1. Introduction
The semi-enclosed Mediterranean Sea combines densely settled human communities, vast marine biological diversity and productivity, and progressive environmental change, making it an interesting place to study the complex linkages between human and marine ecological systems. Twenty-one countries of varying economic developmental status on three continents, Africa, Asia, and Europe, surround a 26,000-km coastline with an estimated 465.5 million inhabitants (
Figure 1). The Mediterranean Sea covers only <0.8% of the world ocean’s surface and includes <0.3% of its volume, but it is home to an unusual amount of biodiversity for a temperate sea [
1]. About 17,000 species live there,
i.e., 4%–18% of the world’s recorded species [
2]. Environmental threats from human activities are manifold, including those from intensive fishing, eutrophication, untreated sewage, heavy shipping traffic, marine litter, and introduction of alien species [
2]. The increase in coastal population and the large number of tourists to the region, attracted by its many cultures and pleasant climate, place additional pressures on the ecosystem [
1]. Layered atop these very localized pressures are progressive global-scale changes that also affect the entire Mediterranean Sea, such as ocean warming and ocean acidification.
Ocean acidification is the long-term change in ocean chemistry caused by increasing atmospheric CO
2 from combustion of fossil fuels, deforestation, and cement production. The global ocean currently absorbs about one-fourth of the anthropogenic CO
2 that is emitted to the atmosphere [
3], which, when combined with water, produces carbonic acid and thereby releases hydrogen ions. Some of the hydrogen ions produced are consumed by reacting with naturally abundant carbonate ions. Thus, ocean acidification increases hydrogen ion concentration [H
+], sometimes called acidity, and decreases pH (defined as −log[H
+]) and carbonate ion concentration. The decrease in carbonate ion concentration leads to a decrease in the saturation state of calcium carbonate minerals (Ω) like aragonite and calcite; saturation states are common metrics used to track ocean acidification. Ocean acidification is irreversible on the scale of at least hundreds of years [
4].
Ocean acidification is expected to adversely affect many marine organisms, including some commercially important species, either directly or indirectly. Ocean acidification may affect marine species directly by altering organism physiology. Ocean acidification may also operate indirectly by disrupting food webs or altering physical habitats, which in turn may affect other harvested species [
5]. The impact of ocean acidification on marine species is known to be highly species-specific (e.g., [
6,
7]), yet meta-analyses and reviews have indicated a general tendency of bivalve shellfish and other calcifiers to demonstrate reduced calcification and survival [
4,
8,
9]. This has been hypothesized to be a result of energetic shortages within organisms, which need to spend more energy building and maintaining hard structures in an acidifying ocean. A handful of studies on unrelated finfish species have identified different behavioral changes related to ocean acidification, such as increased boldness [
10,
11] or anxiety in Rockfish via alteration of GABA
A receptor functioning [
12], whose population-scale effects are not yet known. Whether or not behavioral changes from ocean acidification will be observed across many other finfish species is also not yet known [
13]. In addition, how individual organisms’ responses to ocean acidification that have been documented in laboratory studies scale up to cause population-scale responses is yet largely unknown.
Figure 1.
Map of the Mediterranean Sea (Nordwest, using World Data Base II data) [
14]. Developed countries (red circles): France, Greece, Israel, Italy, Malta, Monaco, Slovenia, and Spain. Other countries (blue circles): Albania, Algeria, Bosnia-Herzegovina, Croatia, Cyprus, Egypt, Lebanon, Libya, Montenegro, Morocco, Palestine, Tunisia, and Turkey.
Figure 1.
Map of the Mediterranean Sea (Nordwest, using World Data Base II data) [
14]. Developed countries (red circles): France, Greece, Israel, Italy, Malta, Monaco, Slovenia, and Spain. Other countries (blue circles): Albania, Algeria, Bosnia-Herzegovina, Croatia, Cyprus, Egypt, Lebanon, Libya, Montenegro, Morocco, Palestine, Tunisia, and Turkey.
Human communities around the Mediterranean Sea seem very likely to experience changes in marine harvests driven by ocean acidification, given their heavy dependence on marine resources and the certainty that ocean acidification will affect this sea and its species. To assess the total possible risk that Mediterranean communities face from ocean acidification, we must evaluate the intersection of the hazard (
i.e., ocean acidification), exposure of valuable assets to ocean acidification, and the communities’ vulnerability or adaptive capacity within the social system [
15,
16]. At present, few studies have reported ocean acidification responses of the most nutritionally or economically important species harvested in the Mediterranean [
17]. In addition, the level of dependence of Mediterranean coastal communities on marine harvests is not extremely well known; data at the national level are more easily accessible, which likely obscures some of the local importance of marine harvests. Nevertheless, we can use existing marine harvest data and our present knowledge about ocean acidification responses to assess the exposure of Mediterranean nations to ocean acidification. This paper reviews our knowledge around ocean acidification’s possible socioeconomic impacts in the Mediterranean within a risk assessment perspective [
16], a method that highlights where more research is needed to completely assess the risk from ocean acidification in the Mediterranean. We begin by reviewing ocean acidification’s progression in the Mediterranean, the ocean acidification responses of Mediterranean species, and fisheries harvest data around the Mediterranean. We then estimate the exposure of Mediterranean nations to ocean acidification via fisheries harvests. We then conclude by discussing how the exposure of Mediterranean nations to ocean acidification might be exacerbated or mitigated by social or ecological factors in a full risk assessment.
2. Ocean Acidification’s Development in the Mediterranean
The Mediterranean Sea has higher alkalinity than the global ocean, which leads to an ocean acidification response that differs somewhat from that of other regions. Alkalinity refers to the acid neutralizing capacity of the water and should not be confused with alkaline (pH > 7). Alkalinity is higher because evaporation is greater than precipitation, and because rivers and the Black Sea provide high alkalinity water to the Sea. It has been proposed that this higher alkalinity causes the rate of acidification of the Mediterranean Sea’s surface waters to be larger than that of the global ocean, based on data-based estimates of anthropogenic carbon [
18,
19]. However, the other data-based methods used to estimate the anthropogenic component of dissolved inorganic carbon in the Mediterranean Sea suggest much smaller changes [
20]. Equilibrium calculations from Orr [
21] confirm the Mediterranean Sea’s greater capacity to take up more anthropogenic CO
2, as well as undergo a greater corresponding reduction in carbonate ion, compared to the global ocean. However, the same calculations demonstrate that the Mediterranean Sea’s average change in surface pH will not differ significantly from that typical of the global ocean.
The first estimates of anthropogenic changes in surface pH from high-resolution, regional models of the Mediterranean Sea confirm that at present the average change in surface pH (1800 to 2001) remains indistinguishable from those for typical surface waters of the global ocean, and have little spatial variability across the surface of that semi-enclosed sea [
20]. For future trends we must rely on equilibrium calculations because no high-resolution model projections have yet to be published. Thus, we used seacarb software [
22], with projected atmospheric CO
2 levels from the Institute Pierre Simon Laplace Coupled Model, version 4 (IPSL-CM4) forced by the Intergovernmental Panel on Climate Change (IPCC) business-as-usual A2 scenario and the more conservative B1 scenario [
22] over the 21st century. With that forcing, pH and related carbonate system variables were computed by assuming thermodynamic equilibrium between atmospheric CO
2 and the surface ocean at the Dyfamed time-series station in the northwestern Mediterranean Sea (total alkalinity of 2560 μeq·kg
−1, salinity of 38 on the practical salinity scale, and temperatures of 13 °C in winter and 26 °C in summer, [
23]) By the year 2100, surface-water pH is projected to decline by another 0.3 units under the A2 scenario, where atmospheric CO
2 reaches 836 ppm (
Figure 2). Under the B1 scenario, the projected change in pH is only about half as much because atmospheric CO
2 is projected to reach only 540 ppm. Under the A2 scenario, the saturation state with respect to aragonite (Ω
A) drops to as low as 1.6 in winter and 2.4 in summer, well below the threshold considered sustainable for tropical corals (e.g., [
24]). Extending the same calculations back over the industrial period (1800 to 2000) shows that the Mediterranean Sea’s pH has already declined by 0.1 units, consistent with model projections [
20]. Simultaneously, the Mediterranean’s Ω
A has declined by 0.7 units.
Figure 2.
Surface-water pH (a) and saturation state with respect to aragonite (b) during the 21st century projected for the business-as-usual IPCC scenario A2 (solid line) and the more conservative B1 scenario (dashed line) under typical conditions for summer (red) and winter (blue).
Figure 2.
Surface-water pH (a) and saturation state with respect to aragonite (b) during the 21st century projected for the business-as-usual IPCC scenario A2 (solid line) and the more conservative B1 scenario (dashed line) under typical conditions for summer (red) and winter (blue).
3. Known Ocean Acidification Responses of Mediterranean Species
Despite the large number of species harvested in the Mediterranean, the ocean acidification response of a relatively small number of species has been tested. Of the 94 harvested and cultured animal species that are of economic relevance in the Mediterranean (
Table A1, data from Food and Agriculture Organization (FAO) data on National Aquaculture Sector Overview [
25] and Cultured Aquatic Species list [
26]), only 19 species of crustaceans, 34 species of molluscs, and 36 species of fish have indeed been tested. In the Mediterranean, 24 species are used only in aquaculture, 68 represent wild catch (fisheries), and only two species of bivalves (the oyster
Ostrea edulis and the clam
Ruditapes decussatus) contribute to both. For this study, we have focused on the three most studied animal phyla in the field of ocean acidification: crustaceans, echinoderms, and molluscs (for general reviews, see [
27,
28,
29], respectively). A literature review of 304 articles, published 1 January, 2014, that reported ocean acidification responses for 157 different species (55 crustaceans, 42 echinoderms, and 60 molluscs) only offered limited information on some of the 54 species that are economically important in the Mediterranean Sea (19 crustaceans, one echinoderm, 34 molluscs;
Table A1). Information on the direct impact of ocean acidification is available for only 12 harvested species (68 articles) species and 19 harvested species (106 articles) if other species in the same genus are included (
Table 1).
Table 1.
Harvested species and the number of articles about this species or genus (A = aquaculture, WC = wild catch). Bold species names highlight those with more than three articles.
Table 1.
Harvested species and the number of articles about this species or genus (A = aquaculture, WC = wild catch). Bold species names highlight those with more than three articles.
Harvested Mediterranean species | Fishery type | # Articles on this species | # Articles on this genus | Other studied species of the same genus (# articles) |
---|
CRUSTACEANS | | | | |
Carcinus aestuarii | WC | 0 | 6 | C. maenas (6) |
Hommarus gammarus | WC | 3 | 1 | H. americanus (1) |
Nephrops norvegicus | WC | 2 | 0 | |
Palaemon serratus | WC | 1 | 2 | P. californicus (1), P. elegans (1) |
Penaeus indicus | A | 0 | 1 | P. plebejus (1) |
Penaeus vannamei | A | 0 | 1 | P. plebejus (1) |
ECHINODERMS | | | | |
Paracentrotus lividus | WC | 8 | 0 | |
MOLLUSCS | | | | |
Crassostrea gigas | A | 13 | 13 | C. hongkongensis (1), C. virginica (12) |
Haliotis tuberculata | WC | 0 | 6 | H. coccoradiata (2), H. discus (2), H. Kamtschatkana (1), H. rufescens (1) |
Loligo vulgaris | WC | 1 | 0 | |
Mytilus edulis | A | 14 | 14 | M. californianus (2), M. chilensis (2), M. galloprovincialis (9), M. trossulus (1) |
Mytilus galloprovincialis | A | 9 | 19 | M. californianus (2), M. chilensis (2), M. edulis (14), M. trossulus (1) |
Ostrea edulis | A, WC | 3 | 0 | |
Patella caerula | WC | 0 | 1 | P. vulgata (1) |
Pecten jacobaeus | WC | 0 | 3 | P. maximus (3) |
Ruditapes decussatus | A, WC | 3 | 1 | R. philippinarum (1) |
Ruditapes philippinarum | A | 1 | 3 | R. decussatus (3) |
Sepia elegans | WC | 0 | 10 | S. officinalis (10) |
Sepia officinalis | WC | 10 | 0 | |
Among those, only five species had available published information in more than 3 articles: 2 species of
Mytilus mussels, the oyster
Crassostrea gigas, the squid
Sepia officinalis and the sea urchin
Paracentrotus lividus. Negative effects, including delayed growth, increased mortality, and altered physiology, are documented for all these species. However, most of the experiments used for this evaluation are based on short-term perturbation experiments. These fail to address some key modulating factors such as acclimation and evolutionary adaptation [
30], ecological interactions, or interaction with other drivers [
5]. Hence, it is then likely that laboratory based experiments will both under- and over-estimate the real impact of ocean acidification. Because responses vary greatly among species, we do not make generalizations or employ meta-analyses that are not representative of individual species responses [
31,
32]. The challenge, then, for evaluating the impacts of ocean acidification on marine resources is to deduce population- and ecosystem-scale responses of organisms that exhibit negative responses to ocean acidification.
Volcanic carbon dioxide vents in the Mediterranean have shown ecological responses to long-term moderate increases in CO
2 levels that retain natural pH variability [
33,
34]. They are also useful for examining response thresholds and determining which organisms are the most resistant to chronic exposures to elevated CO
2 levels [
35]. Communities of organisms exposed to decades of high CO
2 levels provide insights into what to expect in areas that are expected to receive higher-than-average levels of CO
2. There are shortcomings, however, in using volcanic systems as models to indicate how ecosystems will respond to ocean acidification. Although CO
2 vent systems are much larger and longer lasting than the mesocosm and aquarium experiments that have taken place to date, they still only affect relatively small areas of the seabed. Being open systems, their ecology is affected by surrounding areas that have lower CO
2 levels, allowing recruitment and migration of organisms from unaffected habitats [
36,
37]. Moreover, volcanic vent sites can have highly variable CO
2 levels, with steep gradients in pH and carbonate saturation, so caution is required in using information derived from vent studies in projecting future high-CO
2 scenarios [
38]. Thus CO
2 vent systems cannot mimic the effects of global acidification, but they augment predictions based on laboratory and modeling experiments since they show long-term responses of coastal systems to increases in CO
2 levels at a variety of locations worldwide [
39].
Only limited information on commercial species is available from the vent studies. For example, none of the fish [
33] and only nine invertebrates species listed as commercially important in
Table A1 have been studied at Mediterranean CO
2 seeps. The cnidarian
Anemonia sulcata thrives at high CO
2, and the extra inorganic carbon boosts the photosynthetic productivity of their zooxanthellae [
40]. The sea urchin
Paracentrotus lividus is less resilient to elevated CO
2 than other common shallow-water sea urchins, such as
Arbacia lixula [
41]. Many commercially important molluscs (
Arca noae,
Astraea rugosa,
Hexaplex trunculus,
Mytilus galloprovincialis,
Octopus vulgaris,
Ostrea sp.,
Patella caerulea) disappear from marine communities as CO
2 levels rise along natural gradients off Ischia [
33]. Transplantations of adult
Mytilus galloprovincialis at CO
2 vents show that their periostraca can confer short-term resilience to ocean acidification when exposed to corrosive waters, but that the oligotrophic conditions of the Mediterranean may rob the mussels of sufficient energy to cope with acidification. Conversely, transplantations of the commercially important gastropod
Patella caerulea showed that they were able to adapt physiologically to acidification, but the shells lacked periostraca and were weakened by the corrosive waters [
42].
In both laboratory and field studies, results indicate that numerous commercially important Mediterranean species will respond negatively to ocean acidification. Published studies have focused more heavily on crustaceans, echinoderms, and molluscs, which are more heavily studied phyla also in general (see [
27,
29,
43] respectively, for general reviews). However, insufficient data exist at this time to go beyond simply identifying which commercially important species or genera in the Mediterranean also exhibit negative ocean acidification responses. Studies designed to uncover the mechanisms governing ocean acidification responses may be of great help to close the knowledge gap between harvested Mediterranean species and those at risk from ocean acidification.
5. Discussion
This review has uncovered significant data gaps in both social and ecological knowledge that make it challenging to assess the risks that Mediterranean nations face from ocean acidification. However, we can use the data that is available to make a preliminary assessment of the relative exposure of Mediterranean nations to this threat. By exploring the characteristics of acidification, species harvested, fishery makeup, and economic benefits from Mediterranean fishing, we can identify trends and gaps that can direct future research efforts.
Given that the entire Mediterranean is likely to undergo relatively uniform acidification from the absorption of atmospheric carbon dioxide, local processes, such as nutrient overloading and hydrological and groundwater changes [
67], will likely cause the majority of regional variation in the Mediterranean’s acidification signal. From an oceanographic perspective, the exposure of Mediterranean fisheries assets to ocean acidification that is caused only by atmospheric CO
2 (sometimes called “anthropogenic ocean acidification” [
16]) appears fairly uniform at this time; however, the development of basin-scale physical-biogeochemical models may add more detail to this conclusion.
When we consider the ocean acidification response of economically relevant Mediterranean species, we are faced with another set of gaps. Knowledge is growing rapidly about the response of organisms to ocean acidification, but our understanding of the responses of economically relevant species lags far behind. Generally, bivalve shellfish fare worse [
8] under ocean acidification than other taxa, suggesting that if this trend also holds for most Mediterranean harvested species, artisanal and recreational fishers who target these groups may be more exposed to ocean acidification’s effects. Furthermore, different exposure arises among countries depending on the blend of species harvested. For example, the two largest Mediterranean fishery producers, including both wild catch and aquaculture, are Turkey and Italy. Both nations’ production is primarily based on herrings, sardines, anchovies, while Italian fishers also target mussels, clams, cockles, and ark shells.
The lack of disaggregated catch data (volume and value) by boat size or gear type makes it difficult to examine specifically how ocean acidification may impact these different fishing sectors. Generally, industrial fishers are more insulated from shifts in natural resources that may follow from environmental changes than artisanal fishers are. This is partly due to the industrial fleets’ greater ability to increase fishing effort to pursue elusive harvests and partly to their ability to divest from failing fisheries caused by environmental change. Of course, employees of industrial fleets may not have such clear-cut alternatives if the fishery declines, but they may be more able to find work elsewhere (either within a fishery industry or outside of it) compared to artisanal fishers given their lower economic exposure within the fishery. Compared to industrial fleets, artisanal fishers such as those profiled in Turkey have minimal technology available to help them increase fishing efforts. As owner-operators, their capital is heavily invested in region- or species-specific gear, decreasing their ability to adapt to changing environmental conditions. They do tend to harvest a range of species, somewhat insulating them from biogeographic shifts of one target species that follow from environmental change, but if overall ecosystem productivity and species diversity decline from ocean acidification, their harvests could decline as well. Although the economic revenues from artisanal fishing may not be significant, this sector is most exposed from possible impacts of ocean acidification given the small economic margins available from fishing and the significant capital costs associated with any change, not to mention the possible barriers in place regionally from lack of other employment alternatives. As the fishing fleets in non-developed nations, particularly around the southern Mediterranean, are largely artisanal and growing rapidly, yet in need of modernization, they seem to be most exposed from ocean acidification.
Aquaculture operations that raise shellfish may in fact be less exposed than artisanal or recreational fishers who gather shellfish from the wild. Shellfish hatcheries tend to be larger-scale, having more in common with industrial fishery fleets, and can proactively work to avoid harm to production by installing monitoring equipment, as has happened in some United States oyster hatcheries [
68]. Recreational fishers tend to be relatively less exposed than either group since they do not seek to subsist only on the proceeds of their labor the way artisanal fishers or small business owners of aquaculture operations often do.
Nations with large employment ratios of processors to fishers may be relatively more exposed to ocean acidification as well. When larger numbers of coastal residents depend on work and income generated by a single marine resource, the consequences to the human community if the resource declined would be much larger than in communities where diverse employment opportunities exist [
15].
Another factor that increases exposure of individual Mediterranean nations to ocean acidification is consumption of seafood [
69]. Without having dietary data divided up by taxon, without more information on the relationship between artisanal fishing and dietary dependence, and without conclusive information about the responses of harvested species, we can only estimate exposure by assuming that nations with higher seafood consumption are more exposed to ocean acidification. Developing nations presumably have lower access to high quality protein, and may more depend nutritionally on seafood [
69]. A positive outcome of the trade barriers mentioned above may be that these nations’ seafood supply goes to domestic markets (as in the case of Egypt) and offer this nutritional benefit locally, rather than satisfying appetites abroad, which can pay a higher price for the luxury. On the whole, the Mediterranean countries consume more seafood than they produce, so they are likely to be more exposed to ocean acidification than if income from fishing were the only benefit.
Future work to explore the impact of ocean acidification on Mediterranean nations could involve computable general equilibrium models (CGE models) for multi-sectors and multi-countries [
70]. These models require a system of equations to assess the added impact of ocean acidification on linkages across sectors. This would be possible if a good-fitting CGE model existed to which environmental impacts could be added to assess the marginal impact and trickle-down effect of ocean acidification over sectors. From another dimension, it would be ideal to be able to assess the impact of ocean acidification on any chosen economic output variable (such as employment in fisheries, trade, protein intake of households,
etc.) in the region and in a country by conducting data-based sensitivity analysis. Given that most relationships in nature are non-linear, we suggest usage of nonlinear sensitivity models, which suggest that there is not a direct, linear and constant relationship between ocean acidification (input) and economic output variables. Assuming nonlinear sensitivity calls for potentially measuring it with a variance-based sensitivity analysis within a probability frame, where one can decompose the variance of the system output (a chosen economic variable such as the examples above) into percentages caused by several input variables, which include ocean acidification. As an example, if one had data on ocean acidification, agricultural runoff (pollution,
etc.) as input variables in a region, one could measure the sensitivity of the output variable (such as employment in fisheries) to ocean acidification. If, in this hypothetical case, 80% of the protein intake variance was caused by variance in agricultural runoff, 22% by variance in ocean acidification and 8% by interactions between ocean acidification and pollution, these percentages would be measures of sensitivity across the whole input set, because they are nonlinear responses with interactions in non-additive systems and models. Completing estimates of this sort will require coordinated efforts in data collection of same variables across countries and across time.
6. Conclusions
Richer, developed countries can more easily adapt to risks than poorer, non-developed countries [
69,
71]. In the Mediterranean, non-developed countries have been increasing both wild and aquaculture fishery production dramatically, which provides both needed income but also exposes them more to ocean acidification due to their rapid industrialization. These fishermen generally lack advanced technology and include many owner-operators, which enhances their exposure even more. Trade barriers hinder the export of fresh products from developing nations, which encourages domestic consumption. Although this provides households with high quality food, it also increases dependence of people in developing nations on marine resources. Taken together, the factors reviewed in this paper suggest that non-developed Mediterranean nations that are greatly increasing their fishery production via both wild and aquaculture investments, that have a large ratio of processors/distributors to fishermen, bivalve shellfish as a strong part of their aquaculture industry, and large numbers of artisanal fishers and harvesters, are the most exposed to risks resulting from ocean acidification. Nations along the southern Mediterranean tend to fit more of these characteristics than others.
This study must be considered only a first step at assessing elements of the risk that Mediterranean nations face from ocean acidification. A more formal risk assessment [
16] would require the collection of much more data to evaluate the development of ocean acidification in the Mediterranean, at a more detailed level than the equilibrium calculations we have done to assess the ocean acidification response of fishery-targeted species in the region, to gather more detailed harvest data at a species-resolving scale and to understand the interaction of export, domestic, subsistence, and industrial markets in distributing marine harvests from the Mediterranean. It is extremely likely that the risk profile of each Mediterranean nation will differ from its neighbors, as a result of the different factors mentioned above and other external socioeconomic factors, such as the developed/non-developed status of nations’ economies and each nation’s social resilience. This study underscores the need for marine scientists, fisheries economists, and other social scientists to work together to improve our capacity to project future environmental and economic consequences from ocean acidification. To assess possible impacts on humans, it is also critical to lead more studies focused on the species and ecosystems having the most economic importance.