Management of Marine Protected Areas: A Network Perspective

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From Marine Protected Areas to MPA Networks

Ferdinando Boero

Università del Salento – CNR‐ISMAR, Italy

The Ecology of Beauty

Just like terrestrial National Parks, Marine Protected Areas (MPAs) were first established at places where biodiversity had some prominent features. In the Mediterranean Sea, for instance, the first MPAs were established at places that were perceived as ‘beautiful’ by scuba divers who started to explore marine landscapes and singled out the most scenic ones (see Abdulla et al., 2008 for a review on Mediterranean MPAs). The European Landscape Convention (ELC) (Council of Europe, 2000) is in line with this approach to site selection. The ELC, in fact, states that ‘The sensory (visual, auditory, olfactory, tactile, taste) and emotional perception which a population has of its environment and recognition of the latter’s diversity and special historical and cultural features are essential for the respect and safeguarding of the identity of the population itself and for individual enrichment and that of society as a whole’.

What is perceived as valuable in a given environment, then, is part of the heritage of the resident population and contributes to its culture. The positive impressions described in the ELC simply identify beauty, defined as follows in a popular dictionary: ‘a combination of qualities, such as shape, colour, or form, that pleases the aesthetic senses, especially the sight’.

The perception of beauty, however, is directly linked to cultural paradigms and can change with them. Cetaceans, for instance, were once perceived as evil ‘monsters’ that brave sailors had to exterminate, as Melville’s story of Moby Dick tells us. Nowadays, they are worshipped as gods. Even white sharks (Carcharodon carcharias), again depicted as terrifying beasts in movies like Spielberg’s Jaws, are now considered as highly valuable, deserving strict protection.

Following this aesthetic approach, large vertebrates or, in alternative, beautiful and scenic habitats (i.e. the charismatic expressions of nature) are usually identified as deserving protection, whereas important ecological actors are simply ignored. Everybody wants to save the whales, but nobody wants to save the bacteria, even if bacteria are indispensable for ecosystem functioning (and also for our own body functions), whereas whales are not. On the one hand, our impact on bacteria is not so huge: they become rapidly resistant to antibiotics and are not affected much by our influence, being able to evolve rapidly so as to cope with environmental changes. On the other hand we could easily exterminate cetaceans, if only we intended to do it.

The preservation of beautiful portions of the environment, and of the fauna and flora inhabiting them, has been instrumental in the understanding of the value of nature. This approach to the defence of nature is shared by almost all environmentalist movements who evoke charismatic portions of nature in their logos, full of dolphins and panda bears. The growth of human population, with the adoption of economic paradigms aimed at the continuous growth of the economic capital, as if resources were infinite, has led to an alarming erosion of the planet’s natural capital. Habitat destruction, both on land and in the seas, and climate change show that we need more than beauty to preserve nature. Protected areas, in this framework, have been some sort of surrogate that justified the destruction of nature where protection was not directly enforced. Focusing on the unique and beautiful facets of nature, often perceived as the sole expression of ‘biodiversity’, led to protection of natural structures, while disregarding natural functions that are not restricted to charismatic species and habitats.

Beauty is important, but the conservation of nature requires more than aesthetics.

From Landscapes to Habitats

The European Landscape Convention is centred on the way the culture of a population perceives and modifies nature, somehow ‘improving’ it with wise management. This is particularly evident in countries like Italy, where millennia of agriculture and architecture have led to unique landscapes that are considered of paramount importance in Article 9 of the Italian Constitution. In this sense, the landscape is the result of human interventions that led to changing a ‘wild’ expression of nature into a ‘gentler’ one. Usually the products of these interventions are aesthetically valid, and the result is beauty. However, a beautiful landscape might be limited in the expression of biodiversity (especially if agriculture is involved), calling for the need of preserving nature per se, and not its modifications, whatever their aesthetic value. It can happen, furthermore, that a local ‘culture’ adopts some behaviours that are against the integrity of nature, as happened in Region Apulia with date mussel (Lithophaga lithophaga) consumption. The harvesting of date mussels from rocks caused extensive denudation of Apulian rocky bottoms (Fanelli et al., 1994). The destruction of hard bottom habitats came to an end only after a long process of generating public awareness, together with the enforcement of new laws.

To cope with an overly anthropocentric approach to our interactions with the environment, the EU Habitats Directive (92/43/EEC) embraced a completely different perspective: habitats of community importance must be protected, even if this goes against the aspirations of the resident populations!

Sites protected under the Habitats Directive do not necessarily comprise beautiful landscapes, and the low level of ocean literacy in almost every country is often a source of conflict between the expectations of lay people and the preservation of natural capital. The resident communities are puzzled when they are prevented from building a new harbour just because there is a seagrass meadow on the bottom. Local populations often label as ‘algae’ the phanerogam Posidonia oceanica, whose presence can lead to the establishment of a protected site, and consider it as a nuisance. The decomposing leaves that accumulate on the beach repel tourists, who complain about their appearance and smell. The recognition of the ecosystem service of these accumulations of leaves is not part of local cultures, who do not realize that stranded leaves protect the beach from erosion. The stranded leaves are removed, sometimes with bulldozers, and huge quantities of sand are removed with them. Lacking a buffer of amassed leaves, wave action starts to erode the beach. Beaches are a source of income, and the wider they are, the higher the income, since more tourists can be crammed onto them. Beach erosion reduces incomes, and this is redressed by beach replenishment. Without the protection of Posidonia leaves, however, the newly placed sand is also rapidly eroded and often accumulates on the seagrass meadow, smothering it. Posidonia meadows are bioconstructions, since the new rhizomes grow over the old ones, raising the bottom of the sea and making it more stable. The death of the meadow is a catastrophe for the coast, since its role of erosion buffer ceases to protect the shore. Once the protection from erosion is completely gone, due to unwise management of coastal systems, physical defences are built in order to protect the beach, with a radical change of the whole landscape.

It is undeniable that some ‘cultures’ have a vague understanding of the functioning of nature, and the Habitats Directive is an attempt to bring a more objective approach to our relationship with natural systems.

Our land‐based culture, however, still biases the Habitats Directive because although it considers marine habitats that are not necessarily ‘beautiful’, they are invariably benthic. For the Habitats Directive, the marine space is bi‐dimensional, just as the terrestrial one. The third dimension, on land, is occupied just by the size of bodies, and by the temporary presence of flying organisms in the air, so it is right to speak about ‘areas’. In marine systems, however, the water column is a three‐dimensional habitat for a host of organisms that have almost no interactions with the sea bottom. Since oceans cover over 70% of the Earth, the water column is the most widespread habitat of the planet, and it is a volume. Many marine organisms live their whole life suspended in the water, and even benthic ones derive their food from currents, not to mention the spread of propagules. A Habitats Directive which includes the marine biome but does not consider the third dimension of the water column is fundamentally flawed.

Protecting beautiful places, and managing the habitats of European Community importance, is a first step towards recognizing the significance of the marine environment, inviting science to design an approach to its management and protection that goes beyond the biases of the current ‘culture’. Indeed, it calls for actions aimed at developing the ‘ocean literacy’ to alter our scant perception of the values of the oceans that is linked to our terrestrial history.

From Hunting and Gathering to Farming

If we were just like all the other species on the planet, when our populations increase to above the carrying capacity (i.e. the maximum number of individuals of a species an ecosystem can bear), overly eroding the natural capital that sustains us, our numbers should decrease due to a shortage of resources. This would lead to the re‐constitution of the natural capital, according to the popular prey–predator model developed by Lotka and Volterra (Gatto, 2009), in which we are the predators and the rest of nature is the prey. But we are not like the other species. When confronted with a shortage of natural resources, we abandoned hunting and gathering and invented agriculture (Diamond, 2002). We domesticated a restricted set of animal and plant species, and started to culture them so as to satisfy our needs. Agriculture leads to the eradication of all competing species from a piece of land so as to rear just the domesticated one. The terrestrial animals we rear as food are almost invariably herbivores or, in some cases, omnivores, and we cultivate the plants we feed them with. This leads to habitat modification, and what the ELC considers as precious is often just the eradication of natural diversity and its substitution with agricultural systems.

In terrestrial systems there are no natural populations of both animals and plants that can provide massive amounts of resources. In the seas, by contrast, we can still extract resources from natural populations, and fishing is just a form of hunting. In recent decades, however, we have been rapidly passing from harvesting fish, crustaceans, molluscs and so on to aquaculture. What happened on land is now happening in the seas: wild populations cannot feed us all, and our pressure on them is leading several species towards commercial extinction, meaning the benefits from fishing are less than the costs incurred. Increasing the efficiency of fisheries, furthermore, is giving little hope of saving the remaining fish. The transition from fisheries to aquaculture is the final stage in the shift from hunting and gathering to farming. In the sea, contrary to what we do in terrestrial systems, we tend to rear carnivores rather than herbivores.

The Western world, in fact, is fed with farmed carnivorous species, such as sea bream (Dicentrarchus labrax) and salmon (Salmo salar and Oncorhynchus spp.), fed with smaller fish caught from surviving natural populations. This is clearly an unsustainable operation, since it exacerbates the overexploitation of natural populations: after having destroyed the populations of the larger fish, we culture them and we feed them with smaller fish caught from natural populations. Emerging countries cannot afford such costly forms of aquaculture and eat lower quality, but also less impacting, farmed herbivorous species such as tilapia (Tilapia spp.) and pangasius (Pangasianodon hypophthalmus).

The awareness of the impact of industrial fishing did induce some management of natural populations resulting in the protection of target species from overexploitation (Pikitch et al., 2004). This has been done by restricting fishing activities at important places and during important periods. The relevance of these spaces and times depends on the biology of the species under management. Spawning grounds, nursery areas, and feeding grounds are identified species by species, and fisheries are restricted in order to allow for successful recruitment of the managed species. The ban of industrial fishing, per se, is a measure of protection and its positive impact, albeit temporal, is another form of marine conservation even though the aim is just to relieve fish from our excessive pressure, so as to continue to exploit their populations.

The reproductive rates of many fish species are so high that populations can be restored in reasonable time, as the abundance of fish in well‐managed MPAs demonstrates (Guidetti et al., 2008). Since the environmental impact of farming carnivorous species is higher than that of simply fishing, the survival of sustainable natural fisheries is a measure of the health of marine systems, and fisheries science must lead to better results, in conjunction with conservation science.

Landscapes, Habitats and Fish are Not Enough

The introduction of concepts such as ‘ecosystem‐based management’, ‘ecosystem approach’ and ‘integrated coastal zone management’ is the clear expression of a broader view in the way we interact with the rest of nature (Pikitch et al., 2004; Heip et al., 2009). Ecosystems are not just structures, they also function through myriad processes, as their name implies. Knowledge of the connections among the different structures is crucial for managing what we intend to exploit, and to conserve what we want to protect. The link between biodiversity (structure) and ecosystem functioning (function) is the conceptual tool that guides a proper understanding of how the natural world works (Heip et al., 2009). In a strategic document, the European Marine Board identified the adoption of holistic understanding as the greatest challenge for marine scientists worldwide (Arnaud et al., 2013). It is obvious, for instance, that fish do not proliferate as isolated entities from the rest of the environment: they need to be considered as part of ecosystems throughout their life cycle, from the fertilized egg to the adult. This, for instance, should oblige fisheries scientists to consider the impact of predators of fish eggs and larvae, such as gelatinous plankton, in their models of fish population dynamics (Boero, 2013). The match (or mismatch) of a bloom of the by‐the‐wind sailor (the hydrozoan Velella velella) with the spawning of fish species that deliver floating eggs, for instance, can have (or not have) devastating effects on the fisheries yields of the subsequent months (Purcell et al., 2015). However, the cause–effect relationship is usually not perceived since the impact (fewer fish) becomes apparent only when the cause (increased Velella predation and/or competition) is over, the lapse of time depending on the growth rate of the fish species concerned. If larval mortality is treated as a constant in fisheries models, fisheries management cannot be effective. The causes of potential failures in fish recruitment (resulting from depressed larval development) must be ascertained and fisheries science must overcome the almost complete separation from gelatinous plankton science (Boero et al., 2008).

Similarly, the quality of the various habitats that fish frequent during their whole lifespan can have a crucial impact on fisheries yields, determining more or less successful recruitment. Yet, the scientists who study fish populations in MPAs are usually not directly involved in traditional fisheries science, even if their research tends to show that MPAs often improve fish yields due to spillover effects (Planes et al., 2000). Fisheries scientists, though, usually disregard the role of MPAs and propose other management measures to promote sustainable exploitation of fish populations. Fisheries scientists are probably right, since the total surface of MPAs is scant, if compared with the vastness of the oceans, and the protected environments are almost invariably coastal and restricted to the sea bottom. While the current extent of protected marine space can improve local conditions, it is nowhere near sufficient to manage the entirety of fish populations. Furthermore, fisheries are just one of the manifold threats to the marine environment, and a more integrative approach to conservation is badly needed.

Good Environmental Status

Of course, a solution might be to increase the size and the density of MPAs, encompassing the SLOSS debate (Single Large Or Several Small) (Olsen et al., 2013) with the Several Large approach. The increase in both the number and the size of MPAs, however, would cause conflicts between national and local authorities and the resident communities that, usually, are resistant to any limitation of their ‘freedom’ of (ab)using the environment.

Networks of MPAs seem the best solution for this conundrum (Olsen et al., 2013). The Marine Strategy Framework Directive (MSFD, 2008/56/EC) sets the target of reaching Good Environmental Status (GES) in all EU waters by 2020. The situation of the European Seas will improve significantly if this strategic goal can be achieved, or at least if the trend towards its achievement triggers effective conservation measures.

The MSFD includes 11 descriptors of GES, which in their synthetic formulation are:

Descriptor 1: Biodiversity is maintained

Descriptor 2: Non‐indigenous species do not adversely alter the ecosystem

Descriptor 3: The population of commercial fish species is healthy

Descriptor 4: Elements of food webs ensure long‐term abundance and reproduction

Descriptor 5: Eutrophication is minimised

Descriptor 6: The sea floor integrity ensures functioning of the ecosystem

Descriptor 7: Permanent alteration of hydrographical conditions does not adversely affect the ecosystem

Descriptor 8: Concentrations of contaminants give no effects

Descriptor 9: Contaminants in seafood are below safe levels

Descriptor 10: Marine litter does not cause harm

Descriptor 11: Introduction of energy (including underwater noise) does not adversely affect the ecosystem.

As Boero et al. (2015) remarked, pursuing GES based on these measures represents a real revolution in the management of marine ecosystems. In the past, the precise measurement of key environmental variables (temperature, salinity, nutrients, pollutants of any kind) was considered to be sufficient to evaluate the state of the environment. This led to the establishment of sophisticated observation systems that check these variables through the use of satellites, buoys, gliders, and a vast array of sensors. The collected data are then stored in huge databases that contain the ‘history’ of environmental systems. The factors that should inform us about the quality of the environment, however, do not represent the real state of any habitat. From the perspective of GES, these variables acquire a meaning only when they affect the living component: if some of these variables change but this does not lead to any change in the biological component of ecosystems, then the change is irrelevant. The individual stressors, furthermore, do not act in isolation from each other. Instead, they interact with each other, with cumulative effects that might lead to misinterpretations of the quality of the environment. If considered in isolation from each other, these variables can have values that are below the threshold that is known to affect the living component of the environment. These effects are often assessed by laboratory experiments, under controlled conditions, in which only one variable is altered, whereas the others remain constant. The ensuing tolerance curves assess the impact of each stressor on selected species. However, even if the values of each stressor are below the thresholds, it can happen that biodiversity loses vigour, and many key species show signs of distress due to cumulative impacts (Claudet and Fraschetti, 2010).

To cope with this shortcoming, the MSFD defines GES while considering the status of both biodiversity and ecosystem functioning. The first descriptor of GES is just the status of biodiversity, whereas all the other descriptors regard the impact of specific stressors on biodiversity, ecosystem functioning and, in the case of Descriptor 9, human health.

Once a stress is identified, in terms of biodiversity and/or ecosystem function perturbation, then it can be addressed so as to mitigate its impact.

The logic of this approach is impeccable, but its application is far from straightforward. It is very simple to produce sensors that measure physical and chemical variables; even biogeochemistry can be assessed with automated instruments. Moreover, the geological features of the sea bottom can be mapped and assessed with very powerful tools. The descriptors of GES, however, consider biodiversity and ecosystem functioning, and the currently available instruments do not measure these features: they mostly consider abiotic features or measure some simple biotic variable, such as chlorophyll concentrations.

A new way of looking at the quality of the environment is then required, and the study of MPAs is somehow ‘pre‐adapted’ to tackle this problem. Marine Protected Areas have been instituted to protect biodiversity and to enhance ecosystem functioning, and so adhere, at least in theory, to all the specifications of GES. The assessment of the efficacy of MPA management should consider the attainment of GES. If the requirements prescribed by some descriptors are not met, management should be changed in order to remove impediments to the attainment of GES.

Connectivity

The Marine Strategy Framework Directive of the European Union does not require the attainment of GES in MPAs only: GES is to be reached in all EU waters by 2020. This expectation is very ambitious, since GES is not reached even in the best‐managed MPAs, but its logic is flawless. It is futile to hope for GES at any one place, if the surrounding environment is not in good condition as well. Marine Protected Areas are not like islands, separated from each other by the sea: the sea connects them.

Every individual living at a specific location produces propagules (the life cycle stages that propagate the species, whether as eggs, larvae, fragments, adults, etc.) that are taken away by the currents, to colonize other sites. Each site is a source of propagules for downstream sites that are reached by the current passing in its vicinity, and is a sink of propagules coming from the organisms living at upstream sites. Connectivity, then, is the degree of connection across sites within a given area. The very concept of connectivity teaches us that it is pointless to manage specific sites (e.g. MPAs) without managing the systems in which they are nested in terms of connectivity. This insight is leading to a paradigm shift in conservation biology: from MPAs to networks of MPAs (Olsen et al., 2013).

Connectivity is a very general concept: the connections among various parts of a given water body cannot be measured in a way that represents all living beings. Some species have a higher vagility (i.e. propensity to move from one place to another) than others and the differences greatly affect connectivity at a micro level. Grantham et al. (2003) tackled the problem of dispersal distances in a suite of habitats, considering just marine invertebrates, and reached the conclusion that the ensuing connections are very varied and that MPAs must therefore be designed based on the specific habitats that are going to be protected. Accordingly, networks of MPAs should encompass this problem, providing protection over large scales. However, it is also important to design MPA networks so as to respect complex connectivity patterns, in order to achieve a compromise that covers the different scales of vagility of the species assemblages that are going to be protected and/or managed. Knowing the basic biology of species, however, is not enough: ecological constraints and habitat availability can restrict the colonization of localities that can be reached by a given species but that are not suitable for its existence. For example, Johannesson (1988) considered two species of the mollusc genus Littorina with opposite dispersal strategies (planktonic versus brooding). The species with planktonic larvae should be a better colonizer than the brooding one. However, the brooder species had a higher propensity than the one with planktonic larvae to persist at a sink habitat widely separated from source areas. The ‘paradox of Rockall’ (Johannesson, 1988) shows that larval dispersal is not the sole factor responsible for connectivity. Sink areas that are distant from propagule sources tend to be colonized by low dispersal species that can reach them by rafting and that re‐colonize the area without dispersing their propagules. In this regard, Boero and Bouillon (1993), analysing the distribution of more than 300 hydrozoan species of the Mediterranean Sea, showed that species with a long‐lived medusa stage do not have a wider distribution than that of brooding species, brooders often being more widespread than highly vagile species (Shanks et al., 2003).

As a result of such studies, it is clear that the levels of connectivity across an area are better studied by at least four methods:

The reconstruction of the oceanographic framework that potentially connects the various sites

The search for propagules (including asexual ones, and rafters) in the plankton collected in the connecting currents

The similarity of species assemblages across the considered area (so‐called beta diversity)

The similarity in the genetic composition of a suite of species that represent a vast array of taxa.

The integration of the results of these different analyses leads to a more reliable representation of the degree of actual connectivity, helping to design more ecologically coherent networks of MPAs.

Networking According to Nature or to Bureaucracy?

The application of coherent policies of management and conservation of MPAs is particularly well developed in the Mediterranean area. The management entities of many Mediterranean MPAs are part of MedPAN (Webster, this volume) and, through it, the best practices evolved by the directors of each MPA are disseminated and improved, so as to find increasingly better ways of protecting nature. It is undeniable that issues regarding nature conservation have to be addressed over vast scales, and that the comparison of the efficacy of measures at different places is conducive to increasingly better ways of protecting the environment. It is also true, however, that there is not a one‐size‐fits‐all way of solving the problems stemming from our relationship with the rest of nature. Special measures are necessary to protect remarkable properties of the marine environment, such as the presence of unique expressions of biodiversity in terms of either species (e.g. monk seals Monachus monachus, or cetaceans) or habitats (e.g. bioconstructions of any kind). Defending unique structures, however, is not enough: connectivity calls for a more integrated approach than just a structural one. Structures must be coupled with the ecosystem functions that allow for, if not underpin, their existence, and this approach calls for the expansion of management far beyond the boundaries of MPAs.

It is crucial, in this framework, to identify the units of conservation, namely the portions of marine space that are highly connected with each other and whose features are more dependent on each other than on those of sites that belong to other units. The identification of these units leads to the construction of networks of MPAs that are based not only on the enforcement of protection measures through bureaucratic imperatives, but also on the recognition of ecological principles that rule the functioning of the managed environments, just as the definition of GES prescribes.

These units might be based on climatic and biogeographic features, comprising areas where species compositions are similar due to shared climatic conditions; or on oceanographic features, where current patterns determine propagule transport; or on geological features of the sea bottom; or, indeed, on geo‐political features that might be conducive to common management by various states. In such politically fragmented seas as the Mediterranean and the Black Seas, this approach requires development of and adherence to international agreements since it is highly unlikely that a single state will cover the whole extension of ecologically coherent conservation units.

It is evident, however, that the identification of these units of conservation must be holistic, covering most of the features that the single disciplines making up the complex of marine sciences now study in isolation. To satisfy this need, Boero (2015a) proposed to treat the marine environment as a living super‐organism made of cells: the ‘cells of ecosystem functioning’ (CEFs). The exercise of dividing the marine space into larger conservation units than MPAs is not novel (see Olsen et al., 2013 for a review), and its necessity is shared throughout the scientific community and among decision‐makers.

Towards a Holistic View of Marine Systems

The previously mentioned quest for integrated, ecosystem‐based, and holistic approaches to marine conservation requires a complex representation of marine spaces based on the assemblage of the available knowledge in an ecologically coherent fashion.

The physical background is the backbone of ecosystem description. The discovery of the oceanic conveyor belt (Broecker, 1991), with the recognition of the crucial role of polar regions as surface sites of deep water formation, marked a revolution in physical oceanography that parallels the discovery of continental drift to explain the current disposition of continental masses. The oceans are in fact one, the global ocean, and all are connected by horizontal and vertical currents. The cold and dense surface waters of the poles tend to sink and to become the deep waters of non‐polar portions of the ocean system, pushing up the spent waters of the deep. Everything is connected, in the oceans, and life is running on an apparently perpetual conveyor belt that distributes nutrients and propagules throughout the world. The single, interconnected oceanic system, however, can be divided into coherent portions, defined by the disposition of continental masses.

The Mediterranean Sea, in particular, due to its geological, oceanographic and bio‐ecological features, is a miniaturized replica of the world ocean and, due to its smaller size, responds more quickly to the drivers of change that affect the whole planet (Lejeusne et al., 2010). It is convenient, thus, as a first approach to the identification of coherent conservation units, to focus on the Mediterranean Sea so as to set up a feasible rationale that could possibly apply to whole oceanic systems.

From a physical oceanography point of view, the Mediterranean conveyor belts (Pinardi et al., 2004) can be considered as analogous to the large oceanic conveyor belt (see Figure 1.1).

Figure 1.1 Circulation patterns in the Mediterranean Sea. A surface current enters the basin from the Gibraltar Strait, flows through the Sicily Channel and reaches the Levant Basin. The Gibraltar Current flows back at about 500 m depth as the Levantine Intermediate Current. Water renewal below 500 m occurs through the ‘cold’ engines in the Gulf of Lions for the Western Basin and in the Northern Adriatic and Northern Aegean Seas for the Eastern Mediterranean. In the cold engines, cold, oxygen‐rich water flows through canyons (bottom left inset) with a ‘cascading’ process. The canyons outside cold engine areas can trigger upwelling events (bottom right inset). Other patterns of circulation regard the formation of gyres (top inset).

Artwork: Alberto Gennari.

The Mediterranean Sea has a higher salinity than the Atlantic Ocean since freshwater inputs are lower than evaporation rates. The superficial Gibraltar Current enters from the Gibraltar Strait and brings Atlantic waters into the Mediterranean Sea, compensating the water deficit due to excessive evaporation. The Gibraltar Current crosses the Sicily Channel and flows into the Eastern Mediterranean, to flow back at about 500 m depth as the Levantine Intermediate Current that returns to the Atlantic, through the deepest part of the Gibraltar Strait. Since the average depth of the Mediterranean Sea is 1500 m, and the deepest part of the basin, in the Ionian Sea, exceeds 5000 m, the water renewal of the upper 500 m is not enough to bring oxygen to the depths of the Mediterranean Sea, where plants and other primary producers do not have enough light to perform photosynthesis and produce oxygen. Without photosynthesis, deep‐sea animals would rapidly consume the oxygen dissolved in the water, leading to anoxic conditions that are not favourable to metazoan life. Without an oxygen supply from the surface, the Mediterranean deep‐sea biodiversity would be much reduced and just a few simple life forms would survive, as happens in the Black Sea below 300 m depth.

The ‘cold engines’ of the Gulf of Lions, the Northern Adriatic and, from time to time, the North Aegean are crucial to the existence of deep‐sea life in the Mediterranean Sea. At these sites, northern winds enhance evaporation and lower the temperature, causing a marked density increase in the well‐oxygenated surface waters. The thermo‐haline differences of the water masses of the cold engines in respect to the surrounding waters result in the so‐called cascading of dense oxygenated waters that cross the continental shelf and, then, reach the deep sea through marine canyons. The cold engine of the Gulf of Lions renews the deep waters of the Western Mediterranean Basin, whereas the Northern Adriatic engine, sometimes replaced by the North Aegean one, refreshes the depths of the Eastern Mediterranean Basin.

The Gibraltar and the Levantine Intermediate currents join the various parts of the basin, defining the Mediterranean Sea as a single and very large unit. The cold engines produce vertical thermo‐haline exchanges that define the Western and the Eastern Mediterranean as two large sub‐units that, based on coastal morphology, are in their turn divided into the well‐known ‘seas’ that make up the Mediterranean system.

Oceanographic conditions determine further sub‐divisions of the seas that make up the Mediterranean. In the Adriatic Sea, for instance, the cold engine causes a thermo‐haline current that flows southwards across the continental shelf and along the Italian coast to the Ionian Sea through the Bari Canyon. To balance this outflow, an incoming current enters the Adriatic Sea from the eastern coast of the basin, and reaches the Gulf of Trieste, where the circle is closed. The presence of headlands such as those at Istria, Conero and Gargano leads to the formation of a northern, a central and a southern gyre, with horizontal currents that connect the western and the eastern coasts of the basin, along which the currents flow in opposite directions. In this way, the Adriatic Sea could be divided into three coherent oceanographic cells, where ecosystems might function in distinct fashions, while being anyway connected by the northward current along the eastern Adriatic coast and the southward current along the western coast.

The Adriatic Sea is shallow and does not have canyons in its central and northern part, but canyons leading to the deep sea from the coast are a common feature of the rest of the Mediterranean shelf. Some are involved in the cascading phenomena generated by the cold engines but, in the majority of the canyons, the currents that flow parallel to the coast tend to sink offshore, bringing oxygen to the deep sea. These offshore downwellings push deep waters through the canyon, resulting in upwelling currents that connect the deep sea with the coastal areas (Hickey, 1995). There are about 500 Mediterranean canyons that, presumably, play the role of auxiliary engines to the three main cold engines, and underpin the survival of life in the deepest part of the Mediterranean Sea through vertical water exchanges. The upwellings, furthermore, bring nutrients towards the shore, enhancing primary production such as the spring phytoplankton bloom. Based on these oceanographic patterns and on the presence of a higher concentration of resting stages of both phyto‐ and zooplankton than outside the canyons, Della Tommasa et al. (2000) proposed that marine canyons are reservoirs of propagules (in this case resting stages of planktonic organisms) that are injected towards the coast together with the nutrients, so triggering the phytoplankton and zooplankton blooms that are at the base of the functioning of all oceanic systems.

The hydrodynamic patterns, generated by a combination of wind energy, changes in salinity and temperature, and interactions of currents with bottom and coastal morphology, define the physical framework that leads to the formation of masses of water that are more connected within their boundaries than they are with neighbouring masses, while remaining part of a coherent water body. The main sub‐units can be further divided into smaller units according to the presence of fronts, gyres, eddies, upwellings and downwellings, defining what Boero (2015a) called the cells of ecosystem functioning, CEFs, mentioned earlier. With this metaphor, the Mediterranean Sea is a body (which is anyway dependent on other bodies, in this case the Atlantic Ocean) that can be divided into increasingly smaller functional parts, from wide ecological regions sensu Longhurst (2010) to CEFs as the smallest functional units.

The Cells of Ecosystem Functioning

Oceanographic conditions shape the associated ecological processes. The ensemble of areas where physical processes connect different portions of the environment might be considered a CEF. However, the long‐term observation of oceanographic features shows high variability, including sudden and radical changes, as happened with the Eastern Mediterranean Transient (Pinardi et al., 2004). Phenomena such as El Niño, the North Atlantic Oscillation, and, in recent decades, global warming, lead to a suite of multiple states that might not overlap in space. Eddies and gyres, furthermore, can have variable strengths, and even invert their rotation. Upwellings are stronger in some seasons and weaker in others. Extreme events such as the occurrence of very hot or very cold periods can have huge impacts on biological features, with effects that persist for a long time after the occurrence of the episodes. Rivetti et al. (2014), for instance, showed that the deepening of the summer thermal stratification caused large‐scale mass mortalities of resident species of cold‐water affinity. Temperature increases, furthermore, have favoured the massive expansion of non‐indigenous species that continue to enter through the Suez Canal, establishing viable populations in the Mediterranean Sea.

The strong annual (seasonal) and inter‐annual fluctuations and variations of the physical drivers determine the bio‐ecological features that represent an integration of these fluctuations over the long term (Boero, 1994), with episodic events adding variability to this complex situation (Boero, 1996).

The interactions among species assemblages (the expression of biodiversity) and the physical variables lead to the formation of ecosystems and determine their functioning (Boero and Bonsdorff, 2007).

The inter‐annual variability of planktonic communities is well known from long‐term series (Boero et al., 2014), whereas only recently has the long‐term response of benthic communities to important physical changes, mainly due to global climate change, started to be quantified (Puce et al., 2009). It is important, then, to establish not only the potential CEFs, in terms of physical features, but also the tangible CEFs in terms of biodiversity and ecosystem functioning: a CEF is defined by a higher level of internal connectivity compared with connections to nearby CEFs. It can happen, however, that cells that appear physically separated, at least temporarily, such as the central and southern Adriatic cells, defined by two adjacent gyres, might have such connected biological populations that a single, larger cell and, hence, a single large conservation unit, should be defined.

Obviously, these multiple physical states, leading to multiple ecosystem states, can be revealed only through continuous observation and cannot be predicted by current modelling techniques. No model, for instance, predicted the occurrence of the Eastern Mediterranean Transient.

Moreover, the approaches followed so far to assess the quality of the environment are more focused on structure than on function. The evaluation of ecosystem functioning in large marine ecosystems has been assessed only rarely (e.g. Godø et al., 2012).

Mapping the Seas

Mapping benthic communities is relatively easy and, with state‐of‐the‐art technologies, can be accomplished in reasonable time frames. Benthic communities can be subject to strong seasonal variation, especially in coastal areas, but their areas of occurrence are generally rather stable in space. Maps can be made from time to time and compared so as to ascertain changes in habitat distribution.

The Habitats Directive, with the associated Natura 2000 network, applies a terrestrial approach to the marine realm. The description of habitats, furthermore, is based on the features of vegetation and on the concept that the dynamics of communities leads to climax conditions after a series of deterministic seres. These concepts apply only partially to the marine domain. In marine systems the water column is the most crucial component, being the habitat of both plankton and nekton, whose temporal variability is very high if compared with that of the benthos. The connections between the sea bottom and the water column are so intimate that the functioning of their communities cannot be understood if they are considered as separate entities (Boero et al., 1996).

Terrestrial habitat maps are bi‐dimensional and consider the vegetation as a descriptor of diversity. Maps of marine habitats resulting from the application of the Habitats Directive are similar to terrestrial ones, since they consider just the benthic realm. However, marine habitat maps would be far more complex if the water column was taken into account. What is happening at the surface does not necessarily reflect the rest of the water column, and temporal patterns are very distinct, so the same physical space has different ecological features in different periods of the year, usually changing from year to year. The dimensions are four: the two of the surface area of the sea bottom, the third one of the volume of the water column (and its diversity through its entire depth), and finally the time dimension.

As a result, CEFs are fuzzy units that cannot always be sharply defined (due to their temporal instability) but nevertheless are more internally coherent than