The Gulf of Naples as a model system for plankton ecology studies

Abstract

Plankton play a fundamental role in coastal and oceanic ecosystems as a key component of biogeochemical cycles and pelagic trophic webs and contribute to determining and maintaining the health of the oceans. More than half of the world's population living along the coasts relies on services offered by plankton in terms of seafood availability and seawater quality, at the same time altering coastal margins and affecting marine ecosystems (Vitousek et al., 1997). Therefore, monitoring, quantifying and understanding the responses of plankton to the variability of the coastal environment represent an urgent challenge to the scientific community, and even more so in an epoch of rapid changes. Yet, because of the prevalent microscopic nature of planktonic organisms and logistic hindrances, research in this field started developing only in the second half of the XIX century. One of the first marine sites for plankton studies in the world was the Gulf of Naples (GoN), a coastal embayment of the mid-Tyrrhenian Sea in the western Mediterranean. The GoN is located in the temperate zone but with subtropical characteristics, under the anthropogenic impacts from one of the most densely populated areas of the Mediterranean Sea contrasted by the influence of the oligotrophic open Tyrrhenian waters. Consequently, the GoN is a mosaic of areas with different ecological conditions, where highly impacted habitats coexist with relatively pristine localities and marine protected areas. Studies on the plankton of the GoN were fostered by scientists working at the Stazione Zoologica (SZN), the first marine institution in Europe funded in 1872 by Anton Dohrn. Plankton of the GoN were initially analysed to unveil their extraordinary diversity (e.g. Giesbrecht, 1892) and diverse phenology (De Angelis, 1958; Indelli, 1944; Issel, 1934). In the second half of the last century, studies also focused on plankton taxonomy, life cycles and distribution in space and time, until regular monitoring was started in 1984 with a long-term ecological research programme at the site MareChiara (LTER-MC), which is part of the Italian, European and international LTER networks as of 2006. LTER-MC is located two nautical miles off the coast of the city of Naples in an area that can be alternatively influenced by the eutrophic coastal zone and the oligotrophic waters of the Tyrrhenian Sea. Over the years, LTER-MC has proved to be not only a valuable observatory of the diversity, complexity and temporal variability of plankton but also a precious natural laboratory to test hypotheses that emerged from field observations (reviewed by Zingone et al., 2019). In this Special Issue, we have collected the results of the most recent ecological investigations conducted on the plankton of the GoN with the intent to celebrate the 150th anniversary of the SZN foundation, an important occasion that has been widely commemorated (Boero et al., 2023). The Special Issue focuses on phyto- and zooplankton and their environment studied through both field and laboratory investigations, with classical methods as well as taking advantage of recently developed molecular approaches. With this collection, we gather the most updated knowledge on the plankton of the GoN, with special attention to features that may shed light on general ecological questions going beyond the local scale of the sampling site. The topics investigated in this Special Issue span over different temporal scales. Some studies took into consideration a long period of the LTER-MC time series and examined trends of environmental variables (Kokoszka et al., 2023; Romillac et al., 2023) revealing that, in the case of plankton, hydrographic changes including inshore–offshore exchanges, the residence time of freshwater and the shallowing of the mixed layer depth are more important than the simple temperature increase recorded in summer. The response of plankton is seen in the increased intensity over the years of the autumnal blooms, driven by the lengthening of the stratification period, and in significant trends in specific elements of the phyto- and mesozooplankton. Examples are the increase of diatom, prasinophyte and cryptophyte contributions to the phytoplankton biomass (Saggiomo et al., 2023), the increase in carnivores chaetognaths and typical filter feeders, such as cladocerans, appendicularians, thaliaceans and the decline of copepods (Mazzocchi et al., 2023). Interestingly, the observed environmental and biological changes are contrasted by the overall stability of the whole mesozooplankton community (Mazzocchi et al., 2023), which parallels the resistance to interannual variation recently highlighted for phytoplankton communities (Longobardi et al., 2022). When it comes to individual key taxa, the need emerges to consider different aspects of their life cycle, such as fecundity and egg-hutching success, to understand the important role played by biology in shaping the observed seasonal and long-term trends in copepod populations (Carotenuto et al., 2023). At the seasonal scale, the annual patterns of seven different and stable phytoplankton associations, identified by leveraging the multiannual data on species distribution from the LTER-MC time series, show a close relationship with variables related to astronomical factors, that is, temperature, and to the coastal nature of the site, that is, salinity (Zingone et al., 2023). Functional diversity varies across the seasons, with divergent or convergent traits within each association reflecting the variable strength of environmental filtering. A high seasonal signal is also found in dinoflagellate communities investigated in a 3-year metabarcoding data set, which has also revealed a species-rich winter community, so far neglected in the current views of dinoflagellate preference for stable and warm summer conditions (Mordret et al., 2023). A whole range of classical and advanced approaches are used in the different articles to address plankton variability, including the analysis of physical–chemical, biological and diversity data from the natural environment (Kokoszka et al., 2023; Mazzocchi et al., 2023; Romillac et al., 2023; Zingone et al., 2023), laboratory experiments (Carotenuto et al., 2023; Reñé et al., 2023; Traboni et al., 2023) and more sophisticated chemotaxonomic (Saggiomo et al., 2023) and biomolecular approaches (Di Capua et al., 2023; Mordret et al., 2023; Reñé et al., 2023; Russo et al., 2023). The latter studies have addressed temporal trends in groups of species hardly detected by morphological methods, unveiling, for example, a high amount of dinoflagellate diversity not assigned to any described taxa (Mordret et al., 2023). This unknown diversity may correspond to novel species yet to be discovered and described, but may also be the effect of massive gaps in the reference data sets, that is, the dictionaries that allow translating the environmental DNA data into biologically meaningful information. In this respect, the delivery of novel reference sequences from several crustacean zooplankters of the GoN represents a relevant contribution to help interpret metabarcoding data and decipher the hidden diversity of coastal plankton communities (Di Capua et al., 2023). Molecular approaches have also proven useful and usable to address interspecific relationships of different natures. Co-occurrences derived from a 3-year metabarcoding time-series, coupled with background biological information on the size and trophic habits of their components, have revealed a trophic hierarchy and modularity in the trophic network, which would allow quick food-web re-arrangements under the shifting hydrographic conditions that are typical of the coastal area of the GoN (Russo et al., 2023). The same 3-year data set has also been explored in the first investigation on diatom parasites of the GoN, where incubation experiments are combined with microscopy observations and contextual metabarcoding analyses (Reñé et al., 2023). This multi-approach study has shown that chytrid fungi (Chytridiomycota) are a common component of the protist community in the GoN and would deserve quantification with specific techniques to assess their role in the mortality of their hosts. Besides metabarcoding, another special technique, the stable isotope analysis, has provided details of trophic interactions relevant to unveil the complexity of planktonic food webs, which can buffer the environmental variability caused by the specific hydrographic features of the GoN (Merquiol et al., 2023). Finally, laboratory experiments have revealed that copepod daily intake of food is not affected significantly by the presence of microplastics, which are presently one of the most concerning threats to marine habitats and organisms, likely because of their ability to avoid those particles and flexible feeding habits (Traboni et al., 2023). The studies presented in this Special Issue add many new pieces to the complex puzzle of the plankton ecosystem in the GoN, at the same time opening new questions and providing indications for new studies to be developed in the future. Mainly the topics of trophic and parasitic interactions have only started to be explored and highlight the need to take into consideration all levels of the network that connects marine planktonic organisms. While trends are observed in some components of the system, it is necessary to go beyond descriptions and take into consideration the life cycles and reproductive traits of plankton species, along with other functional aspects that allow the unveiling of the mechanism underlying those trends, thus opening the way to the forecast of future scenarios under changing environmental conditions. In this respect, both classical and laboratory studies, coupled with the molecular information obtained from natural populations and interpreted in the light of background knowledge, are expected to provide a formidable new asset to understand plankton and predict their changes in the coming years. In addition to the contribution to the knowledge of the GoN ecosystem, the studies collected in this Special Issue not only emphasize the specificity of the area but also shed light on several aspects of the plankton ecology that go beyond the local scale, pointing to highlight the pivotal role of long-term investigation sites as testbeds for wide-ranging ecological questions. Not applicable. None. Not applicable.