Marine artificial micro-reserves: a possibility for the conservation of endangered species living on artificial substrata

Introduction

As is the case in terrestrial systems, the protection of marine endangered species is generally associated with the protection of natural areas such as parks, reserves or marine protected areas. However, little attention is paid to the fact that some endangered marine species may colonize artificial substrata, like breakwaters, docks and harbours, which lack a protection status that could help to manage the biodiversity that these structures could host.

The ecology of urban and commercial infrastructures in the sea has usually been considered a part of the general ecology of the coast in which the structures have been introduced. One notable exception is work on the ecology of oil platforms in southern California. It is not the case on land, where native landscapes have been studied for many years. In a very recent review, Bulleri & Chapman (2010) point out the differences between the artificial substrata and the neighbouring natural environment, considering the problems that these structures may cause, and stressing the fact that they are not simply surrogates of the natural rocky substrata. According to these authors, the artificial constructions may have several impacts, especially when they are installed in previously soft bottoms, and they do not usually provide optimal substrata. They can enhance the settlement of exotic species or provide previously non-existent connections between populations that could diminish genetic diversity (Bulleri & Chapman 2010). However, this work does not mention the possibility that the artificial constructions may be a refuge for endangered species that have become very rare in natural areas because of human impact from which they are more protected in artificial substrata.

In such cases, some kind of protection could help the preservation of the species, providing refuge for populations that can be a source for the re-colonization of nearby natural habitats. These places, however, given their artificial nature and usually small size, do not fit the features of natural reserves. They differ from artificial reefs, which do not have any industrial or economic use apart from the enhancement of the diversity for which they are conceived.

Intertidal or upper sublittoral species encounter other problems such as human disturbance or collection by people for food, fish bait or souvenirs. In these cases, the laws of some countries, such as Spain, are scarcely helpful because the coastline is considered a public domain and cannot be closed to people. The laws, jurisdiction and political stance on the use of such structures will vary greatly from country to country, and state to state. The legal protection of a species has little effect when a long coast is visited by numerous inhabitants and tourists, which renders effective enforcement problematic.

By contrast, artificial coastal constructions like breakwaters, docks and harbours may be effectively closed by the owners, regardless of whether they are public or private. The species that settle on such structures are free from disturbance because of vigilance and also because these areas are not usually attractive to the general public (Guerra-García et al. 2004a). In these cases the problem may be pollution, but the exterior areas of the harbours, especially the breakwaters, which are exposed to energetic flows, may have sufficient conditions for the development of marine organisms, and can be especially attractive for sessile or sedentary species (Pister 2009). The key word for these cases is custody. In such areas there is no legal restriction on effective enforcement, which, in addition, has a low cost because it is only an extension of the usual security measures that must be maintained in these installations. Furthermore, Pister (2009) indicated that an interesting conservation application of riprap structures might be as marine reserves or other management tools. Unlike many terrestrial habitats, humans can be excluded from riprap without compromising its intended anthropogenic purpose, that is, absorbing wave energy.

The possibility of declaring some kind of environmental protection for these artificial areas would be a very helpful tool for this purpose. Usually, protected areas do not include man-made structures and, subsequently, their legal arrangements can not be enforced. Here we propose a protection concept termed Artificial Marine Micro-Reserves (AMMRs) for artificial sites where endangered species find their main refuge against human disturbance.

The concept of the micro-reserve has been developed in Eastern Spain for rare endemic plants with small distribution zones, for which the usual conservation areas such as parks or reserves are unsuitable (Laguna 2001; Laguna et al. 2004). The Regional Government of the Community of Valencia has given these areas a protection status unique in the world, and has created a network of micro-reserves for rare or relict plant species. The main difference between micro-reserves and other protected areas is their small size, always <20 ha (0.2 km²). Because of this, the planning and management, as well as previous studies for their declaration, are easier than for larger protected areas (Laguna 2001). Micro-reserves are very useful for the conservation of reduced populations of non-mobile organisms such as plants, and should be for coastal sessile animals, which are very similar to land plants in terms of dispersion and substrate occupation.

The plant micro-reserves of the Community of Valencia are located in natural areas, (some of them moderately human-disturbed) but not in artificial places. However, many developed countries, and especially those with high touristic development, like Spain, have many artificial constructions on their coasts that are suitable for the settlement of sessile or scarcely mobile marine animals. Each of these places is usually small in area, but in combination provides a large area of substrate that can be occupied by littoral or upper sublittoral species that can thrive there. A network of AMMRs is the most useful tool for the protection of these populations in order to assure a viable metapopulation.

It is evident that an AMMR must be compatible with the normal use of the installation, but many parts of a harbour or a breakwater (and especially the outer sides) are almost or completely free from commercial or industrial activity.

Environmental protection could help installation owners and managers apply for funds from the environmental authorities and could have a social benefit in terms of owner image and education of the public. The experience with land plant micro-reserves in Valencia was that after their declaration in public areas, some private owners were interested in having micro-reserves on their own properties, as they were provided with economic facilities and compensation. This type of program could be considered a way of involving the private sector in the conservation of nature (Laguna 2001), within the framework of an ‘ecosystem approach’ to conservation (Groom et al. 2006).

The Concept of Artificial Marine Micro-Reserve (AMMR)

An AMMR could be defined as an artificial coastal construction which, by agreements between owners and public administrations, is protected because of the environmental value of the species or ecosystems that it houses.

The creation of the conservation concept of AMMR would be very helpful in offering legal status to this kind of artificial area that is valuable from an environmental point of view. The legal rank would be similar to that of natural protected areas, depending on the level of protection in the local environmental legislation. In addition, the declaration of an AMMR could give better protection to the area by raising the possibility of punishment for offenders. Moreover, an artificial micro-reserve would be easier to guard than natural areas because any emergency plan against catastrophic events such as oil spills could be quickly carried out. Anti-pollution barriers and boats would be close to the artificial micro-reserves and could be immediately used if an environmental emergency occurred.

The environmental protection of artificial substrata is unusual in coastal areas. However, on land there are ways of protecting endangered species when these inhabit cities or artificial constructions. This could be the case for instance for raptors and other protected birds nesting in buildings or urban trees, or the increasing trend to use local plants instead of exotic ones in parks and green urban spaces. This provides connections between the urban space and the surrounding countryside in terms of biological populations for those species that tolerate the urban environment (Niemela 1999; Savard et al. 2000; Breuste 2004; Florgård 2004; Gordon et al. 2009). Parks and green urban spaces are in fact ‘protected areas’ as there are usually laws that punish anyone who causes damage to the plants and animals living in them. The environmental considerations have become a usual topic of urban planning in developed countries, and there are now specific journals addressing the matter. As is the case with the ferruginous limpet (Patella ferruginea) in breakwaters, artificial urban areas are used by wild species that arrive there by natural dispersal, as in urban parks. Furthermore, conservation efforts must focus on ways to blend a rich natural world with the world of economic activity. This revolutionary common ground between development and conservation is called reconciliation ecology: creating and maintaining species-friendly habitats in the very places where people live, work or play (see Rosenzweig 2003).

Not all artificial substrate with endangered species present will be suitable for being proclaimed an AMMR. The most appropriate sites are those that are exposed to clean marine water and that, for whatever topographical, political, economic or other reasons, are not likely to be rebuilt, modified or demolished in the future, at least for many years. The outer side of San Felipe breakwater and Ceuta Harbour in La Línea and Ceuta, respectively (Strait of Gibraltar, Spain), fit these conditions, as the former is well exposed to currents that flow into the Bay from the open sea, and the latter is exposed to strong wave action in the North Bay of Ceuta. Moreover, the proximity of San Felipe breakwater to the frontier between Spain and the British Colony of Gibraltar, precludes enlargement or new construction in its neighbourhood. The designs of potential micro-reserves should focus on artificial structures that are not already adequately protected by existing restrictions on access.

The purpose in the medium and long term is to create a network of AMMRs in suitable places that help manage and protect the species and ecosystems they house. This concept is especially useful for intertidal or shallow subtidal species. The advantages of effective protection could spread over several endangered or exploited species, such as the molluscs Patella ferruginea, Dendropoma petraeum, Charonia lampas, Lithophaga lithophaga and Cymbula nigra in the Mediterranean, Patella candei in the Atlantic, or Lottia gigantea and Scutellastra mexicana in the Pacific. They may also benefit the orange Mediterranean coral (Astroides calycularis) or calcareous algae (Lythophyllum byssoides). Such networks will assure the gene flow among populations and will contribute to the maintenance of viable metapopulations. Once the first site is established, engaging authorities and populations of other localities to join the network will be easier, as occurred in Valencia with the plant micro-reserves (Laguna 2001).

It is important to note that urban and industrial infrastructures usually have adverse effects in the marine environment because they provide a non-natural habitat that does not house the same community as the surrounding natural one (Bulleri & Chapman 2010). Some studies have found that anthropogenic structures facilitate invasions (Bulleri & Airoldi 2005; Glasby et al. 2007) and the prevalence of invasive species may not be related only to how disturbed an environment is, but also to the extent that novel, human-produced habitats are available (Glasby et al. 2007). However, other studies have not stated any relationship between artificial structures and non-native species (see Pister 2009 for discussion of the open coast southern California riprap structures). As Pister (2009) reported, it is very likely that riprap in protected bays and estuaries harbours larger numbers of non-natives in comparison with wave-exposed ones. Therefore, the AMMRs should be placed in areas with relatively great hydrodynamic energy.

Consequently, it is necessary to avoid two potentially negative side effects of the concept of AMMR. One is to consider that the possibility of creating an AMMR could be argued as a positive reason for allowing a new construction project. This is not the case because, first, the negative impact on the whole environment is greater than the possible benefit to some species (see Bulleri & Chapman 2010), but also because we cannot predict that endangered species will settle on the structures once they are deployed. Hence, it must be clear that the possibility of an AMMR is only a possibility of obtaining some positive side effect of an otherwise generally negative action.

The second temptation that must be avoided is to consider that the species occurring in artificial environments receive sufficient protection in them that the protection in natural environments can be relaxed. This is unlikely as the species that we refer to are endangered because they have lost individuals and populations by human action, so all populations must be protected. In addition, artificial environments are always at risk of accidents, pollution or other dangers. If natural populations decay, an accident (like an oil spill, for instance) could wipe out a great number of the individuals of the species. Artificial installations are easier to protect because of their homogeneity in comparison with natural rocky shores, their orientation which is generally perpendicular to the coast, and the available protective facilities, for example against oil spills. They can serve as a reserve and a source of recruits for the general population of the species in question, but the final objective must be the recuperation of the species in its natural habitat, so AMMRs must be considered only as a supplemental measure that assists with this goal.

Advantages of AMMRs: Environmental and Conservational Implications

There are several added advantages of imposing additional administrative and enforcement structures on artificial substrates that could be applied anywhere. The management and protection would be easier than on natural protected areas. In this sense, the deployment of emergency plans would be faster, as mentioned above (e.g. anti-pollution barriers against oil spills). AMMRs would provide a mechanism for more effective response to natural or man-made disasters. In this respect, we propose here the first AMMRs (see below) in the Gibraltar Strait, a geographical area with a high risk of ecological catastrophe because of its marine traffic. The risks are among the highest in the world, with 80,000–90,000 big ships passing per year, many of them transporting dangerous or noxious substances for the marine environment.

Management plans, such as the use of experimental plates to collect recruits for repopulation purposes in natural rocky shores, would be of great interest. It could replace their use on populations settled on natural substrates. The authors have carried out some recruitment tests in jetties, using experimental plates of different roughness, with encouraging results (Rivera-Ingraham, G.A., Espinosa, F. García-Gómez, J.C., unpublished data).

Effective protection can be guaranteed without additional cost while providing a great advantage. In fact, it is one of the great handicaps in marine protected areas, where surveillance usually has an additional cost and is also insufficient. In this sense, security services linked to harbour areas can help with surveillance of sites that can be declared in the future as AMMRs.

There are many direct ecological benefits as well. Effective protection would increase the mean size of individuals (see Keough et al. 1993; Lasiak 1993 for effects on molluscs) and enhance reproductive effort and viability of populations. Size and reproductive output are tightly linked. For example, one 8-cm individual spawns the same oocytes as ten 6-cm individuals in the highly endangered limpet Patella  ferruginea (Espinosa et al. 2006). The distance among populations could be reduced, influencing the connectivity and genetic structures, in a context of increasing habitat fragmentation. This could be accomplished by altering the distance between suitable habitats and thereby facilitating migration (Pister 2009). Moreover, Boudouresque et al. (2005) pointed out that in the Mediterranean, it has been estimated that a large number of small MPAs spaced 10–20 km apart have a more positive effect than a few very large MPAs. Cowen et al. (2000) reported that models based upon realistic levels of diffusion and larval mortality suggest that the number of individuals may drop to zero at distances of 140 km away from the population of origin. Furthermore, the estimated dispersal ability of some endangered species, such as P. ferruginea, would be at least 100–150 km (authors’ unpublished data). Additionally, the size of AMMRs should be as big as possible, although sometimes it is difficult to protect a whole riprap structure. Many sedentary endangered species can achieve great population stocks in a relatively small areas or short linear distances on ripraps (Espinosa et al. 2009; Pister 2009; Rivera-Ingraham 2010). Taking into account the aforementioned information, the AMMRs could play an important role from a conservation perspective if they are set up as a network of micro-reserves with linear extension 100–500 m each, separated by small distances in the range 10–50 km.

In accordance with the aforementioned data, the improvements in management derived from AMMRs would allow the early detection of any non-native species and their removal from the reserve. It would allow the development of sentinel programs in the context of global change, as a parallel objective of AMMRs.

In addition, there are a lot of recreational activities that are currently banned in harbours and other artificial substrate areas, such as swimming or fishing, and this can prevent humans visiting such areas. Only in visitor-free areas is it possible to find large specimens of several species (Espinosa et al. 2009). Therefore, effective protection and recognised legal status in these artificial substrates could avoid the plundering of target species.

The Case of Patella ferruginea Gmelin, 1791 (Ferruginous Limpet)

Patella ferruginea is a large (up to 10 cm long) intertidal limpet endemic to the Western Mediterranean (Fig. 1). It is the only marine invertebrate species considered to be at risk of extinction in Europe and is either mentioned or protected by different laws and conventions: the Spanish National Catalogue of Endangered Species, Annex IV of the Habitat Directive, Annex II of the Barcelona Convention and Annex II of the Berne Convention. Recently, the Sectorial Conference on Environment of the Spanish Ministry of Environment and Rural and Marine Domains published the National Strategy for the Conservation of P. ferruginea (MMAMRM 2008).

Patella ferruginea is restricted to the middle intertidal, and thus is very accessible to people from land. Its large size and conspicuous shell (with marked ribs and ridges) make it very attractive for collection (as food, bait or simply for ornamental purposes). Evidence of shell collection has been found in archaeological sites associated with the Homo neandertalensis, and currently, the species is seriously endangered, especially by harvesting, collection and habitat loss (Espinosa et al. 2009).

The current locations of the species include sites in Northern Africa (e.g. the Spanish sites of Ceuta, Melilla and Chafarinas Islands; Natural Park of Alhucemas, Morocco; Habibas Islands, Argelia; Cape Bon and Zembra Island, Tunisia) as well as sites in Europe (e.g. Southern Iberian Mediterranean coast, Corsica and Sardinia). On the Iberian coast it is considered to be at serious risk of extinction, with fewer than 1000 individuals counted in the last 5 years; most of them are recorded from the Bay of Algeciras (Espinosa et al. 2005; Moreno & Arroyo 2008) and Alboran Island (Moreno & Arroyo 2008). The African Spanish sites (Ceuta, Melilla and Chafarinas Islands) have nearly 100,000 individuals, but they are concentrated in a few places, where they are vulnerable to disasters like oil spills, which are unfortunately very possible in an area like the Strait of Gibraltar with intense maritime traffic.

It is not only the accessibility of P. ferruginea’s habitat that has made the species extremely vulnerable. The reproductive biology of the species also plays an important role. Patella ferruginea is a protandric hermaphrodite with external fertilisation. Females are usually larger than 40 mm, quickly increasing their size over 60 mm (Espinosa et al. 2006, 2008a). As a consequence of this reproductive feature, females (more conspicuous because of their larger size) are more likely to be collected. In addition, because fecundity increases with body size, the removal of larger specimens decreases population fertility. This is very damaging for a broadcast spawner whose reproductive success is highly dependent on the gamete concentration (Espinosa et al. 2006, 2009).

Current work on the populations of P. ferruginea of the Strait of Gibraltar (Guerra-García et al. 2004b; Espinosa et al. 2005, 2009) has not detected major sources of mortality from diseases or other effects of overpopulation, even in the densest populations. Thus the natural situation of the species, previous to human impact, was that of a common intertidal species whose populations were probably connected by free spawning. Bulleri & Chapman (2010) point out that artificial substrata could favour an unnatural connection of populations, thus giving rise to a loss of genetic diversity. On the other hand, increasing connectivity could counter the downward pressure on genetic diversity caused by habitat fragmentation. In the case of P. ferruginea, however, the main problem seems to be the currently unnatural isolation of the existing populations, most of them less dense and sparser than would be expected without human pressure. Hence, the advantages of preserving the populations, even those on artificial substrata, will be greater than the possible disadvantages. It must be also stressed that we do not propose the installation of new populations, but the protection of existing ones, or those which could appear in the future, established by the species itself.

Towards a Network of Micro-Reserves of Patella ferruginea in Artificial Substrata

Recent studies in Ceuta and the Iberian coasts (mainly in Algeciras Bay) have shown that some of the most dense populations of Patella ferruginea occur in harbour breakwaters (Fig. 2) (Guerra-García et al. 2004a,b; Espinosa et al. 2005, 2006, 2009). Pister (2009) also reported a similar pattern in the endangered limpet Lottia gigantea in southern California. Espinosa et al. (2009) found that, out of eight populations in which size frequencies were measured, those populations located on breakwaters under custody (for being military areas or private properties) present the largest sizes, even larger than inaccessible natural areas. All these populations are in areas with enough replacement and satisfactory quality of water. In fact, this species is a good bio-indicator of non-polluted waters (Espinosa et al. 2007). Translocation of individuals from exposed to protected areas is not an alternative. Espinosa et al. (2008b) demonstrated that the survival of the transplanted specimens was very low, mainly due to the fact that each individual needs its own home scar in the substrate to avoid desiccation when emerged and to keep firmly attached during strong wave episodes. Transplanted limpets cannot produce home scars sufficiently rapidly to avoid mortality from desiccation or wave removal. In this sense, future research must be undertaken to find good transplantation techniques.

It is likely that the populations protected by private restriction of public access in areas of artificial hard substrata in Gibraltar, contribute most to reproduction in Algeciras Bay (Espinosa et al. 2009), because of the larger size (and hence higher fertility) of their individuals. Consequently, effective custody of the population becomes the best conservation measure.

The outer side of Gibraltar Airport (an artificial substratum) is one of the sites with larger individuals and higher density on the European coasts (Espinosa et al. 2005, 2009). It is very effectively protected by the authorities because of its military status. On the other hand, the population settled on San Felipe breakwater (La Linea Harbour, Fig. 2D) is one of the most abundant in that area (Espinosa et al. 2005). However, a recent study revealed that, of 45 individuals recorded from the beginning to the middle of the breakwater, only one reaches 60 mm long; all the others were smaller. Probably, larger individuals are subject to higher rates of exploitation because access is not as restricted as on the outer side of Gibraltar Airport. With this size distribution, this population is probably very scarcely reproductive.

The eastern side of the Bay of Algeciras has entrance currents that flow from Gibraltar to La Línea (Fa 1998). This pattern of water movement suggests that most individuals of San Felipe are recruits from the reproductive populations of Gibraltar. It has been corroborated by observation that the larger individuals in San Felipe are commonly collected by people. The high number of small individuals found shows that this site is otherwise suitable for the development of an important population, with the condition that there is effective custody against collection.

Given the length of the breakwater, an increase in the density of the population and, even more importantly, the body size of the individuals, the region could become one of the most important populations of P. ferruginea in the Iberian Peninsula.

Ceuta (Fig. 2C), located in the African side of the Strait of Gibraltar, presents a very dense and abundant population (Guerra-García et al. 2004a,b; Espinosa et al. 2009), mainly in the harbour breakwaters, where people do not disturb it. The particular conditions of the Harbour of Ceuta, with a channel that allows some inside water circulation, make it a very interesting site for studying what may be done to combine industrial development with species conservation. One of the most abundant known populations of P. ferruginea occurs in this harbour (Guerra-García et al. 2004a,b; Espinosa et al. 2009).

As in the Bay of Algeciras, the largest individuals in Ceuta are found in areas with restricted access, such as the areas belonging to the Spanish Guardia Civil military base and the locally known ‘Parque Mediterraneo’, which is private property (Espinosa et al. 2009). The breakwater of the harbour supports a dense population in both the outer and inner sides, but because access to people is not restricted, individuals do not reach the sizes of those in the areas under private or governmental control. Given the length of the breakwater, restricted access would allow an abundant population with large individuals, with the above-mentioned benefits.

Ceuta Harbour (Northern Africa; 0.5 km ×2, comprising both the outer and inner sides; coordinates outer side: 35º53′46.55′′ N/5º18′48.48′′ W; coordinates inner side: 35º53′26.70′′ N/5º18′51.74′′ W).) and San Felipe breakwater (La Línea Harbour, Algeciras Bay, Southern Europe; 2.3 km; coordinates: 36º09′18.33′′ N/5º21′42.70′′ W), are less than 20 km apart. We proposed them as the first two AMMRs of several that could set up a future net of AMMRs in the Strait of Gibraltar (a geographical triangle of coastal cities Ceuta-La Línea-Tarifa) integrated for at least five units of AMMRs. Effective custody could be accomplished to avoid human access to the limpets by means of an enclosure and, eventually, surveillance cameras. This enclosure could even be convenient because the intertidal level may be dangerous, but it would not be necessary to prohibit people walking on the pedestrian upper area of the breakwater, which could be an interesting visitor attraction. Limpets may be seen from the walkway, and explanatory posters will be installed, making the breakwater a vehicle of environmental education and public awareness of the richness of the local environment. The general purpose is to make progress from the current simple prohibition of collection towards more active protection measures.

The Conservation Strategy of the Ferruginous Limpet (MMAMRM 2008) establishes that, because limpets are often present in artificial substrata, the owners of these substrata must contribute to its conservation. Although both private and public installations are mentioned, it is obviously easier to enforce protection measures on public areas rather than on private ones. Most of the artificial substrata in the Spanish coast of the Bay of Algeciras and Ceuta are on public property managed by their respective harbour authorities, that of the Bay of Algeciras (Spanish acronym APBA) and that of Ceuta (Spanish acronym APC). Both harbour authorities are part of the Spanish State Harbours Trust (Puertos del Estado), dependent on the Spanish Government. Thus, the government can play a key role in the protection of P. ferruginea.