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4 Marine Organisms As Biomonitors WITPress_BMTA_ch004.qxd 11/26/2007 17:00 Page 81 4 Marine organisms as biomonitors M E Conti & M Iacobucci 1 Introduction Biomonitors are organisms mostly used for the quantitative determination of contaminants in the environment (see Chapter 1). The present chapter discusses mainly the employment of seaweeds, sea phanerogams and molluscs as bioindi- cators of heavy metal contamination, since they are the organisms of choice in most of the programmes of biological monitoring of coastal marine waters (see Water Framework Directive 2000/60 EC (WFD) [1]). Bioindicators provide an integrated view of the presence of micropollutants, and in the aquatic environment they respond only to the fraction presenting a clear ecotoxicological relevance (see Chapter 1). Among the different methodological approaches of biological monitoring of a marine ecosystem, the approach based on the bioaccumulation capacity of some chemical species, as for instance trace metals, is among the most important. This capacity is particularly present among macroalgae, sea phanerogams, molluscs, oysters, etc. These organisms can be proposed as possible bioindicators when the presence of a direct correlation between internal and environmental levels of the various metals has been verified [2]. Therefore, the chemical analysis of the tissues of such organisms represents a method for measuring the integrated bioavailability of trace metals in the marine environment over time, given their remarkable bioconcentration capacity [3–5]. Comparing the levels of metals in the organisms collected at different sites is a very useful way to gather information on the biologically available levels of inor- ganic contaminants in the areas under study. In general, micro and macroalgae, marine phanerogams, mussels, oysters, tellinid bivalves, polychaets and crus- taceans are some of the organisms used as bioindicators of marine ecosystems [4]. Marine organisms can accumulate contaminants present in solution and in the particulate material, thus determining a variation in the level of bioaccumulation depending on the trophic level occupied. Some marine invertebrates can take contaminants from the particulate material of the sediment, especially when their physico-chemical conditions are being altered. Algae and phanerogams take contaminants in solutions and many herbivorous crustaceans reflect their concentrations. Therefore, in order to have a full picture of the bioavailability of the vari- ous pollutants of water ecosystems, it is necessary to use several kinds of WIT Transactions on State of the Art in Science and Engineering, Vol 30, © 2008 WIT Press www.witpress.com, ISSN 1755-8336 (on-line) doi:10.2495/978-1-84564-002-6/04 WITPress_BMTA_ch004.qxd 11/26/2007 17:00 Page 82 82 BIOLOGICAL MONITORING: THEORY & APPLICATIONS bioindicators: macrophytes algae responding mainly to metals in solution, marine phanerogams, which are higher plants provided with a root apparatus and responding also to the amount of metals biologically available in sediments; sus- pensivorous filter feeders (like mussels) responding to dissolved and suspended contaminants and detritivores taking recent deposits on the sediment. 2 Algae and bioaccumulation of heavy metals Heavy metals are natural constituents largely distributed in the environment; when highly concentrated they are harmful to animals and plants. Moreover, they cannot be eliminated from the water body: they settle on the ocean bottom, and currents bring about a slow release which causes serious risks of contamination for the organisms [6]. The existing balance between suspended metals and metals present on the sedi- ments was in many cases broken by human activity which caused a wholesale increase in the concentration levels of metals through uncontrolled discharges, especially in highly industrialized areas. In chronically polluted areas, algae and sea plants tend to accumulate metals in very high and dangerous levels [7, 8]. The levels of bioaccumulation of contaminants in older algal tissues can be compared to the accumulation on more recent tissues of the same individuals and thus help determine the evolution of the contamination process for the organisms present in a given geographical area. Sea macroalgae belong to divisions Chlorophyta, Rhodophyta and Phaeophyta. From Chlorophyta the species of green algae (Chlorophyceae) pertaining to the genera Enteromorpha [6, 9–16], Ulva [11–13, 17–25], Cladophora [10, 12, 26], Codium [11, 27], Caulerpa [11, 12] and Chaetomorpha [10] have been selected as bioindicators of heavy metals in the marine environment. From Phaeophyta the species of brown algae (Phaeophyceae) used in moni- toring studies belong to the genera Dictyota [11, 28], Scytosiphon [28], Colpomenia [29, 30], Padina [16, 31–33], Fucus [34–37], Ascophyllum [38, 39] and Macrocystis [29, 40]. From Rhodophyta the species mostly used were the red algae (Rhodophyceae) of the genera Gracilaria [10, 12, 17–19], Pterocladia [11, 28], Gelidium [28], Gigartina [11, 29, 30] and Porphyra [28]. Not only the selection of the appropriate bioindicators but also the knowledge of biological variables (age, sex, size, seasonality, portion of the plant analysed) related to the specific organism selected or particular features of the algal species (degree of submergence in the sea, tolerance to metal stress) may be taken into account in the sampling design [41, 42]. In algae, apart from sampling considerations (see below), metal concentrations depend both on external factors (pH, salinity, inorganic and organic compounds) and on physico-chemical parameters (temperature, light, oxygen and nutrient) [8]. Metal bioaccumulation is a function of the total enrichment in metal by a specific WIT Transactions on State of the Art in Science and Engineering, Vol 30, © 2008 WIT Press www.witpress.com, ISSN 1755-8336 (on-line) WITPress_BMTA_ch004.qxd 11/26/2007 17:00 Page 83 MARINE ORGANISMS AS BIOMONITORS 83 algal organism, taking into account those metal forms, known as bioavailable species, that are more easily integrated by the organism [43]. Sea life benefits from algae, which are at the basis of the food chain. The net amount of global oxygen produced by algae through photosynthesis is an esti- mated 30–50%. Macroalgae have a multicellular organization, their structures can be complex and quite large in terms of size, and sometimes they have a differen- tiated thallus in organs analogous to those of higher plants [44]. Some chlorophyte like Caulerpa and others are multinucleated unicellular organisms equally able to show complex structures [45]. The degree of metal bioaccumulation in aquatic organisms has been widely studied and can serve as a reference point for further monitoring studies as well as to help prevent potentially harmful effects on higher organisms. The earliest studies, dating back to the 1960s [46, 47] found a linear correla- tion between zinc concentrations in Ulva and Laminaria digitata and mean con- centrations of zinc in the surrounding water. Also Seeliger and Edwards [48] showed an existing correlation of 0.98 for copper and 0.97 for lead between seawater and a number of algal species (Blidingia, Enteromorpha and Fucus). Generally, suspended metals present in water are a function of the kind and quan- tity of sediments and only partially do they depend on climatic and hydrographic processes [8, 48]. Biomonitoring studies require therefore rigorous sampling procedures. Moreover, metal concentration in algae can vary along both the vertical and the horizontal position of the water column, in relation to the variation of the degree of exposure to contaminants [2, 47]. Algae only bind free metal ions whose concentrations depend in turn on the nature of suspended particulate matter which is formed by organic and inorganic compounds [8, 49]. At an early stage, algae accumulate metals on their external surface through a reversible physico-chemical uptake process, followed by a process regulated by cellular metabolism [8, 50]. This kind of uptake has been the object of debate among researchers. Other authors, for instance, found that zinc accumulation in some brown algae is irreversible [35, 51]. In general, it is widely accepted that the metal uptake through cellular mem- branes is mainly due to diffusion rather than an active transport mechanism. The kinetics of uptake through passive diffusion is described by Fick’s law. Depledge and Rainbow [52] suggest that Fick’s equation may require some modification in order to take into account also the differences in the electrical potential existing through many cellular barriers [52]. Figure 1 shows a general model of the distribution of metals in aquatic ecosystems. The accumulation mechanisms of metal on the part of algae takes place through the way metals bind to the external cellular wall. This can be of an ionic kind or through the formation of complexes with the ligands of the cellular wall. The polymers constituting the cellular wall are rich in carboxylic, phosphoryl, aromatic and hydroxyl groups that can bind cationic metals [53, 54]. WIT Transactions on State of the Art in Science and Engineering, Vol 30, © 2008 WIT Press www.witpress.com, ISSN 1755-8336 (on-line) WITPress_BMTA_ch004.qxd 11/26/2007 17:00 Page 84 84 BIOLOGICAL MONITORING: THEORY & APPLICATIONS ORGANIC COMPLEXES SPECIATION IONS OR ION PAIRS SOLUBLE PHASE INORGANIC COMPLEXES M E T PLANKTON A SORPTION L PARTITIONING BY ORGANIC PARTICLES S O INORGANIC U R C E INSOLUBLE DEPOSITION RESUSPENSION PRECIPITATE Figure 1: General
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