerable’.) 9 Hippocampus brevirostris Schinz, 1822: CITES (Appendix II species not necessarily threatened with extinction, but in which trade must be controlled to avoid utilization incompatible with their survival) and Government of Gibraltar Nature Protection Ordinance 1991 (category ‘strictly protected’). The bivalves P. nobilis and P. rudis were not located directly on the specific substrates under study but were found within soft sediments between the compositional units of the breakwaters or in very close proximity to these (Fa & Finlayson 2008). It is surmised that these specimens derive direct protection from the presence of the breakwaters, due to reduced access but also from the destructive effects of bottom trawlers, a result also observed around wrecks and harbour breakwaters around Gibraltar. These structures also modify water currents which may also contribute to the survival of these species. In fact, P. nobilis has almost completely disappeared from the area studied, except for some isolated specimens detected outside some of the port levees of Gibraltar. Other species whose exploitation is regulated Spongia agaricina (Pallas, 1766), Homarus gammarus (Linnaeus, 1758), Palinurus elephas (Fabricius, 1787), Scyllarus arctus (Linnaeus, 1758), Maja squinado (Herbst, 1788), Paracentrotus lividus (Lamarck, 1816), Epinephelus marginatus (Lowe, 1834), Sciaena umbra Linnaeus, 1758: Barcelona Convention (Annex III), Berne Convention (Appendix III) and/or IUCN Red List. Maja squinado is also strictly protected under the Government of Gibraltar Nature Protection Ordinance 1991. The ‘reserve effect’ in AMMRs The Port of Ceuta is exceptional from an environmental point of view because of its two antagonistically located inputs, creating a high-energy hydrodynamic pump which flushes the entire harbour every 6-h tidal cycle (Fig. 1). Due to this unique circumstance, some 4000 specimens of the endangered marine limpet P. ferruginea are established within the Port (Rivera-Ingraham et al. 2011a). We infer that during the reproductive phase, synchronously released gametes from both sexes are trapped for a while within the port, thereby increasing the probability of external fertilization above that expected in the open sea. Moreover, the larvae can only exit via the northern harbour mouth or via the mediaeval moat to the south, locally known as the ‘Foso’, depending on the state of the tide. An extensive survey and census of the protected species P. ferruginea was carried out by Rivera- Ingraham et al. (2011a) within the southern bay of the Port of Ceuta. We have re-analysed the data presented to test the hypothesis that the ‘reserve effect’ is acting within this harbour, which would therefore be operating as an AMMR. The present study confirms that the breakwaters within this area are heavily colonized by numerous individuals of P. ferruginea, highlighting for the first time significant differences in the spatial distribution of densities. When data are grouped into 10-m- long transects along the breakwaters, the highest densities are obtained along the sides closest to and facing the moat (6.62 5.25 ind.·m—1), with the outward-facing sides presenting significantly lower densities (3.99 4.33 ind. m—1) (K = 3.71, P < 0.05). This observation is best explained via a model of higher viability of successful settlement due to the hydrodynamics of the larval-carrying outflow from the moat. The results are presented graphically in Fig. 1. This significant density differential is evident even on breakwaters very close to the outflow such as the breakwater immediately to the west of the moat, which is essentially a continuation of its western side. We suggest that this is probably due to the great difficulty of forcing the outgoing hydrodynamic tidal current output to loop back on itself, and supports our view that these sub-populations of the South Bay are fed by recruits from reproductive events occurring inside the port. This clearly illustrates the positive effects that AMMRs can have due to their ability to export larvae and encourage recruitment in surrounding areas. However, molecular or equivalent work is necessary to fully assess the possibility that there is genetic flow with populations elsewhere outside the harbour. Similarly, the observation that the average size of individuals located along the sides of breakwaters facing the moat exit is significantly larger than that of individuals on sides facing in the opposite direction (3.76 1.55 cm versus 3.04 1.50 cm, respectively, K = 261.95, P < 0.001). This finding is of particular interest if we consider that individuals along both sides of any breakwater are exposed to the same probability of collection by humans. This effect further supports the hypothesis that the sides of breakwaters facing the moat channel benefit from not only a higher larval recruitment but also from increased nutrient levels stemming from the interior of the Port, which result in increased algal microfilm biomass and turnover, reflected in turn by an increased growth rate in the limpets. To confirm that the Strait of Gibraltar houses a significant population of P. ferruginea (mainly in Ceuta and, to a lesser extent, in Gibraltar and the surrounding coastline) we censused numbers of this species along port structures (Estepona, Marbella and Benalmadena) along the Southern Mediterranean coastline. The results obtained indicate a decreasing number of individuals with increasing distance away from the area of the Strait, regardless of the fact that the general structure and orientation of all the port areas studied were remarkably similar. These results are shown in Table 2 and Fig. 4. Applied Ecological/Conservation Aspects and Environmental Implications of AMMRs and AMMRNs: A Discussion Protected species and the reserve effect in AMMRs and AMMRNs: principal supporting arguments for their validation as a new form of protection. Espinosa et al. (2009) found that along artificial breakwaters protected by strict security restrictions, such as the rock armoury of the Airport of Gibraltar or the restricted area surrounding the Civil Guard Station in the Port of Ceuta, P. ferruginea, the most emblematic species of potential AMMRs in European waters, tends to grow to its maximum size (about 9–10 cm) corresponding mostly to females. This limpet is a proterandrous hermaphrodite: when juvenile individuals reach sexual maturity they are all male and over time and with increasing size, become females. A welldistributed range of size classes with correspondingly large individuals favours a more balanced sex ratio in the population (very easily affected by direct extraction of the larger specimens) and increased reproductive output. Figure 5 graphically illustrates how the observed distribution of sizes within the Port of Ceuta varies depending on whether the area is (i) not guarded (the curve tends to be slightly skewed to the left, with the 2–3-cm size category being the most common), (ii) guarded but inconsistently monitored (again, the 2–3-cm category has the highest frequency, but there is a slight extension of the tail to the right, indicating some larger specimens, and (iii) under strict surveillance (here the curve tends to be heavily right-skewed, most the 7–8-cm size category being the most frequent). The latter clearly reflects a positive ‘reserve effect’ within a strictly monitored area. Reserves can increase the density and average size of individuals (Polunin & Roberts 1993; Roberts 1995). Because larger, older individuals are typically much more important to reproduction in a population than young, small individuals, this change in the population structure can drastically increase the reproductive output of the population protected in reserves (Bohnsack 1992). In fact, Espinosa et al. (2006) reported results which showed that a single female of 8 cm length would release a similar amount of oocytes as 10 females of 6 cm size. This 10- fold increase in reproductive potential with only a 2-cm increase in length means that to avoid the decline of certain endangered species, it is important not only to keep wild populations in a balanced sex ratio but also to maintain high numbers of large females. This is one of the most obvious benefits that future AMMRs could provide. The establishment of the ‘reserve effect’, with balanced sex ratios and large reproductive specimens, could over time lead to long-term viability of these populations, provided that official bodies already implementing security restrictions along certain coastal installations support the initiative, at no additional costs to the relevant authorities. The efficiency of reproduction within the port can be deduced from the lowered dispersal probability of gametes when compared with open and exposed coastlines. It is known that sperm in such marine species disperses quickly, making fertilization unlikely some distance from the male who released it (Handel 1976; Wilson 1983; Pennington 1985; Denny & Shibata 1989; Okubo & Levin 1989; Grosberg 1991; Levitan 1991; Babcock et al. 1994). This is a limitation that can severely affect reproductive success in marine invertebrates with external fertilization (Levitan & Petersen 1995). This problem, for the reasons outlined above (reduced water movement and wave action, but not stagnant), should be quite diminished in a port such as that of Ceuta and indicates ways in which coastal developments might incorporate design features that maximize fertilization and recruitment. Many coastal infrastructures are important habitats for protected species, many of which reach very high densities in these sites (García-Gómez et al. 2012). The importance of such structures as potential reserves has already been suggested by Guerra-García et al. (2004b). In this sense, the surveillance of some of these artificial enclaves for security or other similar reasons has reduced the mortality associated with public access such as harvesting for different purposes or trampling, ensuring that many specimens reach the maximum size, thereby exponentially increasing reproductive capacity (Espinosa et al. 2006, 2009). Consequently, these enclaves, which have been under strict surveillance, have become conservation hotspots that export larvae to adjacent areas. The importance of individuals reaching larger sizes is paramount for the future viability of populations, so that eliminating sizebased collection of larger individuals is vital to prevent local extinctions. In this regard, population viability analyses (PVA) can be very useful. Rivera-Ingraham et al. (2011c) carried out PVAs for different types of size-based mortality (Fig. 6). A population in which only specimens larger than 5 cm were protected from non-natural mortality (by harvesting or other factors) had a low probability of extinction (Fig. 6A) with a long-term outlook very similar to a population in which all limpets were protected from non-natural sources of mortality (Fig. 6B); populations where non-natural mortality occurs to largesized individuals led to very rapid population collapse (Fig. 6C). The preliminary census of P. ferruginea in Mediterranean ports near the population hot-spot of the Strait of Gibraltar (the Ceuta Harbour population has been estimated at over 14,000 specimens, Rivera-Ingraham et al. 2011b), indicates a progressive reduction of limpet numbers, despite the favourable dispersing influence of the current loop of the Alboran Sea. In this sense, our observations (see Table 2, Fig. 4) are in agreement with the surface dispersion model formulated by Peri ´ a n ~ ez (2007) for the Alboran Sea, which predicts the current path (from west to east) in the Southern Iberian Peninsula (eastern coast of Andalusia), from the Northern Straits of Gibraltar to the Alboran Sea. It shows the position of particles 2.5, 12.5 and 27.5 days after instantaneous liberation from the central part of the Gibraltar Strait (10 m s—1 wind blowing from the East is included) and supports the necessary connectivity which must be ensured between the constituent units of a network of AMMRs in Southern Iberian coasts. We therefore conclude that P. ferruginea probably has a low dispersal capacity, which reinforces the need to create networks of AMMRs, each with no more than 30 km distance between its constituent units (ideally even less), and provided that there are no reproductive populations in intermediate natural areas. These multiple population foci can generate genetic bridges, provide stability and encourage growth for the re-establishment of a continuously distributed breeding population. This is consistent with the proposal of Shanks et al. (2003) and Boudouresque et al. (2005), who considered such a scheme of a small network of marine reserves separated by a few tens of km as a particularly suitable model, from a conservation point of view, for the Mediterranean. In the context of MPAs, connectivity must be guaranteed to achieve conservation objectives, for which the size and distance between MPAs is one of the main factors. In this context, there is a reasonable scientific consensus that networks of a high number of small reserves will be more effective than a smaller number of large ones in the marine environment (see Shanks et al. 2003). With regard to distance, some authors (Boudouresque 1996; Shanks et al. 2003) estimated that reserves spaced c. 20 km apart should support long-range dispersing species, by encountering reserves frequently enough to ensure sustainability of populations and stocks. The AMMRNs fit the abovementioned requirements. 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Species Dolomitic quarried rock Cubic concrete block Concrete tetrapod Vertical concrete wall Presence/absence data for each of the protected intertidal species for each substrate type Lithophyllum byssoidesa + + — + Patella ferrugineaa + + + + Cymbula nigraa + + + + Dendropoma petraeuma + + — + Presence/absence data for each of the protected subtidal species for each substrate type Tethya aurantium + — — — Astroides calycularisa + + — + Lithophaga lithophagaa Pinna nobilisb Pinna rudisb + + + — + + — + + — Charonia lampas + + — + Lurida lurida + — — — Centrostephanus longispinus + + — + Ophidiaster ophidianus + + — — Hippocampus brevirostris + — — — Presence/absence data for each of the species whose exploitation is regulated for each substrate type Spongia agaricina + + — — Homarus gammarus + + — — Palinurus elephas + — — — Scyllarus arctus + — — + Maja squinado + + — — Paracentrotus lividusa + + + + Epinephelus marginatus + + — — Sciaena umbra + — — — aStrictly sessile or sedentary species (when adult) frequently found on potential AMMRs with high numbers of reproductive individuals. bPinna nobilis and Pinna rudis individuals have been found within sediments both between and immediately surrounding artificial reefs and breakwaters. There is evidence that the protection afforded to these and similar soft-bottom species by their close proximity to breakwaters from activities such as sea bed conch raking allows the long-term survival of larger individuals that can contribute disproportionately to the species’ survival prospects, and moreover extends the conservation value of AMMRs to associated substrates (see text). Table 2. Reduction in numbers of Patella ferruginea individuals along the Southern Mediterranean coastline of Andalucía with increasing distance away from the Strait of Gibraltar (nearest location containing high densities of specimens with a significant proportion of large, actively reproducing individuals). Size (cm) Distance from the Strait of Gibraltar (km) No. of individuals Mean SD Estepona Port 38 62 3.35 0.88 Marbella Port 56 27 3.6 0.77 Benalm´adena Port 86 4 4.37 1.22 FIGURES FIGURE 1 A B C D FIGURE 2 FIGURE 3 FIGURE 4