The Spatiotemporal Variability of Marine Plankton Ecosystem Services at the Regional Scale: A Combined Approach Using a Systematic Review and Network Analysis

Abstract

Marine plankton include organisms driving multiple ecosystem services (ESs). In this study, we identified ESs provided by planktonic consortia worldwide from the analysis of scientific literature. We also mapped the identified ESs onto forty-nine plankton trophic networks derived from presence–absence data obtained from two coastal surveys in three areas along the coast of the Campania region in the Tyrrhenian Sea (NW Mediterranean). The systematic review evidenced that ESs associated with goods provision and ecosystem regulation were the most studied categories, while cultural ESs were the least considered. The mapping of ESs across the Campania coast revealed significant spatiotemporal variations in plankton-based ESs, which depend on seasonal variability and local environmental conditions. Among the ESs, those connected with the regulation and maintenance of marine ecosystems dominated both temporally and spatially, highlighting the crucial role of plankton in ecosystem stability and resilience. Moreover, although the direct provision of goods and materials was less represented, food provision to higher trophic levels was widespread within each coastal sector, highlighting the crucial role of plankton biodiversity in directly sustaining the whole marine ecosystem and related economic activities such as fisheries and aquacultures.

1. Introduction

Marine ecosystems and their biodiversity provide multiple ecosystem services (ESs), including carbon storage, primary production, the provision of food and materials, and recreational opportunities [1,2]. Based on the Common International Classification of Ecosystem Services (CICES), ESs fall into three main categories: (i) regulating and maintenance, which includes ESs that ensure optimal environmental conditions for ecosystems (e.g., water quality and climate regulation); (ii) provisioning, which mainly includes ESs related to the direct provision of goods such as food and materials; and (iii) cultural, which includes non-tangible, immaterial benefits like recreational and educational activities [3].

ESs represent a vital connection between natural ecosystems and their social and economic benefits to humans [4,5]. In this latter respect, coastal marine ecosystems host rich biodiversity and provide ESs for human populations, given their proximity to where most people live [4]. As a result, coastal waters play a pivotal role in supporting key economic activities, including fisheries, aquaculture, and tourism [6,7]. Even though identifying the ESs provided by all components of a marine community is essential for offering decision-makers and stakeholders the necessary information for accurate marine ecosystem management [4,8], the ecosystem service assessment of coastal waters must be improved [8]. As the services of a specific ecosystem or region are generally linked to local biodiversity [9,10,11,12,13], the spatiotemporal variability of the effects of biodiversity on ESs should be primarily investigated within marine environments (e.g., [11,14,15]).

Plankton are pivotal life forms within marine ecosystems and include highly dynamic and strongly interacting organisms spanning from unicellular to metazoan organisms [16,17,18]. The former include groups like heterotrophic bacteria (prokaryotes), phytoplankton (cyanobacteria plus strictly autotrophic protists), and protozooplankton (mainly heterotrophic protists, also including ‘mixotrophic’ organisms capable of performing both predation and photosynthesis) [19]. Moreover, planktonic metazoans (zooplankton) include all invertebrate phyla, which are numerically dominated by the crustacean copepods, together with gelatinous organisms like jellyfish (i.e., Cnidaria, including colonial forms such as siphonophores and Ctenophora) as well as the very diverse larvae of benthic and nektonic species [18,20]. Plankton communities show high spatiotemporal variability [21,22,23], which is particularly pronounced in coastal marine ecosystems [23,24] characterized by steep bathymetric gradients, freshwater inputs, and human activities [23,24,25].

Plankton provide multiple ESs, such as nutrient and organic matter storage and cycling [26,27]. Phytoplankton are responsible for about half of the world’s net primary production and offer a range of nutraceutical and biochemical resources [27,28]. Zooplankton feed larger animals, from commercially exploitable planktonic crustaceans, mollusks, and fishes to iconic mammals like whales [29,30]. Despite their importance, the role of plankton in providing ESs is underexplored, with assessments focusing only on broad groups such as phytoplankton or zooplankton rather than on the entire planktonic diversity (e.g., [30,31,32,33]). In this context, Naselli-Flores and Padisák (2022) [31] compiled an exhaustive review about the ESs provided by marine and freshwater phytoplankton, while B-Béres et al. (2022) [33] reviewed all the ESs associated with freshwater and marine diatoms. Botterell et al. (2023) analyzed all the ESs provided by zooplanktonic organisms such as copepods, krill, and jellyfish [32], while Lomartire et al. (2021) focused on the analysis of the role of zooplankton in providing food for higher trophic levels such as fish [30].

This study aims to explore the literature on marine plankton-related ecosystem services, identifying those provided by different plankton groups—i.e., consortia of species behaving similarly from the ecological point of view—at the global scale. Additionally, this study maps the ESs identified by a literature search against 49 plankton trophic networks that include taxa belonging to the above-mentioned groups and stemming from data collected during 2 biodiversity surveys along the coastal waters of the Campania region (Gulfs of Gaeta, Naples, and Salerno) in the Tyrrhenian Sea (Mediterranean Sea). This exercise allows us to explore the relationship between the spatiotemporal variability of plankton biodiversity and the ESs they provide.

2. Materials and Methods

2.1. Literature Search of Global Plankton Ecosystem Services

This systematic review followed the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) checklist [34] (Supplementary Materials S1 and S2). The search (Web of Science database, accessed on 20 February 2024) utilized a specific set of keywords within the titles, abstracts, and keywords of papers, listed in the following text:

(i)

plankton OR megaplankton OR macroplankton OR mesoplankton OR microplankton OR nanoplankton OR picoplankton OR microbial OR microbiome OR microbe* OR bacteria OR archaea OR holobiont OR prokaryote* OR cyanobacteria OR nanoflagellate* OR protist* OR protozoa* OR chlorophyt* OR diatom* OR bacillariophy* OR coccolithophor* OR prasinophyt* OR cryptophyt* OR haptophyt* OR phytoplankton OR microalgae OR euglenozoa OR alveolat* OR dinoflagellat* OR ciliat* OR ciliophora OR radiolaria OR rhizaria OR cercozoa OR mixoplankton OR mixotroph* OR protozooplankton OR zooplankton OR ichthyoplankton OR meroplankton OR “planktonic metazoa*” OR copepod* OR “planktonic crustacean*” OR calanoid* OR cyclopoid* OR jellyfish OR gelatinous OR medusae OR cnidaria* OR “planktonic tunicate*” OR salp* OR amphipod* OR chaetognath* OR cladocer* OR decapod* OR euphasiid* OR appendicularia* OR heteropod* OR ostracod* OR pteropod* OR rotifer* OR foraminifer* OR ctenophor* OR fungi OR basidiomycota OR ascomycota OR virus* OR viral (Topic)

(ii)

AND marine OR sea OR ocean OR coastal OR shelf OR estuary (Topic)

(iii)

AND “ecosystem services” (Topic).

The first group of keywords permitted the retrieval of the whole biodiversity within plankton, including taxa associated with prokaryotes, phytoplankton, protozooplankton, and zooplankton. The second group made it possible to associate the planktonic taxa within the context of marine ecosystems. For the latter, we used only the keyword “ecosystem services” to include only papers that strictly express the connection between plankton and the ESs they provide, following Liquete et al. (2013) [1].

A PRISMA flow diagram outlining the literature-filtering process appears in Figure 1. The initial search yielded 728 papers (Supplementary Table S1). Subsequently, this work screened the titles and abstracts of all the retrieved documents for their relevance to the research theme. Only those papers that evidenced the relationship between plankton and the provision of ESs participated in the subsequent analyses. This selection resulted in 27 papers analyzed to obtain a detailed description of the main ESs provided by plankton. As detailed information about ESs of specific plankton taxa was mainly unavailable in the literature, this work assigned ESs to major plankton groups (Supplementary Tables S2 and S3). The ESs provided by each plankton group identified from the literature review, based on the CICES classification [3], were visualized through an alluvial diagram using the alluvial package (https://github.com/mbojan/alluvial, accessed on 20 February 2024) in R version 4.3.2 [35].

2.2. Spatiotemporal Network Analysis of Plankton Ecosystem Services at a Regional Scale

This work mapped the ESs identified from the literature onto 49 conceptual and unweighted plankton trophic networks (see the following paragraphs for further details) derived from taxa presence–absence data collected at 49 sampling stations during two seasonal research surveys in the frame of the FEAMP-ISSPA project (https://feamp-isspa.it/, accessed on 20 February 2024) (Supplementary Table S4). These surveys took place in autumn 2020 (September–October) and summer 2021 (June–July) along the coastal waters of the Campania region (Tyrrhenian Sea, NW Mediterranean), namely, from north to south: the Gulf of Gaeta, the Gulf of Naples, and the Gulf of Salerno. The Campania region is highly affected by human pressures from the Naples metropolitan area (ca. 4 million inhabitants) and by two of the largest ports on the Mediterranean Sea, those of Naples and Salerno [36,37]. Campania is a relevant socio-ecological area, with numerous fishery consortia, aquaculture, and maritime activities [36] and a rich cultural heritage attracting millions of tourists yearly [38]. During the first survey, samplings occurred at 22 stations (9, 7, and 7, in the Gaeta, Naples, and Salerno Gulfs, respectively), and during the second survey, at 27 stations (9, 12, and 6, in the Gaeta, Naples, and Salerno Gulfs, respectively). The sampling strategy and taxonomic identification followed standardized protocols [39], which are available in Bellardini et al. (2024) [40].

The workflow of plankton trophic network construction included the following steps: (i) taxa identification on all 49 sampling stations at the finest possible taxonomic resolution; (ii) the building of a presence–absence matrix (Supplementary Table S4); (iii) the definition of network nodes based on the trophic habits of retrieved taxa according to information from the literature and specific online databases like Globi [41] (see Supplementary Table S5); (iv) the definition of network links (from prey to predators) based on trophic compatibility among co-occurring taxa.

Following the methodology of Keyes et al. (2021) [42], all the ESs identified by the literature search (see previous section) and associated with plankton groups took part in the planktonic trophic networks; this operation resulted in 49 meta-networks containing both planktonic and ecosystem service nodes (Supplementary Tables S6 and S7). These networks included two types of links: trophic interactions among network nodes and linkages between nodes and the ESs they provide (from plankton to ESs) (see Supplementary Tables S6 and S7). The linkages between the ESs and protozooplankton were analogous to those among ESs and phytoplankton due to the similarity of these categories in terms of phylogeny and dimensions [14,18,43], and since no specific literature information was available.

This work applied network analysis to the 49 plankton trophic networks mentioned above by calculating the redundancy and the trophic level (sensu [42]) for each ES (Supplementary Table S8), following Keyes et al. (2021) [42], to explore the relationships between plankton biodiversity and ESs. Redundancy for the ES nodes stemmed from the inDegree centrality [42], i.e., the total incoming links associated with the planktonic taxa providing a specific ES, calculated using the iGraph R package version 2.1.4 [44]. In this way, the InDegree of a node informed us about the number of planktonic taxa providing specific ESs. The trophic level of the ESs stemmed from the mean trophic level of ES providers (i.e., the nodes directly linked to ES nodes) [42], calculated using the NetIndicies R package version 1.4.4.1 [45]. The following step was to analyze, using the non-parametric pairwise Wilcoxon test in R [35], possible differences between the three gulfs and the sampling sites based on trophic level and the InDegree of the ES categories. Furthermore, the calculation of the sampling site-specific ratios (non-parametric pairwise Wilcoxon test in R [35]) for ‘unicellular vs. metazoan’ and ‘phytoplankton vs. protozooplankton’ nodes (Supplementary Table S9) made it possible to characterize the relationships between plankton biodiversity, the trophic levels they occupy, and the ESs they provide.

3. Results and Discussion

3.1. Plankton Ecosystem Services

From the twenty-seven selected papers [30,31,32,33,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69] (Supplementary Table S2), several ESs emerged belonging to all the three main ES categories (regulating and maintenance, provisioning, and cultural services, based on the CICES classification) and coming from five main plankton groups (planktonic bacteria, phytoplankton, planktonic crustaceans, jellyfish, and other zooplankton, the latter including other metazoans such as salps, chaetognaths, and appendicularians) (Figure 2). Overall, the review evidenced that provisioning and regulating and maintenance were the ecosystem services categories mainly associated with different plankton groups; the cultural category was weakly associated with plankton, with planktonic bacteria absent from it.

3.1.1. Regulating and Maintenance Ecosystem Services

Marine plankton provide numerous regulating and maintenance ESs, which play crucial roles in ocean biogeochemical cycles (Figure 2). Planktonic bacteria, i.e., the major consumers of dissolved organic carbon [70], are fundamental for carbon, nitrogen, phosphorus, and sulfur remineralization through decomposition processes [71,72]. Planktonic bacteria reintroduce organic matter into marine communities being preyed on by protozooplankton (i.e., the so-called microbial loop [73]), which in turn feed planktonic metazoans [70]. Phytoplankton perform a similar function, reintroducing organic matter and nutrients within marine communities and serving as prey for zooplankton [74,75,76]. Moreover, diazotrophic cyanobacteria can fix atmospheric nitrogen, making it available to other phytoplankton groups and secondary consumers as organic matter [31].

Among planktonic metazoans, copepods contribute to biogeochemical cycles within marine ecosystems (Figure 2) by transporting carbonic matter from the surface towards water column layers at higher depths as they produce fecal pellets and undertake diel vertical migration [26]. Planktonic crustaceans and other zooplanktonic taxa can also remineralize carbon by eating fecal pellets produced by metazoans [26]. Salps (herein within the other zooplankton group) feed on a wide range of prey, spanning from pico-plankton (<2 µm) to macro-plankton (up to 1 mm) [77], and produce fast-sinking fecal pellets [78]. The slow sinking of small-sized phytoplankton (e.g., cyanobacteria) facilitates their vertical transportation of carbon to the ocean interior [79,80,81].

Carbon cycling also occurs during the sinking of the dead bodies of planktonic crustaceans and other zooplanktonic taxa like salps, which are estimated to export high amounts of carbon to the ocean bottom [81,82]. Jellyfish, often seen as pests [46,83] and a cause of damage for marine ecosystems and economies (e.g., fisheries and aquaculture) [84], also contribute to biogeochemical cycles through feeding processes (excretion of fecal pellets) and the sinking of their carcasses [80,85,86]. Altogether, through the sinking of dead bodies and the production of fecal pellets, planktonic metazoans play a crucial role in sequestering carbon from the surface to the ocean depths (climate control, see Figure 2) [32].

Regulating and maintenance ESs exploit biotic interactions occurring in plankton communities. For instance, jellyfish help control invasive species populations through predation (biological control, Figure 2). In the North Sea, jellyfish helped reduce the population of the invasive ctenophore Mnemiopsis leidyi [87]. Solitary and colonial jellyfish provide protection and food to copepods and small fish, harboring them under their bells or between their tentacles [46,88]. On the other hand, diatoms (phytoplankton) provide surfaces for other unicellular organisms (e.g., planktonic bacteria and cyanobacteria) to grow, facilitating ecological processes [33]. Moreover, non-toxic phytoplankton can reduce the spread of toxic species through competition for resources [31,89].

Moreover, plankton play a role in indicating and regulating water conditions. Planktonic metazoans, such as copepods, respond rapidly to environmental changes [90,91,92] and are used as indicators of water quality (Figure 2) and to assess the effects of pollutants such as heavy metals, chemicals, and microplastics on marine ecosystems [93,94]. Some species of copepods are involved in the bioremediation of eutrophic waters by removing nitrogen and phosphorus in excess in coastal environments [95,96]. Planktonic bacteria and phytoplankton taxa, such as diatoms, are also known to degrade anthropogenic pollutants, heavy metals, and toxins, thus exerting water-quality control on marine ecosystems [51,97,98].

Primary production is a pivotal and well-recognized ecological process associated with plankton (Figure 2) [99]. Nearly half of the global net primary production comes from phytoplankton, despite these latter organisms accounting for only about 1% of global photosynthetic biomass [31,99,100]. Diatoms contribute the most to this production (20–40%) [101,102] and are responsible for about 40% of total oceanic carbon uptake [103]. The so-called carbon sequestration (falling into the climate control category, see Figure 2) performed by phytoplankton occurs as the oxygen produced during photosynthesis uses CO₂ as a carbon source [31,51]. Coccolithophores (phytoplankton) use this carbon to calcify their external structure, i.e., coccoliths made of calcium carbonate (CaCO₃). These structures can sink to the ocean interior and remove copious carbon from the atmosphere [31,104]. Collectively, the phytoplankton sequester about 20–35% of global annual CO₂ [31,105].

3.1.2. Provisioning Ecosystem Services

Among the ES categories, provisioning links directly with economic activities, including natural food and material supply [3]. As a foundational component of the marine food web, plankton sustain entire marine communities by serving as a primary food for higher trophic levels (Figure 2). Zooplankton play a crucial role by connecting their prey, i.e., planktonic bacteria, phytoplankton, protozooplankton, and zooplankton [106], to larger marine metazoans such as fish, sharks, and other top predators [30] (food for higher trophic levels). This ecological process translates into economic activities such as fisheries and aquaculture, where plankton feed the animals [30].

In aquaculture, phytoplankton are food for zooplankton, which become nutrition for fish [30,107] (food for higher trophic levels). The most used food sources for cultured zooplankton, the microalgal genera Nannochloropsis, Tetraselmis, Pavlova, and Isochrysis [30,108], are rich in polyunsaturated fatty acids and docosahexaenoic acid, which are necessary for growth, tissue development, and immunity function in the juvenile stages of fish, mammals, and birds [30,108,109]. Diatoms (phytoplankton) also contain high concentrations of essential nutrients, and they are used as food sources within aquaculture for vertebrates and invertebrates [33,110,111], as well as the larval stages of marine finfish species [33,112] (food for higher trophic levels).

Jellyfish are generally considered a low-quality food source due to their low specific calorific values compared to other marine species [113,114]. However, they contain high-quality proteins [114] and represent a food source for many organisms, such as leatherback turtles [113,115], several fish species (e.g., bluefin tuna and swordfish), sea birds, and penguins [113,116]. For these reasons, jellyfish are a common food source in aquaculture, where they are eaten by planktonic crustaceans and fish [117,118] (food for higher trophic levels). Jellyfish are also a direct source of food for humans (Figure 2), with dedicated fisheries distributed worldwide [119]. They are a popular food in Asia but not in Western countries, where policymakers still do not consider them a proper food for humans [32,46,120,121,122]. Indeed, China is the world’s major consumer of jellyfish [123], with these animals being part of the traditional diet for over 1700 years [124]. Their consumption in other Asian countries like Japan, Malaysia, and Singapore has significantly increased in the last century [123].

Plankters smaller than jellyfish are seldom directly consumed by humans. Asian regions base their cuisine on planktonic crustaceans as ingredients of many traditional umami dishes [125]. Planktonic crustaceans such as krill and some species of the genus Calanus provide oil supplements [32,126]. Concerning phytoplankton, the most eaten organism by humans belongs to the freshwater genus Arthrospira (also known as Spirulina) [67,127], which is a cyanobacterium that has been harvested to provide food for thousands of years [31,110] and has been traditionally used in western countries for nutritional purposes since the 1970s [67,128] (food for humans).

Phytoplankton are also widely used as food and nutritional supplements (biochemical products), with several microalgae being important sources of antioxidants, pigments, oils, and vitamins [67,129,130]. Spirulina, Chlorophyta Haematococcus spp., and Dunaliella spp. can accumulate high quantities of antioxidants like astaxanthin and β-carotene [67,131,132]. The genus Chlorella (Chlorophyta) has a high protein and carbohydrate content, and it is also rich in B vitamins [67,132]; the genus Nannochloropsis (Chlorophyta) is a source of eicosapentaenoic acid [67,131] (biochemical products). The chrysophytes Mallomonas and Paraphysomonas can produce bioactive compounds such as polyunsaturated fatty acids [133,134]. The chrysophyte Synura produces sterols like β-sitosterol and cholesterol, which are precursors for vitamin D [134,135] (biochemical products). Planktonic bacteria produce compounds such as exopolysaccharides and methanol [66]. Moreover, jellyfish are used in soil fertilizers (biochemical products) as they increase the nitrogen, phosphorus, and potassium contents of the soil [32,136].

Some phytoplankton genera (e.g., Arthrospira, Chlorella, Dunaliella, Haematococcus) and planktonic bacteria produce compounds beneficial to human health like antifungal, anti-viral, anti-inflammatory, and immune system stimulants [57,67] (human medicine). Several diatoms can produce high amounts of bioactive compounds such as polyphenols, carotenoids, and sulfated polysaccharides identified as immunostimulants (human medicine) [33,137]. Compounds extracted from diatoms are also reported to be effective against HIV and cancers [33,138]. Among the 30,000 microalgal species known, only a few are the objects of chemical composition studies, and even fewer participate in commercial cultivations [131,139]. This significant imbalance between the vast phytoplankton biodiversity in marine ecosystems and the limited number of microalgae used in biotechnology is due to the challenges associated with cultivation in artificial settings [131,139]. Moreover, as any novel species must follow the Novel Food regulations, the commercialization of new microalgae or their products is further impeded by administrative hurdles, which promote food safety but are perceived by stakeholders as costly and time-consuming processes [67].

Concerning metazoans, some jellyfish contain high levels of collagen, a compound used in the biomedical industry for tissue engineering and regenerative medicine, for instance, to cure osteoarthritis [32,140,141]. Jellyfish toxins are used as anticancer compounds [46,142,143] and antioxidant nutritional supplements [46,144] (human medicine).

Several phytoplankton genera (e.g., Botryococcus, Chlamydomonas, Chlorella, Dunaliella, Skeletonema) can also produce large amounts of hydrocarbons, which are used for biofuel production (Figure 2) [31,145]. Lastly, planktonic bacteria, phytoplankton, and planktonic metazoans are also fundamental genetic resources (Figure 2) [31,32,146]. For example, the Green Fluorescent Pigment, a luminescent marker extensively used in molecular experiments as a biological gene-expression marker, is isolated from jellyfish [32,46,147]. Diatoms are also used as genetic resources in genetic engineering studies [31].

3.1.3. Cultural Ecosystem Services

Cultural ESs encompass intangible benefits related to religious, artistic, educational, and recreational values [148]. Plankton have historically inspired myths, legends, and artistic expression, contributing to cultural heritage, educational values and recreation (Figure 2). Several planktonic microalgae color surface waters during blooms, giving rise to various myths and legends [31]. The first plague in Egypt, where fish died and people could not drink the water from the River Nile, was likely due to a harmful algal bloom [31,149]. The myth of the phoenix may have stemmed from blooms of bioluminescent dinoflagellates (e.g., belonging to the genera Alexandrium, Protoceratium, Noctiluca). When a bird takes off from coastal areas where these blooms occur, it appears to shine as its feathers are drenched with these bioluminescent dinoflagellates: the mechanics of flight trigger the luciferase–luciferin reaction, creating the impression of a glowing bird [31].

Plankton have also inspired science and art. Various species of planktonic microalgae have inspired bracelets, pendants, and earrings [31]. The German biologist Ernst Haeckel’s multivolume series Kunstformen der Natur [150] features intricate drawings of plankton, including unicellular organisms like diatoms and radiolaria, as well as metazoans like jellyfish, later inspiring mosaics, chandeliers, and windows in the Oceanographic Museum of Monaco, Montecarlo, and influencing Art Nouveau design and architecture [31,151,152]. Dinoflagellates were also represented in pioneering artworks [153] by scientist and artist Franz Schütt, who was one of the scientists who worked on the “Plankton expedition” of 1889 with Victor Hensen, i.e., the scientist that coined the term “plankton” [154]. Planktonic crustaceans like copepods are popular in many movies, TV shows, and cartoons [32].

Planktonic organisms are also attractions for tourists. Jellyfish, an iconic group with several species exhibited worldwide [46], generate economic income through recreation and educational values for the public [32,46] and provide recreational activities like scuba diving with the jellyfish Nemopilema nomurai in the Sea of Japan and with the jellyfish Mastigias in the Pacific Island nation of Palau, where over 30,000 visitors annually swim with them [32,46]. Blooms of bioluminescent species like the heterotrophic dinoflagellates Noctiluca scintillans and the ctenophore Mnemiopsis leidyi generate tourism and a sense of inspiration, education, and recreation in those observing these natural events [32].

3.2. Spatiotemporal Variability of Plankton Ecosystem Services

This study mapped the ESs provided by plankton, resulting from a systematic literature review, on 49 planktonic trophic networks referring to plankton samples collected across two seasons and within the three gulfs of Gaeta, Naples, and Salerno along the Campania coast. The applied meta-analysis revealed the spatiotemporal variability of the relationship between plankton biodiversity and the related ESs. Regulating and maintenance services were the ESs potentially provided by the largest number of planktonic taxa, showing the highest redundancy (highest values of InDegree) within all the gulfs and in both the seasonal sampling surveys; cultural and provisioning ESs showed similar InDegree values (Figure 3). This finding is further supported by the non-parametric pairwise Wilcoxon test, evidencing a general statistically significant (p-value < 0.05) difference between regulating and maintenance ESs and the cultural and provisioning ESs (Supplementary Figure S1).

Provisioning ESs showed the highest variability among sampling stations, suggesting a higher influence of plankton biodiversity on this ES category (Figure 3 and Supplementary Figure S1). This observation is explained by considering the specificity of the ESs included in the provisioning category (Supplementary Figure S2), like the biofuel and primary production ESs (Supplementary Figure S2), which are associated with organisms able to photosynthesize (i.e., phytoplankton and mixotrophic protists). Consequently, biodiversity is more likely to impact these ESs than more redundant ESs (i.e., those showing a higher InDegree). Among the latter ESs, food for higher trophic levels had one of the highest InDegree values, highlighting the crucial role of plankton in sustaining marine biodiversity and economic activities such as fisheries and aquacultures.

The ES InDegree analysis across the two seasonal sampling surveys revealed a general increase in potential plankton-associated ESs from autumn to summer (Figure 3 and Supplementary Figure S1). The planktonic ESs in the Gulf of Naples showed the highest InDegree in both seasons, followed by the Gulfs of Gaeta and Salerno (Figure 3). These results agree with the study by Bellardini et al. (2024) [40], reporting seasonal differences in environmental conditions across the gulfs and suggesting a significant influence by riverine inputs. Indeed, the Volturno River, one of the largest rivers in southern Italy, influences the Gulf of Gaeta, and the Sele River influences the Gulf of Salerno. The plume of the Volturno changes orientation based on the season, extending further offshore in winter and towards the coast in summer [40,155,156,157]. Similarly, the Sarno River influences the Gulf of Naples, characterized by seasonal water column stratification in the summer and mixing in the winter [40,157,158]. In contrast to salinity, temperature remained relatively uniform across the gulfs and seasons, with a significant difference only reported between autumn and summer temperatures in the Gulf of Salerno [40]. These conditions may have significantly affected the spatiotemporal variability of ESs across the study area and the seasons investigated.

3.3. Trophic Levels of Plankton Ecosystem Services

The different environmental conditions and plankton biodiversity characteristics of each gulf and season led to notable variations in the trophic levels of the ESs. Compared to the InDegree values, the analysis of ES trophic level revealed an even greater spatiotemporal variability, with a general statistically significant difference observed among the trophic levels of all the ES categories at each gulf and season (Supplementary Figure S1). Notably, ESs from all categories exhibited higher trophic levels during summer than autumn, indicating that these ESs depend on organisms with higher trophic levels during summer (Figure 4). Among the gulfs, the planktonic community in the Gulf of Salerno displayed the highest ES trophic levels in both seasonal surveys (Figure 4 and Supplementary Figure S1). The Gulf of Naples was, in both seasons, second in rank when looking at the ES trophic levels, with the Gulf of Gaeta showing the lowest values among the gulfs in each survey (Figure 4 and Supplementary Figure S1).

The analysis of the unicellular to metazoan and phytoplankton to protozooplankton diversity ratio explains the above-mentioned results (Figure 5). The unicellular vs. metazoan plankton ratio was consistently higher during summer (second survey), with a slight increase in the Gulf of Naples, a large but not significant increase in the Gulf of Gaeta, and a statistically significant increase in the Gulf of Salerno (Figure 5). This result agrees with chlorophyll a concentrations, which were higher in the summer than in autumn within each of the three gulfs [40]. The overall increase in unicellular organisms within each gulf stemmed from a significant rise in the number of species of protozooplankton over those belonging to phytoplankton in all the gulfs from autumn to summer (Figure 5).

The observed increase in the ES trophic levels during summer was not due to a higher presence of planktonic metazoans but rather to the increased contribution of protozooplankton. This finding is consistent with the high trophic redundancy among planktonic metazoans and protozooplankton, which can establish similar trophic interactions and exhibit closely related trophic levels (e.g., [159,160]). This result confirms the crucial ecological role exerted by protozooplankton within the planktonic communities [159,161,162] by improving the stoichiometry of food quality and increasing the efficiency of transfer of organic matter towards the higher trophic levels [161,163]. However, despite the growing literature on these organisms [161] and the production of exhaustive databases reporting the trophic habits and ecological behaviors of protozooplankton and mixotrophic protists [43,164], a significant knowledge gap remains concerning this group of organisms [161]. This gap could depend on the phytoplankton–zooplankton dichotomy, where the marine food web are represented by just two main groups of organisms: the primary producers and their metazoan grazers [161].

The phytoplankton–zooplankton dichotomy has likely influenced even the systematic review conducted in this study, which revealed a lack of information on the ESs directly provided by protozooplankton (Figure 2). In this context, the European Union Marine Strategy Framework Directive (MSFD), i.e., the primary EU directive for managing marine ecosystems, uses 11 descriptors to assess environmental status, where ‘phytoplankton’ and ‘zooplankton’ are referenced in two descriptors (Biological Diversity and Food Webs) and protozooplankton are, remarkably, absent [161]. Since functional diversity is a critical aspect of biodiversity when evaluating ecological functions within natural communities, it is essential to analyze the entire spectrum of biodiversity in the ecosystem services assessment [4].

Natural communities often exhibit significant variations across spatiotemporal scales, thus influencing the delivery of ecosystem services [14,15]. This aspect is particularly relevant for plankton, whose composition depends on environmental factors (e.g., [23,159]). Along the Campania coast, plankton undergo seasonal [23,40] and trophic changes [90]. The analyses applied herein also confirmed the seasonal variability of the planktonic communities of the Campania region (Figure 5), highlighting the effect of the different trophic statuses of the water on plankton communities and the ESs they provide within each gulf and season. Bellardini et al. 2024 [40] reported higher chlorophyll a concentrations during the summer in each gulf compared to autumn, with the Gulf of Naples consistently showing the highest values, indicating a more eutrophic status. In line with this, our findings revealed a general increase in the potential ESs provided by plankton biodiversity from autumn to summer, along with their trophic level during the summer within each gulf (Figure 3 and Figure 4). These results suggest that the higher concentrations of chlorophyll a (i.e., a proxy for photosynthetic organisms [165]) observed during summer determined a slightly higher supply of ESs provided by organisms standing at higher trophic levels when comparing eutrophic to more oligotrophic water conditions. Despite these differences, all the gulfs analyzed herein can sustain fisheries and aquaculture, offering substantial support for local economic activities (Supplementary Figure S2) and confirming the strong connection between coastal habitats and human social and economic benefits [4].

Further research needs to elucidate better the relationship between plankton biodiversity and the overall economic valuation of ESs, as reductions in food security, livelihoods, income, or health can negatively impact societal well-being (Supplementary Figure S2). Adopting a network approach is crucial for identifying trade-offs between ES values, because providing a higher inDegree, such as that attributed to educational ESs in this study, does not necessarily imply a higher societal value (monetary assessment) compared to other ESs with a lower inDegree (e.g., the intangible benefits society receives from cultural heritage ESs). Conversely, recreation from cultural ESs and climate regulation from regulating and maintenance ESs can exhibit high monetary valuations (e.g., [166,167,168,169,170]) in line with the high inDegree values found in this study.

Moreover, future advancements in policy-relevant information should also include the consideration of ecosystem disservices. In the context of plankton, such disservices include harmful algal blooms or jellyfish proliferations that can adversely affect tourism and fisheries [32,33]. However, ecosystem disservices quantification remains a significant challenge due to data limitations and knowledge gaps [32].

4. Conclusions

Marine planktonic communities offer multiple ESs, including the regulating and maintenance of anthropized ecosystems, food and material provisioning to industrial economic activities, and cultural values that inspire artistic expression and promote tourism. This study found that the former two categories were predominant in the literature, while the cultural services require more scientific attention. The methodology applied in this study reinforces the view of a strong connection between environmental conditions, plankton biodiversity, and ESs, emphasizing the need to account for spatial and temporal variability when assessing the socio-ecological status of targeted marine areas [8,15]. This latter aspect is even more crucial considering the increment in the production of biodiversity data, such as those from environmental DNA techniques in marine observatories [171]. However, to further implement the proposed methodology, our paper calls for improving data analysis and knowledge about plankton biodiversity and ecology, particularly regarding underexplored groups such as planktonic bacteria and protozooplankton [161].