Description of trophic status, hyperautotrophy and dystrophy of a coastal lagoon through a potential oxygen production and consumption index—TOSI: Trophic Oxygen Status Index

Abstract

Seasonal changes of trophic status of the Sacca di Goro lagoon (northern Italy) are analysed through time series of oxygen metabolism for two stations in which separate measures of planktonic, macroalgal (Ulva rigida), and benthic exchange are available. These component results and their sums (i.e. total ecosystem metabolism) are compared using conventional analyses and an index obtained from oxygen fluxes (Trophic Oxygen Status Index, TOSI). The TOSI is derived from the Benthic Trophic Status Index (BTSI) proposed earlier by Rizzo et al. [Estuaries 19 (1996) 247] and basically represents the net potential metabolism. The index results from the relationship between net maximum productivity (NP), measured at saturating light, and dark respiration (DR). The index was developed to provide a simple portrayal of oxygen processing over time and space for shallow aquatic systems and has two modes: a categorical classification and a graphical representation. The categorical classification of the index from autotrophy to heterotropy provides a rapid assessment of the potential oxygen balance and thus evidences critical situations in the lagoonal metabolism. In the graphical representation of the TOSI, three pieces of information are given: the categorical TOSI, the magnitude of flux for both NP and DR and the time line of the fluxes. Where flushing is slow, the TOSI reflects dissolved oxygen dynamics since the NP:|DR| ratio clearly correlates with both the maximum oxygen concentration (MOC) and the daily quantity of oxygen remaining in the water column (RO). However, TOSI is less well related to MOC and RO in open systems in which oxygen concentrations are dominated by physical factors. The graphical representation of TOSI seems also suitable to represent the degree of intrasystem disturbance that is related to the excess of primary production and changes in oxygen availability. It can also discriminate among different photoautotrophic conditions, including hyperautotrophy, as an abnormal oxygen production with respect to the biomass build up, and dystrophy, as the subsequent abnormal oxygen deficit which causes prolonged anoxia and the onset of anaerobic metabolism. Overall, the index provides a tool for rapid assessment of system metabolism and potentially its consequences.

Introduction

The trophic status of aquatic ecosystems results from the net biotic metabolism, which basically represents the difference between primary production and community respiration (Kemp et al., 1997). Ecosystems that rapidly export or bury the autochthonous photosynthetic product can be considered autotrophic, since most of the primary production is not available to heterotrophs. In contrast, ecosystems that accumulate organic matter become heterotrophic, since most of the primary production and organic matter import are processed throughout the detritus foodweb (Duarte and Cebrian, 1996). The debate on whether coastal ecosystems are heterotrophic or autotrophic has often focused on the accumulated organic matter budget and C:N:P stochiometry (Smith, 1993). Nevertheless, trophic conditions are usually assessed considering oxygen metabolism as a measurement which integrates ecosystem properties (Murray and Wetzel, 1987, D’Avanzo and Kremer, 1994, Cowan and Boynton, 1996, Cowan et al., 1996, D’Avanzo et al., 1996, Rizzo and Christian, 1996, Rizzo et al., 1996). When flushing is slow, oxygen concentration basically represents autochthonous processes, namely photosynthetic production and uptake by respiratory and biogeochemical processes, and it summarises trophic status. However, the oxygen budget results not only from biological processes but also from physical forcing and therefore the link between oxygen concentration and community metabolism may not necessarily be strong (Stanley and Nixon, 1992, Kraines et al., 1996).

In coastal marine environments, the oxygen budget depends on the structure of the primary producer community, which may span phytoplankton–seagrasses–seaweed, with potentially important contributions by benthic microalgae and cyanobacterial mats (Sand-Jensen and Borum, 1991). In estuaries and shallow coastal systems, increased nutrient inputs have led to the progressive replacement of seagrasses with fast growing ephemeral seaweed (Duarte, 1995, Borum, 1996, Valiela et al., 1997, Hemminga, 1998). Here, most of the processes regulating trophic status are restricted to the benthic system, where sediment–water interactions play a prominent role (Castel et al., 1996).

There have been numerous methods applied to the determination of benthic production and respiration; the merit of any given approach depends heavily on the system under study, logistic constraints, etc. (for more details see Kemp and Boynton, 1980, Revsbeck and Jørgensen, 1983, Miller-Way et al., 1994, D’Avanzo et al., 1996, Wiltshire et al., 1996, Asmus et al., 1998). Recently, Rizzo et al. (1996) presented a comparative index to assess oxygen metabolism in shallow aquatic environments: the Benthic Trophic Status Index (BTSI). The BTSI was designed to provide a categorical classification of benthic systems relative to their potential for heterotrophic and photoautotrophic activities as measured through hourly oxygen uptake in the dark (community respiration, CR) and production or uptake at light saturation (net community production, NCPmax). It includes four categories: total heterotrophy (NCPmax≤CR<0), net heterotrophy (CR<NCPmax≤0), net photoautotrophy (0<NCPmax≤|DR|) and total photoautotrophy (0<|DR|<NCPmax). Overall, negative values indicate a net oxygen uptake by the sediment, while positive values indicate a release to the water column. Rizzo et al. found differences in BTSI associated with sediment type, depth and salinity regime among a variety of estuarine systems within the US, with CR and NCPmax from −50 to 50 mg O₂ m⁻² h⁻¹, which are relatively low. The designated categories provide information to rapidly assess the balance of oxygen metabolism but not the intensity of either potential NCPmax or CR. This can be accomplished graphically, as done by Viaroli et al. (1996a) in assessing the trophic status of several benthic estuarine systems in Europe and by Sundbäck et al. (2000) for microphytobenthic sites in Sweden.

In estuarine and coastal ecosystems of temperate and subtropical regions, the occurrence of ephemeral seaweed and, to a lesser extent, of other primary producers may cause a strong imbalance of the oxygen metabolism, since periods of high photoautotrophic activity coupled to labile organic matter accumulation are followed by predominantly heterotrophic phases. This leads to large and pulsed oxygen variations, spanning from supersaturation to complete anoxia on both seasonal and diurnal time scales (D’Avanzo et al., 1996, Viaroli et al., 2001). The most common trophic criteria are based on concentrations of dissolved inorganic phosphorus and nitrogen, phytoplankton chlorophyll a and organic matter (Premazzi and Chiaudani, 1992, Nixon, 1995). These methods and the comparative index mentioned earlier are not well suited to represent those environments where a great primary production excess—i.e. hyperautotrophy—feed strong decomposition processes causing complete anoxia through the water column, i.e. dystrophy.

Herein we test and validate an index of trophic status through analysis of oxygen metabolism and exchange in the Sacca di Goro lagoon, Italy. We report results of time series of maximum potential oxygen production (NP) and dark respiration (DR) of the community for two stations in which we have separate measures of planktonic, macroalgal and benthic exchange. We compare these component results and their sums using conventional analyses and the categorical and graphical representations of the BTSI by Rizzo et al. (1996). Further, we attempt to correlate NP and DR with water column oxygen data. Finally, we propose an extension of the BTSI categories by considering hyperphotoautotrophy and dystrophy. We refer to our extension of the application of the BTSI as a Trophic Oxygen Status Index (TOSI), since it may now include not only benthic but also other ecosystem components.

The Sacca di Goro is a shallow-water embayment of the Po River Delta (44°47′–44°50′N and 12°15′–12°20′E) (Fig. 1). The bottom is flat, and the sediment is composed of typical alluvial muds with a high clay and silt content in the northern and central zones. Sand is more abundant near the southern shore-line, while sandy mud prevails in the eastern area. The eastern zone is very shallow (maximum depth 1 m) and accounts for one-half of the entire area and for one-fourth of the total water volume, while the central area is on average 1.5 m deep. The freshwater discharge from the Po di Volano and minor canals is about 0.5×10⁹ m³ per year. An approximately equivalent amount is discharged by the Po di Goro River during flooding. The lagoon is microtidal, with a maximum tidal amplitude of approximately 1 m. The water temperature range is typical of sub-Mediterranean regions with summer peaks up to 30 °C and winter minima around 5 °C. The lagoon is subjected to anthropogenic eutrophication, which results in phytoplankton blooms in the deeper central zone, although Gracilaria verrucosa contribute to production. Excessive growth of the seaweed Ulva rigida C. Agardh (Chlorophyta: Ulvales) occurs in the sheltered eastern area, where the decomposition of macroalgal biomass is responsible for summer anoxia (see Viaroli et al., 2001, and references therein). The abnormal growth of Ulva causes extreme variability in oxygen patterns with periods of supersaturation followed by prolonged anoxia.