Testing the saprobity hypothesis in a Mediterranean lagoon: Effects of confinement and organic enrichment on benthic communities
Graphical abstract
Introduction
Ecological aspects of brackish-water environments, such as coastal lagoons, have been investigated for some time because of their multifunctional uses and potential for exploitation. The large geomorphological, hydrological and biological heterogeneity of such environments has prompted numerous conceptual models and synthetic patterns aimed at explaining the main processes and mechanisms of lagoon biological functioning (Ardizzone et al., 1988, Basset et al., 2006; Tagliapietra and Ghirardini, 2006).
The main impact of salinity has been stressed since the earliest studies (Remane, 1934, Venice System, 1959). D’Ancona et al. (1954) and Sacchi (1961) went on to note the role of “vivification” (i.e. water renewal) from the adjacent marine ecosystem. Subsequently, the importance of sea water renewal in lagoonal systems was taken in account in the drawing up of the Guélorget–Perthuisot [P–R] model for so-called “paralic” (i.e. confined) environments (Guélorget and Perthuisot, 1992). Some authors discussed the ecological factors linked to the confinement of paralic environments (Sacchi and Occhipinti Ambrogi, 1992, Barnes, 1994, Koutsoubas et al., 2000). Such environments' intra- and inter-heterogeneity has also been discussed in the light of the mechanical energetic gradient, according to the “ergocline theory” (Legendre and Demers, 1985, Galuppo et al., 2007). Moreover, because of lagoons' hydrological regime and morphology with restricted outflows, a large amount of organic matter (OM) settles and decomposes in the sediment; such OM includes continental and marine detritus, and the majority of the biomass produced inside the lagoon (Barnes, 1980, Magni et al., 2005). Thus, trophic loading inside the lagoon is increased by the substantial accumulation of decaying organic material which remains trapped (De Falco et al., 2004, Magni et al., 2004, Como et al., 2007).
The selective role of trophic loading on benthic communities' structure and distribution in some Italian coastal lagoons has been highlighted by Fresi et al. (1985) and Gravina et al. (1988). The latter introduced the idea that, within a defined range of confinement, the brackish-water communities are re-arranged depending principally on the trophic pattern. More recently, Pusceddu et al. (2007) showed that the trophic state of brackish-water ecosystems is closely linked to ecosystem efficiency and biodiversity. Furthermore, Magni et al. (2009) demonstrated the applicability of the Pearson–Rosenberg [P–R] model (Pearson and Rosenberg, 1978), describing a generalized pattern of response of marine benthic communities in relation to organic enrichment, to coastal lagoons.
Building upon an extensive body of literature, Tagliapietra et al. (2012) reviewed classic conceptual models describing the succession of benthic communities along a gradient of OM enrichment for freshwater (e.g. the Saprobiensystem; Kolkwitz and Marsson, 1908, Kolkwitz and Marsson, 1909), coastal marine (the P–R model) and lagoonal (the G–P model) ecosystems. The authors combined the above models under a single conceptual framework of habitat saprobity for coastal lagoons. They referred to saprobity as the “state descriptor” of an aquatic ecosystem resulting from the (exogenous and endogenous) input of OM, its biodegradation and the clearance of catabolites. The microbial decomposition of OM involves physico-chemical modifications to the medium which are selective for the biota. The main selection factors are low dissolved oxygen (DO) concentrations, leading to reducing conditions and lower pH, and the accumulation of the toxic by-products of anaerobic metabolism. Clearance depends mainly on the reuse of OM catabolites by microorganisms (often referred to as re-mineralization or self-depuration), on burial and on export from the system by means of water exchange and the release of gases into the atmosphere. These aspects imply that saprobity cannot simply be equated with the OM standing stock or budget of the system, or with single metabolic processes such as respiration, but involves ecosystemic processes (Tagliapietra et al., 2012). The saprobity level of a water body can be ascertained both by metabolic-dynamic measurements and by the analysis of its living communities (Caspers and Karbe, 1966, Sládeček, 1967). The higher the saprobity, the more impaired the system, with progressively poorer benthic communities characterized by species that are increasingly tolerant of reduced conditions and toxicity. In coastal lagoons, these processes are strongly driven by hydrodynamics, which govern the land-sea gradient. This is marked contrast to estuaries where the environmental gradient is mainly structured by the flow of fresh water, which generates a salinity gradient. Within this framework, saprobity was suggested to be a suitable “state descriptor” for characterizing the natural conditions of coastal lagoons and assessing their environmental quality (Tagliapietra et al., 2012).
The concept of saprobity was developed for rivers and lakes more than a century ago in relation to the discharge of organic waste (Kolkwitz and Marsson, 1908, Kolkwitz and Marsson, 1909). Saprobity is a selection agent for species in all aquatic environments. It is particularly important, however, in coastal lagoons and enclosed coastal basins, especially under microtidal and nanotidal conditions (Tagliapietra and Ghirardini, 2006), where reduced hydrodynamics allows OM to be trapped within the basin and to accumulate on the sediment surface (De Falco et al., 2004), and where most degradation processes occur (Viaroli et al., 2004). Although the application of the saprobity concept to lagoons dates back to the first half of the twentieth century (Potereaev, 1936, cited by Milovidova, 1975, Vatova, 1940a, Vatova, 1940b), it was little developed and mostly ignored in subsequent years. For these reasons, we aimed to investigate the applicability of the saprobity concept in a Mediterranean lagoon by analyzing benthic communities' distribution along a putative “saprobity gradient”, as determined by a number of interlinked environmental variables, such as DO, phytopigments and sedimentary OM, as well as the basin hydrodynamic features, such as water current and water residence time (Tagliapietra et al., 2012). In particular, we tested a) the hypothesis that the benthos is distributed according to both the P–R and G–P models, which can be unified under the concept of habitat saprobity for coastal lagoons (Tagliapietra et al., 2012) and b) the hypothesis that indicator species of different saprobic levels can be identified among dominant taxa. The possible effect of salinity as an additional agent of selection in brackish environments, particularly at the oligohaline and hyperhaline extremes (Tagliapietra et al., 2012), was also considered.
Section snippets
The Cabras lagoon system
The Cabras lagoon is a shallow water body located on the west coast of Sardinia, Italy (Fig. 1). With an area of about 22 km2 and a mean depth of 1.4 m (maximum of 2.2 m), the Cabras lagoon is the largest lagoon in Sardinia. The watershed of the Cabras lagoon extends over an area of ca. 430 km2, this inhabited by approximately 38,000 people. Most of the freshwater input to the lagoon originates from the Rio Mare e Foghe, which drains an area of 313 km2. A minor tributary, Rio Tanui, is located
Water and sediment variables
Water temperature varied from 8.8 °C (site C2) to 32.4 °C (site C3), salinity from 0.5 psu (C1, winter) to 29.1 psu (C3, summer), and DO from 2.2 mg l−1 (C1, summer) to 15 mg l−1 (C3, winter) (Fig. 2). Major differences between sites were found for salinity and DO. Salinity consistently increased along the salinity gradient from C1 to C3 in summer, ranging about 10–25 psu at C12 (Magni et al., 2005). However, at C3 salinity drastically decreased from 27 to 3 psu in the subsequent winter. DO
Discussion
The results of the present study emphasized major environmental and biotic differences between distinct zones of the Cabras lagoon. These differences were consistent with the concept of habitat saprobity, recently proposed by Tagliapietra et al. (2012) as a unifying approach for coastal lagoons of both the Guélorget and Perthuisot [G–P] (1983, sensu confinement) and the Pearson and Rosenberg [P–R] (1978, sensu organic enrichment) models. At the four investigated sites, the habitat heterogeneity
Acknowledgments
This research was supported by the Flagship Project RITMARE – The Italian Research for the Sea – coordinated by the Italian National Research Council and funded by the Italian Ministry of Education, University and Research within the National Research Program 2011–2013. The authors would like to thank Andrea Satta and Andrea Camedda, CNR-IAMC Oristano, for technical and field assistance, and Marcello Giorgi, University of Rome “Tor Vergata”, for technical support in data analysis procedures. We
References (53)
A critical-appraisal of the application of Guélorget and Perthuisot's concepts of the paralytic ecosystem and confinement to macrotidal Europe
Estuar. Coast. Shelf Sci.
(1994)- et al.
Temporal changes of a macrobenthic assemblage in harsh lagoon sediments
Estuar. Coast. Shelf Sci.
(2009) - et al.
Sediment characteristics and macrofaunal distribution along a human-modified inlet in the Gulf of Oristano (Sardinia, Italy)
Mar. Poll. Bull.
(2007) - et al.
Spatial variations in δ13C and δ15N values of primary consumers in a coastal lagoon
Estuar. Coast. Shelf Sci.
(2012) - et al.
Distribution and ecological relevance of fine sediments in organic-enriched lagoons: the case study of the Cabras lagoon (Sardinia, Italy)
Mar. Poll. Bull.
(2008) - et al.
Sediment features, macrozoobenthic assemblages and trophic relationships (δ13C and δ15N analysis) following a dystrophic event with anoxia and sulphide development in the Santa Giusta lagoon (western Sardinia, Italy)
Mar. Poll. Bull.
(2008) - et al.
Animal-sediment relationships: evaluating the ‘Pearson-Rosenberg paradigm’ in Mediterranean coastal lagoons
Mar. Poll. Bull.
(2009) A new method for non-parametric multivariate analysis of variance
Austral Ecol.
(2001)- et al.
Management of Coastal Lagoon Fisheries and Aquaculture in Italy
(1988) - et al.
The ecology of coastal lagoons in central Italy
Anim. Hum. Biol.
(1991)
Coastal Lagoons
Short-term effects of hypoxia and bioturbation on solute fluxes, denitrification and buffering capacity in a shallow dystrophic pond
J. Exp. Mar. Biol. Ecol.
Typology in Mediterranean transitional waters: new challenges and perspectives
Aquat. Conserv. Mar. Freshw. Ecosyst.
Trophie und Saprobität als stoffwechseldynamischer Komplex. Gesichtspunkte für die Definition der Saprobitätsstufen
Arch. Hydrobiol.
Change in Marine Communities: an Approach to Statistical Analysis and Interpretation
Il trofismo della Laguna Veneta e la vivificazione marina
Arch. Oceanogr. Limnol.
Sediment grain-size and organic carbon distribution in the Cabras lagoon (Sardinia, west Mediterranean)
Chem. Ecol.
Characterization of exopolysaccharides produced by seven biofilm-forming cyanobacterial strains for biotechnological applications
J. Appl. Phycol.
Ecologia e distribuzione dei Crostacei Anfipodi nella laguna di Orbetello
Boll. Mus. Civ. Stor. Nat. Verona
Note sui Crostacei Anfipodi delle lagune laziali e campane
Boll. Mus. Ist. Biol. Genova
Coastal lagoon isopods (Crustacea, Peracarida) of Latium
Nova Thalass.
Considerations on the Relationship Between Confinement, Community Structure and Trophic Patterns in Mediterranean Coastal Lagoons
Habitat types and distribution of benthic macroinvertebrates in a transitional water ecosystem: Alimini Grande (Puglia, Italy)
Trans. Waters Bull.
Selecting factors in polychaete communities of central Mediterranean coastal lagoons
Int. Rev. Ges. Hydrobiol.
Descriptive analysis and classification of benthic communities in some Mediterranean coastal lagoons (Central Italy)
Mar. Ecol. P.S.Z.N.I
Le domaine paralique. Expression géologique, biologique et économique du confinement
Cited by (25)
Diversity of decapod crustaceans in a neotropical coastal lagoon interconnected with the sea/estuary
2024, Regional Studies in Marine ScienceTaxonomic and functional diversity of nematode fauna: two sides of the same coin in the ecological quality assessment of transitional environments
2023, Estuarine, Coastal and Shelf ScienceSeagrass macrobenthic biodiversity does not vary in conformity with a leaky-lagoonal confinement gradient
2023, Marine Environmental ResearchDynamics of polychaete communities in the intertidal soft bottom of Alexandria coast, Egypt
2022, Regional Studies in Marine ScienceNatural stress vs. anthropogenic pressure. How do they affect benthic communities?
2022, Marine Pollution Bulletin