Biodiversity Monitoring in Mediterranean Marine Protected Areas: Scientific and Methodological Challenges

Abstract

Biodiversity is a portmanteau word to indicate the variety of life at all levels from genes to ecosystems, but it is often simplistically equated to species richness; the word ecodiversity has thus been coined to address habitat variety. Biodiversity represents the core of the natural capital, and as such needs to be quantified and followed over time. Marine Protected Areas (MPAs) are a major tool for biodiversity conservation at sea. Monitoring of both species and habitat diversity in MPAs is therefore mandatory and must include both inventory and periodic surveillance activities. In the case of inventories, the ideal would be to census all species and all habitats, but while the latter goal can be within reach, the former seems unattainable. Species inventory should be commeasured to investigation effort, while habitat inventory should be based on mapping. Both inventories may profit from suitability spatial modelling. Periodic surveillance actions should privilege conspicuous species and priority habitats. Efficient descriptor taxa and ecological indices are recommended to evaluate environmental status. While it seems obvious that surveillance activities should be carried out with regular recurrence, diachronic inventories and mapping are rarely carried out. Time series are of prime importance to detect marine ecosystem change even in the absence of direct human impacts.

1. Introduction

Biodiversity is a portmanteau word that expresses the value of biological variety at different levels of integration, from genes to the entire ecosystem [1,2]. For many authors, the meaning of biodiversity is above all linked to the concept of species richness, that is, the number of species found in a specific site, region or ecosystem. Although widespread, this acceptation is too simplistic, as it neglects the other levels of biological variety [3]. Perhaps as a reaction, the term ”ecodiversity” has been coined to focus on the variety of habitats, rather than species [4], while on the opposite side of the biodiversity spectrum, environmental DNA is increasingly being used to assess genetic diversity in marine ecosystems [5].

The significance of biodiversity as an indicator of the health of the environment and the functioning of ecosystems is fully recognized, not only by scientists, but also by mass media, administrators and public opinion [6]. Conciliating human development with biodiversity conservation is at the root of the emerging discipline of socioecology [7]. However, most of the attention and debate on biodiversity has concerned predominantly the terrestrial environment, while marine biodiversity has historically received less attention [8]. From this point of view, the situation in the Mediterranean Sea is no exception [9], despite the great cultural and economic importance that the sea has always had for the Mediterranean countries [10].

It is claimed that biodiversity on land is much greater than in the sea, but we must remember that three quarters of the number of terrestrial species are insects, mainly beetles. It could therefore be argued that a significant part of terrestrial biodiversity depends on the evolutionary success of a single higher taxon. On the contrary, the marine environment shows a higher phyletic diversity and a greater functional and trophic diversity [11]. Apart from these differences, however, the role and problems of biodiversity at sea are the same as on land: they are simply less known and/or perceived [12,13]. Compared to terrestrial ecosystems, the sea has been much less studied, and the capacities for underwater exploration have not been developed until the second half of the 20th century [14,15]. Thus, the historical basis of knowledge of marine biodiversity is short [16,17]. Naturalists of the 18th and 19th centuries, such as Jean Baptiste de Lamarck (1744–1829) and Thomas Huxley (1825–1895), did not believe that the extinction of marine species by humans was possible [18]. Their opinion reflected the widespread belief that the oceans were an inexhaustible source of food and resources for humanity [19]. These ideas have persisted to the present day, and only recently awareness has grown that marine species may also be at risk of extinction and marine ecosystems at risk of degradation [20,21]. Marine biodiversity is declining at fast rate [22], and consensus that it must be protected is growing [23,24]; a new paradigm is needed for the human relationship with the ocean [25].

Marine Protected Areas (MPAs), although mostly designed to manage fisheries [26], have proved capable to enhance the status of species and habitats [27,28], and are thus viewed, notwithstanding some controversy [29], as the primary strategy for the conservation of marine biodiversity [30,31]. The number of MPAs worldwide has grown from virtually zero to more than 1200 in less than 25 years [32], and this number is expected to increase further in the next years to achieve the goals of the Agenda 2030 for the sustainable development [33]. However, only 31% of MPAs globally are effective, the majority being little more than ”paper parks” [34].

If it is true—as it is true—that the natural capital due to biodiversity also epitomizes an economic capital [35,36], then there is no doubt that its amount must be adequately quantified and then followed over time. Monitoring activities on biodiversity in MPAs must therefore include both the inventory and the surveillance [37]. The present viewpoint paper will discuss these aspects mostly based on experiences in Italian MPAs, expanding and updating previous contributions [38,39].

2. Monitoring as an Inventory

Commonly, the establishment of a MPA is preceded by a series of investigations that typically include inventories of species and habitats [40,41]. This may have generated, in the minds of those who were subsequently called to manage that MPA, the idea that the local biodiversity was “already known” and that no further information was needed.

This way of thinking, much more widespread than one might imagine, undoubtedly derives from the belief that marine communities tend to be stable and in perfect balance with the average conditions of the environment; most changes, seasonal cycles apart, are thus attributable to human impacts [42]. From this belief, which identifies the so-called “equilibrium ecology” and has its roots in the paradigms of the balance of nature dating back at least to the Greek philosopher Herodotus (V century BCE), can derive the falsely reassuring tranquillity that, where human impact is excluded (as in protected areas), it is no longer necessary to invest in the inventory of biodiversity. Equilibrium ecology has been challenged by non-equilibrium ecology – or “new ecology”—which denies that biologically accommodated communities are better structured (i.e., with a greater number of niches realized and therefore higher diversity) than physically controlled communities. Disturbance has assumed a key role as regulator of the composition and structure of communities [43]: communities will be more structured at intermediate disturbance levels, also through physical heterogeneity and space-time mosaics generated by the so-called “patch dynamics” [44]. In altered disturbance regime, or when disturbance intensity exceeds a certain threshold, unpredictable change may occur, leading to abrupt phase shifts [45,46,47].

The new ecology led to a revolution in the way we see biological communities: equilibrium ecology describes them as deterministic and predictable; non-equilibrium ecology considers them non-deterministic and unpredictable, due to stochastic disturbance events [48]. The idea has also emerged that biological communities are chaotic, i.e., deterministic but unpredictable due to the great sensitivity to small variations of the initial conditions [49]. In the last decades of the 20th century, ecology went through a phase of crisis, which has been the melting pot where a new conceptual vision has been forged [50]. Such a critical phase saw as essential to focus on change rather than on equilibrium [51]. Today, the concept of stability in ecology is questioned [52], and it has been fully realized that marine communities neither tend to, nor fluctuate around, equilibrium [53]: they simply change, and such changes occur at time scales shorter than one might have thought [54]. The emerging ecology should probably be understood as “the ecology of change” [48]. It is from this awareness that the need arises for a diachronic (i.e., repeated over time) inventory of species and habitats within the MPAs [55,56].

For the inventory of species, specimen sampling and/or observation (including photo and video) are a current approach. However, three innovative techniques are emerging that do not require the collection of organisms: environmental DNA, passive acoustic methods, and baited remote underwater video systems.

Marine organisms leave traces of their DNA in seawater or sediments, so that the detection of species-specific environmental DNA (eDNA) fragments may represent a non-invasive and sensitive tool to investigate the whole marine biota, from microorganisms to vertebrates [5,57,58,59]. A major advantage of the eDNA approach is that sampling water or sediments is rapid and easier than other methodologies currently used for assessing biodiversity, and can routinely applied on a large scale [60]. Studies on fish showed that eDNA may detect cryptobenthic, pelagic, and rare species that are often overlooked by the traditional visual surveys [61]. The potentiality of the method is still to be fully explored: experiences to date indicate that it is not yet capable of reliably identifying all the species actually present in a given area but anyway provides an important complement to traditional methods [62]. At present, biodiversity assessments based on eDNA are limited by the availability of sequences in barcoding reference databases [63].

Deploying remote acoustic sensors in the sea allows capturing all the sounds in the surrounding environment [64]. This underwater soundscape emerges from geophysical, biological, and anthropogenic sources [65]. The variety of sounds produced by organisms has been labelled acoustic biodiversity, which includes several organizational levels, from individuals to ecosystems, and provides a long list of ecological information, such as: species absence/presence, population density, population structure, community structure, seascape architecture, animal phenology, reproduction period, migration period, species interactions or ecosystem functions [64,65,66]. Marine species show species-specific acoustic signatures that can be used by naturalists for identification without visual contact [66]. Examples in the Mediterranean Sea include the study of the circadian rhythms of snapping shrimps and fishes [67], the occurrence and habits of dolphins [68,69], the relationship between fish and benthic reef assemblages [70] and the comparison between fish inventories by passive acoustics and standard visual census surveys [71,72]. Indices have been devised to provide non-invasive information on the temporal and spatial patterns of marine biodiversity and on the anthropogenic impact on marine life [73]. At the present state of the art, however, the application of acoustic indices to assess marine biodiversity needs caution [74], as they still need to be complemented with traditional observer-based methods [64,75].

Baited remote underwater video (BRUV) systems consist of single or stereo underwater cameras filming a bait canister that attract fish and invertebrates. The technique affords the only non-extractive sampling option for some situations (e.g., at depth), but more often can complement other traditional methods. A limitation is that samples from baited video are biased towards predatory or scavenging species and exclude herbivorous or omnivorous species [76]. The use of BRUV in the Mediterranean Sea is still sporadic, but it has shown consistency with visual census surveys and better performance in detecting high-level predators [77].

An important aspect seldom highlighted in studies on marine biodiversity is that the number of species found must be commensurate with an estimate of the effort required to take their census, such as cost or time, number of samples or the investigated area. For example, the fish fauna diversity of a MPA in which a certain number of fish species are observed during a single dive is likely to be greater than that of a MPA in which a comparable number of fish species can only be seen doing many dives. One of the most widely used methods to commensurate species richness and census effort is the species-area curve or species-area relationship [78]; other measures of the sampling effort (e.g., time or number of samples) can be used instead of area [79]. In its simplest form, this curve can be described by an equation such as: S = c·A^z, where S is the number of species, A is the area (or another measure of effort), and c and z are two parameters. The parameter c can be considered as the number of species that may be expected with a unitary sampling effort (a proxy for α diversity, in term of species richness). The parameter z, the slope of the curve, represents the rate of increase in the number of species, which may depend on the biogeographical region under consideration and other factors but above all on the heterogeneity of the habitat (β diversity). Since z is independent from the value and unit of measure of the parameter on the abscissa, it can be used as a non-dimensional measure of species richness [80]. The value of S when A tends to infinity can represent a measure of the theoretical maximum number of species living in that region (γ diversity). A simple method to estimate γ diversity (as the theoretical maximum number of species) is plotting the reciprocals 1/S of the cumulative number of species against the reciprocals 1/A of the number of sampling effort units and fitting the plot with a straight line of equation y = ax + b (Figure 1a): the reciprocal of the intercept b, therefore, will represent the number of species to be found after an infinite sampling effort [80]. This approach is particularly useful when comparing species numbers obtained with different sampling efforts (Figure 1b): for instance, a dramatic decrease of epibenthic sessile species richness over 25 years was evidenced, notwithstanding reduced investigation effort (numbers of dives), in an area deprived of any form of protection against fishing and anchoring [81].

For the inventory of habitats, the main tool is mapping [82]. In the terrestrial environment, thematic environmental cartography has long played a role of prime importance for land management [83]. At sea, this is not yet the case, both because of a lesser tradition of considering the sea as a “territory” [84] and because of the obvious operational difficulties and costs [85]. It would take 125–200 ship-years to survey the oceans, costing billions of euros: thus, less than 30% of the seafloor has been mapped to date [86]. This does not detract from the fact that there is an important tradition of ecological cartography in the Mediterranean Sea, in origin mainly by the French [87] and Italian schools [88], but currently also in many other countries. Several of these maps are strictly monothematic, especially aimed at mapping the meadows of the seagrass Posidonia oceanica [89] adopting a binary approach (patch-matrix), while the so-called bionomic (or biocoenotic) maps rely on the patch-mosaic model [90] and take into consideration all the benthic habitats present in the area [91]. In absence of bionomic maps, fishery maps may sometime provide information on the distribution of marine habitats [92].

Non-destructive mapping procedures, based on remote acoustic and optical techniques [93], should be preferred, minimizing the collection of physical samples. Common adopted acoustic methods include single-beam echosounder, multibeam echosounder and side-scan sonar [94]. A comparison of the three techniques has been carried out mapping a reef of the horse mussel Modiolus modiolus in the Irish Sea [95]: it was concluded that side-scan sonar was the most discriminating method but that the reef was anyway reliably mapped by all the three acoustic techniques. However, the three maps exhibit differences that may compromise comparability in routine monitoring (Figure 2).

Acoustic methods cannot be employed in very shallow water because of boat draft and restricted manoeuvrability in proximity of the coastline; they can be complemented by optical remote sensing, which on the contrary is inefficient in waters deeper than 10–20 m due to the reduced penetration of light in the water [82]. Optical remote sensing techniques include satellite imagery [96], aerial photography [97], and satellite-like multispectral and hyperspectral sensors [98], such as LIDAR (Light Detection And Ranging) [99], CASI (Compact Airborne Spectrographic Imager) [100] and others, mounted on aircrafts or on UAV (unmanned aerial vehicles, also known as drones) [101]. Cost and efficacy of the different optical techniques may differ greatly [102].

The combination of acoustic and optical data has been shown to be the most reliable approach to obtain high-resolution benthic habitat maps [103]. Algorithms do exist for the automated interpretation of acoustic and optical outputs with an unsupervised approach; however, a supervised approach, with inspections in situ (“sea truth”) using towed video cameras, ROVs (Remotely Operated Vehicles), AUVs (Autonomous Underwater Vehicles) or diving, are typically necessary for disambiguation [104,105]. Combining acoustic methods and ROVs, for instance, allows efficient surveying also at great depths [106]. The characterization and definition of marine habitats may benefit of a seascape approach, which merges mesological, geological and biological data [13,107,108,109] and stands at the basis of the ecotypological classification of marine ecosystems [110,111]. Geological features may often contribute to the environmental value of marine habitats [112,113,114].

The scale at which the cartography of the habitats of a MPA must be produced is of fundamental importance, as it dictates the resolution and hence the number of habitats found. Large scales (>1:5000) are suitable for illustrating in detail small areas where rocky bottoms dominate, which is often the case with MPAs [115,116]. Intermediate scales (between 1:10,000 and 1:25,000) are useful for acquiring a synoptic view of the entire MPA when the MPA is large or to embrace the whole physiographic unit where it is located [117,118,119,120]. Small scales (1:50,000 or less) can highlight the ecological situation of the MPA in the context of the natural region to which it belongs [121,122]. To reconcile relatively large scales and regional coverage, atlases have been proposed whose pages contain contiguous or slightly overlapping maps [123,124,125,126].

It must be emphasized that the choice of the scale does not only involve, as is obvious, a greater or lesser detail: it affects the very meaning of the phenomena represented [127]. There is no “natural” scale of ecological systems [128], but rather a hierarchical series of spatial and temporal scales: changing the scale of study and representation of phenomena means describing intrinsically different typologies, levels of organization, and functions [129]. While at limited spatial scales it is not possible to predict the structure of communities—which fluctuates between different alternative states equally probable [130]—at seascape scale the probability increases, as the proportion of habitats in each state tends to remain relatively constant [131]. This is of considerable scientific and practical importance, since the assessment of human impacts requires, as a reference framework, the expected frequency of different states. It may therefore be informative that bionomical maps highlight not only the extent and distribution of the various habitats present, but also their state and dynamic trend, based on the presence of indicator species and other biological and ecological indicators [118,132,133]. The same indicators may also help elaborating sets of evaluation maps, of immediate use for management [85,134]. Combined with maps of human pressures, habitat state maps are of prime importance for marine spatial planning, an important decision-support tool for finding efficient management solutions [135].

It is obviously impossible to establish conservation plans for something that has not been found yet [136]. To maximise the probability of finding what is searched for, inventories of species and habitats may benefit from suitability modelling, which allows predicting their occurrence on the basis of known environmental variables, such as depth, distance from the coast, bottom type, etc. [104,137]: in this way, maps of expected occurrence for either species (Figure 3) or habitats can be produced, verifying their actual presence with a selected number of sea truth checks.

Examples of repeated habitat mapping in MPAs are unfortunately few [138,139,140], notwithstanding their importance to evaluate change over time [141]. Maps produced in different periods may be processed with GIS (Geographical Information System), using overlay vector methods and diachronic analyses to quantify the percent gain or loss of extent of given habitats through concordance (i.e., no difference) and discordance (i.e., difference) maps [142,143]. Errors in data acquisition and processing by different operators may blur the evaluation of change over long time-scales, so that compliance with rigorous design is mandatory [144]. Using some caution, however, diachronic mapping may provide useful information even in presence of errors. Analysing a time series of 13 maps of Posidonia oceanica meadows in the Bergeggi MPA (Ligurian Sea, NW Italy) between 1987 and 2018 [116,126,145], it has been possible to recognize three major sources of error or unreliability: (i) scale too small, (ii) positioning accuracy, and (iii) survey technique [146]. Maps were therefore classified as highly reliable (4 maps), moderately reliable (7 maps) or little reliable (2 maps). Assigning the information taken from the maps different “weights” (3, 2, 1, in the order) according to their reliability (Figure 4), the resulting trend illustrates a decline during the last decades of the 20th century (consistently with a general trend in the whole Mediterranean basin [147]), followed by an apparent partial recovery in recent years, in coincidence with the adoption of protection measures [148,149].

How often should diachronic inventories be made? It is possible that there is no univocal answer, and that much depends on the biogeographical, ecological and anthropogenic specificities of the area in which the MPA is inserted. Repeating species censuses and habitat mapping at least every 10 years is however desirable [85].

3. Monitoring as Surveillance

Carrying out exhaustive inventories with great frequency is out of the question for reasons of cost and operation. Drawing up the list of the species present in a MPA can cost thousands of euros per km of coastline, even if only considering the “most important” taxa, whatever is meant by this expression (see below); the cost per species may range from a few euros (in the case of common species) up to hundreds of euros (in the case of rare species) [39].

It is therefore essential to implement continuous surveillance plans that take into consideration a selected number of species and habitats. In this case, however, monitoring does not address the verification of the presence, but rather the detection of some quantitative parameters. In the case of species, for example, the size and demographic structure of the populations are among the most recommendable parameters [150,151,152,153]. Contrary to the logic of inventories, this type of monitoring does not invest most of the sampling effort in finding what is rare, but in defining as strictly as possible the quantity and conservation status of some selected species. It should be emphasized that this is the approach that usually provides the most immediate and most noticeable measure of the reserve effect to the general public [154]: the presence of rare species is generally felt less interesting than the increase in the number and size of groupers or other popular fish [39].

As for the type of sampling to be adopted for the surveillance of biodiversity in MPAs, also in this case there is growing consensus on the use of non-destructive techniques, which do not require the collection and sacrifice of specimens. Photographic sampling responds to this need and also has the advantage of obtaining nonetheless a physical “sample” (the photographic image) that can be analysed and archived [155,156]. Similarly, video imagery has acquired great relevance in the last decades [157], especially for the monitoring of mesophotic habitats [158,159]. Another technique that has undergone great development is visual census, which can be used both for species belonging to the sessile or sedentary epibenthos [160] and for fish [161]. It is not applicable to the infauna except indirectly, such as counting of burrows, pseudofaecal accumulations or other signs on the sediment surface [162]. Obviously, it cannot be used for tiny mobile fauna or plankton (with the possible exception of the gelatinous macroplankton [163]). Counts are carried out in permanent plots along paths (transects) or within well-defined surfaces (quadrats) suitably located in space (Figure 5), in order to ensure the possibility of a rigorous statistical treatment of the data [81,156]. The adoption of precise standardized survey protocols and training of the investigators minimizes the subjectivity and error inherent in visual censuses [164].

4. What to Monitor?

In the case of inventories, the ideal would be to be able to census all species (from microorganisms to vertebrates) and all habitats. While the latter goal should be within reach, the former seems unattainable [165]. However, the inventory of the entire planet’s biodiversity might even be an attainable goal [166], as was the creation of the map of the human genome when there had been a strong will to invest in the necessary resources [167]. The MPAs could represent a concrete opportunity to try to become closer to the goal of taking a census of the biodiversity of our seas.

However, it should be emphasized that when asked what to monitor, different answers are possible depending on the specific purpose. Starting from the case of checking the size and state of populations of certain species, it is likely that these species belong to a category at risk. In conservation biology it is customary to distinguish three situations, according to the criteria of the IUCN (International Union for Conservation of Nature): “endangered species” are close to extinction; “threatened species” are those that risk disappearing in the foreseeable future; “endemic species” are those with a narrow distributional range [168].

The Mediterranean has numerous endemic species, many are currently threatened and some are probably in danger [169,170]. The mass media, public opinion and administrators are realizing this problem, but their interest mostly concerns the so-called “flagship species” [171], i.e., charismatic species [172] mostly belonging to mammals, turtles, some fish and a small number of popular invertebrates and plants [173,174].

This attitude reflects how humans value other living beings [175,176]. It is relatively easy to obtain public consensus for the protection of seals and dolphins, since humans have a kind of sympathy for large mammals [177,178]; but who cares about the extinction of a marine alga? This is an attitude that finds some justification in the concept of exergy, recently developed in systems ecology and which embraces energy and information [179]: considering the genetic information contained in individual cells, it is possible to estimate about 600 non-repetitive genes in bacteria, about 850 in algae, about 30,000 in higher plants and about 140,000 in mammals [180]. Thus, it can be argued that the organisms placed highest in the evolutionary “tree of life” are the most important for the ecosystem. The charismatic megafauna typically include wide-ranging species that may act as “umbrella”, i.e., focal or surrogate species whose protection implies the protection of many other species living within their range [181,182]. The rising awareness among common people about the actual meaning of biodiversity and the importance of its monitoring has recently led to the launch of citizen science projects, in which volunteers (e.g., students, fishermen, divers) are involved in gathering data that would otherwise be impossible to collect because of limitations of time and resources [183,184]. Proper training and validation and verification by taxonomic experts can provide quality-filtered data that improve taxonomic representation and the geographic breadth of species monitoring [185,186].

There are therefore both scientific and opportunity reasons to suggest that surveillance activities preferentially target populations of species attributable to the aforementioned categories and familiar to the general public (fish and other marine vertebrates, large molluscs, decapod crustaceans, etc.). Frequently, these species are found in top positions in food chains and therefore exert a top-down control over the functioning of ecosystems (“keystone species” [187]). However, priority must also be given to those species which, by giving shape to the submerged landscape (erect sponges, gorgonians, seagrass, large phaeophyceans) or even by building bioherms (coralline algae and many bioconstructional invertebrates [188]), exert a bottom-up control of ecosystems (“structural species” [187]). Both keystone species and structural species have the capacity of modifying physically the environment in which they thrive, and have been thus defined ecosystem engineers [189], allogenic the former (they modify the environment with their behaviour), autogenic the latter (they modify the environment through their own mass).

As regards the actions of diachronic inventory of the species, the priorities must be chosen above all in terms of efficiency. Since it is hardly possible to census all living species in MPAs, it may be wise to start with those belonging to taxa that can act as “efficient descriptors” of biodiversity [190]. Among the requirements of a taxonomic group to be considered an efficient descriptor, the following can be mentioned:

• contain numerous species;

• large dimensions;

• wide distribution in the different habitats of the MPA;

• sufficiently simple identification;

• easy and productive sampling, possibly with non-destructive methods.

Not all the major taxa of marine organisms meet these requirements: algae and most invertebrates require the intervention of specialists [191]; fish and to some extent molluscs (Figure 6) are undoubtedly among the most suitable groups. A coordinated research effort among Mediterranean MPAs to identify which taxa to monitor and to develop the necessary skills would be desirable.

As regards the monitoring of habitats, first of all it should be emphasized that the criteria diverge from those adopted for species. Public opinion has a different attitude in the two cases. For habitats, the criterion is essentially that of utility. It is considered useful to have healthy marine ecosystems mainly because they are more appreciated for bathing, tourism or simply for aesthetic enjoyment. For species, the main evaluation criterion is “sympathy”. Animals (especially mammals) should be protected mainly because they appear cute and friendly [192]: this has been called the “Walt Disney effect” [38]. Eating dolphin meat is a crime, eating lobster meat is just a gourmet choice.

It is not always clear that protecting species and protecting habitats are the two sides of the same coin. An example that illustrates this difficulty is the case of the date mussel (Lithophaga lithophaga), a seafood appreciated since the times of the ancient Romans and still highly sought after in the finest cuisines. It is a bivalve mollusc that lives inside limestone rocks. Its collection causes the removal of part of the substrate and, consequently, of all the marine life that thrives on it, thus leading to the desertification of large rocky areas of the infralittoral zone [193], and references therein. For this reason, the collection of date mussels is forbidden by law in many Mediterranean countries. However, being the species abundant and not particularly deserving of sympathy, people do not understand why the law protects the date mussel: the damage caused to the environment by its collection is not seen except by divers; and, after all, water quality does not seem to be compromised for bathing and tourism purposes. Only recently a gradual shift from a species-centred to an ecosystem-based management has been emerging in biodiversity conservation [194].

Most of the main marine habitats of the Mediterranean are currently in danger but national laws or European Community directives in practice mostly identify seagrass beds and, less so, rocky reefs, coralligenous reefs, and sea caves as deserving protection [195]. It seems therefore logical to consider that the surveillance activities, on a seasonal or annual basis, should primarily target these habitats, monitoring their extent and state of health.

The assessment of the health state of marine habitats typically requires numerical targets and specific reference values, to allow comparison in space and/or time [196]. In the last decades, a vast array of biotic indices has been developed to this purpose, mostly as a consequence of European Directives [197]. Indices have been devised based on indicators at different ecological complexity levels [198,199]: indices working at individual level take into account the phenology of a key species (e.g., a seagrass); indices at population level use abundance, spatial extent, density or size distribution frequency of a key species; indices at community level consider taxonomic composition, diversity, and the sensibility of different species towards environmental quality; indices at ecosystem level are based on the identification of functional compartments (e.g., in the food web) and on the evaluation of the status of each of them; indices at seascape level typify and quantify different elements and their spatial configuration, paying special attention to the morpho-structural traits of the species. Among the most utilized indices are CARLIT (Cartography of Littoral and upper-sublittoral benthic communities), for shallow water algal-dominated reefs [200], PREI [Posidonia Rapid Easy Index], for Posidonia oceanica meadows [201], ESCA (Ecological Status of Coralligenous Assemblages), for coralligenous reefs [202]. Many of these indices are multimetric, combining and integrating several individual indices [203]. Integrated indices are more appealing to environmental managers and administrators, who see in them a clear and synthetic indication of the health state of the habitat in question; however, multimetric indices homogenize the different components and may hide the specific nature of alteration [199,204]. Averaging low-values and high-values of distinct metrics may result in a “mediocre” synthetic value [85], which is not informative about the real ecological status of the habitat. The case of the MPA of Portofino (Ligurian Sea), analysed in 1990–1993 (before the MPA establishment) and in 2008–2014 (after the MPA establishment), illustrates the point: the ecosystem-based multimetric index reef-EBQI [205] rated as moderate the environmental quality of the rocky reefs in both periods. However, a dramatic decrease of algae has occurred, counterbalanced by an increase in fish abundance (Figure 7), which highlights the necessity for managers not to take into account just the final score: the scores of the individual components of the index must always be checked in order to set thresholds and select the required management actions [206]. Comparing the time-evolution of different biotic indices can provide relevant information on ecosystem change [207].

While regular surveillance activities should privilege the above mentioned habitats (seagrass beds, rocky reefs, coralligenous reefs, sea caves), the inventory activities, using diachronic cartography at multi-year periodicity, should take into account all the habitats contained within the MPA, including the sandy, muddy and detrital bottoms [208]. Several biotic indices exist also for soft bottom communities [209], and references therein.

5. Final Remarks

Change has always been the rule in marine biodiversity [54]. The Mediterranean marine biota has changed dramatically over the past, and is continually changing under the influence of both local and global pressures [10,210].

Biodiversity is probably the tool that ecosystems adopt to deal with environmental fluctuations (insurance hypothesis): through the distribution of resources and the alternation in the contribution to biomass, a flexible composition in species can allow ecosystems to maintain their functioning [211]. A high biodiversity buffers the effects of environmental variation since tolerant species can more easily be present. It seems a paradox, but in ecology change promotes stability [212].

Distinguishing environmental stress due to climatic changes from that due to local anthropogenic pressure is often difficult [213,214,215]. For instance, the loss of canopy forming macroalgae of the order Fucales, observed in many regions of the Mediterranean Sea, has been considered by different authors as due to either climate or human impact [149]. A network of MPAs can represent the reference system for understanding the influence of humans and for developing guidelines for an integrated management of the coastal zone for the purpose of sustainable development. MPAs must be seen as elective sites where natural changes can play their role independently from the interaction with local anthropogenic impacts, which should not represent a major driver of change there [38,164]. Assessing change over time requires long term data series, which – notwithstanding their importance for both scientific understanding and conservation planning [216,217] – are rarely available [54,218]. In absence of such data series, the revisitation of sites already surveyed in the past has proved successful [16,46,153,164,219,220,221,222,223,224,225].

A new marine ecological research policy is needed to address biodiversity problems, as they are becoming increasingly urgent. The MPAs can play a primary role in this field [226,227].

In the first place, a better understanding of the meaning and expressions of biodiversity requires continuous research in those scientific areas now considered out of date by the funding bodies, such as systematics, biogeography and natural history. Specialists in these disciplines who retire are not being replaced by young scholars: therefore, as biodiversity problems are growing, biodiversity skills are being lost [228].

Secondly, to assess the natural variability of marine ecosystems, and to understand the effects of change on their biodiversity, it is essential to start monitoring biodiversity at the scale of the entire Mediterranean. Neither species nor ecosystems recognize borders between nations, and neither climate nor human impacts do. An internationally coordinated network of MPAs in the Mediterranean would be indispensable for long-term marine biodiversity monitoring projects. These projects must be of such a duration as to include at least the life span of the dominant organisms and the time scale of the most important influencing factors, but funding and other constraints force ecologists into projects lasting 2–3 years at the most: few natural patterns have such a short duration, major changes in the biota occurring with cycles lasting 10 years or even longer [229]. Small-scale, short-term approaches undermine the possibility to assess change in marine ecosystems, whether natural or human-induced. Only continued monitoring will help understanding the consequences of the ongoing transformations driven by sea water warming and other components of global change [46]. Long-term monitoring efforts are a multi-generational deal and require commitments by institutions that persist beyond the working lives of individuals [230]. Marine Protected Areas are the best placed institutions to accomplish this task in the years to come.

Author Contributions

Conceptualization, C.N.B. and C.M.; methodology, A.A., C.N.B., S.C., M.M., C.M., A.O., A.P. and S.S.; software, A.A. and A.O.; validation, M.M.; formal analysis, C.N.B.; investigation, A.A., C.N.B., S.C., M.M., C.M., A.O., A.P. and S.S.; resources, A.A., C.N.B., S.C., M.M., C.M., A.O., A.P. and S.S.; data curation, A.A., M.M. and A.O.; writing—original draft preparation, C.N.B., M.M., C.M. and A.O.; writing—review and editing, A.A., C.N.B., S.C., M.M., C.M., A.O., A.P. and S.S.; visualization, C.N.B. and C.M.; supervision, M.M.; project administration, C.M.; funding acquisition, C.N.B. and C.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Acknowledgments

This viewpoint paper derives from concepts developed, and from experiences made, in many years of work in different contexts on the issues of marine protection. The authors thank all the colleagues who shared with them field work and profitable moments of discussion. Thanks are also due to three anonymous reviewers, whose suggestions improved this viewpoint, whereas Giuseppe Manzella (La Spezia, Italy) provided advice on the distinction between monitoring and surveillance. C.N.B. and C.M. wish to dedicate this paper to their unforgettable masters Enrico Tortonese (1911–1987), Jean Marie Pérès (1915–1998), Ramón Margalef (1919–2004), Cesare Sacchi (1926–2016), Alan J. Southward (1928–2007), Paolo Colantoni (1934–2015), and Eugenio Fresi (1943–2010).

Conflicts of Interest

The authors declare no conflict of interest.

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Figure 1. Applications of species-effort relationships: (a) an example of plot of the reciprocals of cumulative species number (1/S) against the reciprocals of sample number (1/A) to allow computing the theoretical maximum number of species as the reciprocal of the intercept: in this case, 1/0.008 = 125 (from [80], redrawn and modified); (b) species–dives curves (with shadowed area representing the 95% confidence intervals) to compare the cumulative number of species S observed in three different years (1991, 2009 and 2016) with a different number of dives D (from [81], redrawn and modified).

Figure 2. Maps of a Modiolus modiolus reef in the Irish Sea obtained by three different acoustic methods. (a) single-beam echosounder (RoxanneTM); (b) multibeam echosounder; (c) side-scan sonar (original drawings based on imagery in [95]).

Figure 3. Suitability modelling to locate a species of conservation interest in a marine protected area: (a) the slipper lobster Scyllarides latus; (b) its preferred depth according to literature information; (c) habitat suitability model superimposed to the seafloor map (obtained by merging aerial photography and multibeam survey) of Mesco Point, in the Cinque Terre MPA (NW Italy, Ligurian Sea), together with sea truth results by scuba diving (based on information in [137]).

Figure 4. Change of Posidonia oceanica cover in the Marine Protected Area of Bergeggi (Ligurian Sea, NW Italy) between 1987 and 2018 (based on information in [116,126,145]). Data are classified according to their reliability (see text).

Figure 5. Examples of non-destructive techniques for biodiversity monitoring: (a) underwater photography; (b) quadrat; (c) transect; (d) quadrats and transects can be complementary, rather than alternative, techniques.

Figure 6. Ordination model of marine benthic communities from Tyrrhenian Sea sedimentary bottoms: (a) 147 invertebrate taxa; (b) 76 mollusc species; (c) 50 conspicuous (>3 mm) and easily identifiable mollusc species. Molluscs are “efficient descriptors”, as the loss of information with respect to the whole community is negligible. Dots represent sampling stations, clustered according to sediment grain size and depth: mud at 20–75 m (green); muddy sand at 10–20 m (brown); sand at 5–10 m (red); fine sand at 3–4 m (yellow). Redrawn and modified from [190].

Figure 7. Ecosystem-based ecological assessment of the rocky reefs of Portofino, in the Ligurian Sea, before (a) and after (b) the institution of the MPA. The spider-web graphics represent the ecological status(semi-quantitative scale from 0 = bad to 4 = high) of each compartment of the ecosystem. EBQI = Ecosystem-Based Quality Index. Redrawn and modified from [205].

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