Many studies finalised to a reclamation project of the industrial area were carried out on the industrial site of Bagnoli (Naples). Among these studies, the sedimentological, chemical, and ecological characteristics of marine sediments were analysed. Seven short cores, located in the proximity of a steel plant, were analysed for grain-size, polychlorobiphenyls, polycyclic aromatic hydrocarbons and heavy metals. As well, benthic foraminiferal assemblages were investigated. Sediment pollution was mainly due to heavy metals; in particular, copper, mercury and cadmium showed a ‘spot’ (site-specific) distribution, while iron, lead, zinc and manganese showed a diffuse distribution, with a gradual decrease of concentration from coast to open sea. Heavy metals pollution seems to explain some of the variation in the foraminiferal abundance. The combined copper and iron contamination might be the cause for the complete absence of foraminifera in the four shallower cores. Moreover, the ratio between normal and deformed specimens of Miliolinella subrotunda and Elphidium advena could be indicative of heavy metal pollution. In particular, Miliolinella subrotunda could be a potential bioindicator for copper pollution, since the abundance of irregular specimens of this species could be related to copper concentrations.

Introduction

A recent law (decree n.468/2001—National program of remediation and environmental recovery), promoted by the Ministry of Environment of Italy, focused attention on the contamination determined by the presence and the activity of some disused heavy industrial plants located near the Italian coast. Such a law requires a complete environmental study before the start of a reclamation project on the marine polluted area. A multidisciplinary approach is necessary to evaluate the chemical-physical and ecological characteristics of marine sediments in order to plan the reclamation. The Bagnoli steel plant was the object of the first research; the related characterisation survey was considered as pilot research for all the contaminated Italian sites.

In the context of the wide interdisciplinary research, a study on seven short cores from the inner shelf, in the proximity of the Bagnoli plant, was carried out. They were analysed for grain size, polychlorobiphenyls (PCBs), polycyclic aromatic hydrocarbons (PAHs) and heavy metals (Al, As, Cd, Cr, Cu, Fe, Hg, Mn, Ni, Pb and Zn). In addition, qualitative and quantitative studies of benthic foraminiferal assemblages were performed.

The aim of this research is a preliminary characterisation of marine sediments through the analysis of sedimentological, chemical and ecological features. The response of individual foraminifera was investigated in order to evaluate the impact of pollution on the sea-bottom ecological health and to identify possible bioindicators.

Foraminifers are protozoans that belong to phylum of Reticulosa (reticulopodial amoebae) (Cavalier-Smith, 1993). Most benthic foraminifers have a mineralised, calcareous or arenaceous, shell or ‘test’ that has a high fossilisation potential.

Benthic foraminifers are recognised as useful tools in pollution monitoring because they are ubiquitous in coastal marine environments and they are very sensitive to environmental changes, to which they respond in short periods owing to their brief life-cycle (few weeks-some months). The analysis of the foraminiferal assemblages may be conducted on a statistical basis, using small sediment samples. Consequently, a study may be conducted on samples from cores, which offer a picture of environmental evolution (Yanko et al., 1999).

The first research on foraminifers as related to pollution were conducted in the early 1960s (Watkins, 1961). In the last decade a great number of studies have reported effects of many types of pollutants on the structure and composition of benthic foraminiferal assemblages and on the morphology of tests. Chemical pollution may determine a decrease of species diversity and faunal density. Frequent aberrant specimens and/or assemblages with stunted specimens were found in sites contaminated by heavy metals pollution (Alve, 1991a; Sharifi et al., 1991; Yanko et al., 1994). Most recently, the interest of researchers has been focused on the correlation between specific alterations and single pollutants (Yanko et al., 1998; Alve and Olsgard, 1999; Samir and El-Din, 2001). In cases of moderate pollution, percentages of abnormal tests do not exceed the natural background, but the distribution of some tolerant pioneer species shows a strong correlation with one or several contaminants (Debenay et al., 2001).

The study area

The study area is included in the eastern part of the Gulf of Naples (Southern Italy), located between Nisida Island and the town of Bagnoli. It belongs to the Phlegrean Fields volcano-tectonic system (Figure 1a, b). The geology is very dynamic and related to intense and relatively recent volcanic activity. Bradyseismic movements, land and underwater gas emissions are associated to the volcanic activity. The Pozzuoli Gulf is an area of recent volcanic collapse (12–10 kyr BP), characterised by four morpho-structural units: the coastal shelf (up to 50 m depth), a central collapse area, the volcanic submarine banks (Nisida, Penta Palummo and Miseno Banks) and the external shelf (De Pippo et al., 1984).

Sediments from Bagnoli were recognised to reflect the industrial activity in the region due to the high concentrations of Cu, Fe, Hg, Mn, Pb and Zn found in the littoral areas, near industrial centres (Damiani et al., 1987). Industrial and agricultural activity is also reflected through elevated concentration of PCBs, PAHs and DDT. Sharp and Nardi (1987) found anomalous high values for Ag, As, Cd, Co, Cr, Cu, Hg, Ni, Pb and Zn mainly between the two long piers of the Bagnoli plant. A correlation analysis revealed the presence of two major suites of associated elements: the first one is constituted by Pb, Cd, Zn, As, Cu, Co and Ag and the second one by Ni, Cr, Co and Ag. The authors estimated for this area a sedimentation rate of 0.4 cm y−1, deducing that the time of maximum pollution occurred about 70 years ago.

The industrial activity of the steel plant started in 1905 and high steel production levels were maintained from 1913 to 1943 (Figure 1c). In 1930 two long piers were built in order to allow the berthing of large tonnage boats. At the northern pier, raw materials such as fossil coal and iron ores were discharged while at the southern one, finished products were loaded on boats. Industrial production was interrupted from 1943 to 1946 due World War II activities. In the early 1960s, contaminated soil from the industrial area was used to fill part of the sea stretch between the two piers to allow for widening and the development of the industrial activity. Consequently, the natural coastline was altered and the new spaces so obtained were utilised for the construction of industrial buildings and the storage of coal. From the comparison of bathymetric maps of different historical periods it may be deduced that the sea-bottom morphology, especially near the piers, was modified by the fall of materials during loading and unloading operations (Abbate et al., 1998). In 1990, industrial production ceased.

Materials and methods

Seven cores (F1, F3, G4, H4, R1, T1 and T3) were taken in September 1999 by a scuba diver using a PVC liner with 6 cm internal diameter. The location of the sampling site was determined by Global Positioning System (Table 1). Two separate replicas were taken for chemical-physical and foraminiferal analyses. The two replicas generally had different length, due to the difficulty of sampling by hand the sandy sediment in the sub-marine environment.

Granulometric parameters, heavy metals (Al, As, Cd, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Zn), 15 PAHs and PCBs were determined for all the samples. Samples for grain-size analysis were treated with a 30% H2O2 solution and separated by wet sieving. The > 0.063 mm fraction was dried and fractionated by ASTM series sieves, while the lower fraction was analysed by X-ray sedigraph (Romano et al., 1998). They were classified according to Shepard (1954).

Heavy metal analyses were performed on aliquots of whole homogenised sample and analysed by Atomic Absorption Spectrometry according to Giani et al. (1994).

Analyses of PAHs were performed by a preliminary extraction and successive purification on silica gel; the determination by high performance liquid chromotography with spectrofluorimetric detector was carried out (Ausili et al., 1998). Determinations of PCBs were by preliminary extraction and subsequent purification by Florisil®. The determination was carried out by ECD gas chromatograph.

For foraminiferal analyses, the seven cores were divided into 5 cm thick (F1, H4, T1) or 3 cm thick (F3, G4, R1, T3) samples (bottom samples were thicker in some cases). The samples were washed through 125 μ m screen and dried at 40°C. All samples were subjected to qualitative analysis. Quantitative analysis was performed only on three cores (G4, H4, T3) in which the faunal density was sufficiently high. Samples from these cores were split into fractions containing about three hundred specimens, which were picked and identified following the generic classification of Loeblich and Tappan (1988).

The results of the quantitative analyses were subjected to statistical analyses using the program SPSS version 10.1. Q-mode Hierarchical Cluster Analysis (HCA) was performed on samples in which at least 300 benthic specimens were counted in the > 125 μ m fraction. The original matrix included the 123 species recognised in all the samples of cores G4, H4 and T3. Given the high number of species identified, it was necessary to reduce the number of variables in order to obtain a significant statistical analysis. In order to simplify the matrix, some species were grouped on the basis of their taxonomy, when they had homogeneous environmental significance (e.g., Bulimina spp., Quinqueloculina spp.) so that only species or groups more abundant than 10% in at least one sample were considered for the statistic analyses. For HCA, distance is given in percentage by the Euclidean equation, while the similarities of the new fused clusters are calculated with the Average Linkage method (within group), the most widely used in statistical ecology (Pielou, 1984; Parker and Arnold, 1999).

For each sample, species diversity was quantified through the α -index (Fisher et al., 1943) and benthic productivity was estimated through the Benthic Number (BN) > 125 μ m (i.e., the number of foraminifers counted in 1 g of dry sediment > 125 μ m), as reported in Coccioni (2000).

Results

Grain-size and chemical data

The cores were mainly constituted of sand; in cores F3 and H4 there were significant percentages of fine fraction (silt + clay). In both these cores, a decrease in the sandy fraction from top to bottom was recorded (Figure 2).

Polycyclic aromatic hydrocarbon concentrations recorded in the present study were high, if compared with the Mediterranean values reported by UNEP (1996). In particular, very high values were found in some levels of the F1 and F3 cores (Table 2). They probably correspond to casual and local episodes because no correspondence was found in neighbouring cores.

The PCB concentrations were in the range of Mediterranean coastal areas subjected to antrophic impact (UNEP, 1996). In spite of this, such values may be considered medium-high in relation to the grain-size of sediment samples (Table 2). In cores F1, H4 and R1 high values were recorded in the top samples, decreasing towards the bottom of the core. Low values are present in the cores T1 and T3.

The heavy metals analysed, Cd, Cu, Hg Pb and Zn showed high values, if compared with average values for Mediterranean and Tyrrhenian areas (UNEP, 1996; Romano et al., 1998). The highest concentrations were located in the marine area in front of the industrial site (Table 2). In particular, Cu, Hg and Cd showed ‘spot’ distribution, while Fe, Pb, Zn and Mn had a more regular distribution, with decreasing values from the plant to the open sea (Romano et al., 2004). The highest Cu concentration occurred in core T1; cores F1, F3 and R1 show the highest Fe contamination, while cores H4 and R1 show the highest Zn contamination.

Benthic foraminiferal data

We identified 123 foram species: 3 Textulariina, 20 Milioliina and Rotaliina. Cores F1, R1 and T1 were completely barren of benthic foraminifers. All samples of core F3 contained a few tests per gram of such species as Quinqueloculina seminulum, Q. dimidiata, Ammonia parkinsoniana and Neoconorbinaterquemi, but it was impossible to carry out a quantitative analysis. Nevertheless, the topmost sample seemed slightly richer in foraminifers than those further down.

Foraminifer data from cores G4, H4 and T3 were subjected to HCA (Figure 3). In the dendrogram, each cluster included samples with similar assemblages corresponding to somewhat homogeneous ecological conditions. The dendrogram shows that, with rare exceptions, the three main clusters represented the three cores; cores H4 and T3 show little similarity, while core G4 seems somewhat related to the other two.

Samples of core H4 showed a high degree of similarity, marked by low values of Euclidean distance, and contained an assemblage dominated by Quinqueloculina spp. (mainly Q. dimidiata and, secondarily, Q. parvula and Q. bosciana). Among the Milioliina, Miliolinella subrotunda was steadily abundant at the 8 to 10% range. Among the Rotaliina, Tretomphalus concinnus and Haynesina depressula were also abundant. The presence of Bulimina aculeata (up to 14%), a typical species of fine sediments, was significant. Only the bottom sample was slightly different from the other ones, due to the lower percentages of Bulimina aculeata and Tretomphalus concinnus and higher values of Haynesinadepressula. Species diversity in core H4 was very high (α -index: 30–42). As well, faunal abundance was rather high (BN > 125 μ m: 644–2325), with the maximum value corresponding to the topmost sample (Table 3). All specimens had a reduced mean size and many tests of Miliolina appear to be transparent, that is, not well calcified. The number of deformed tests was never high (1.40–3.74% of the entire assemblage). Those present belonged primarily to Miliolinella subrotunda. The irregularity consisted mainly in an incomplete or irregular development of the last chamber. The inorganic fraction of the sediment contained several irregular iron grains derived from the Bagnoli steel plant activity.

In the HCA, the G4 core was almost entirely grouped at a high hierarchic level with the H4 core, because in both cores Quinqueloculina spp. (mainly Q. dimidiata) was dominant with similar abundances and Haynesina depressula showed comparable values. In the assemblage of the G4 core Elphidium advena (up to 27%), Buccella granulata (up to 18%) and Lobatula lobatula (up to 11%) were also frequent. Faunal abundances were extremely low (BN > 125 μ m: 7.5–28.89) in all the samples. High species diversity was shown by high α -index values (15.39–28.97), with the highest ones corresponding to the top and the bottom of the core (Table 3). Neither parameter showed a distinct trend in relation with the depth of samples in the core. Generally, species are represented by rather small specimens; the number of aberrant tests does not exceed the natural background. Nonetheless, many specimens of Elphidium advena showed a slightly irregular test, mostly derived from the anomalous size of one or more of the last chambers. The inorganic fraction of the sediment was rich in antrophic grains, mostly coal grains and iron dross.

In the T3 core, all samples were dominated by Elphidium advena (19–46%), a typical species of infralittoral sandy bottoms and byBuccella granulata (6–15%). Quinqueloculina spp. (5–24%; mainly Q. dimidiata and Q. annectens) was abundant especially in the higher core levels, while Lobatula lobatula was more frequent in the lower part of core. The α -index covered a wide range of values (14–30), similar to those of core G4; the benthic number, on the contrary, was extremely low (8.46–22.5) and rather constant (Table 3). All species were represented by small specimens; the deformed species never exceeded 3% of the assemblage. Nevertheless, the major part of these belonged to Elphidium advenam many of whose tests were more irregular than deformed. Deformed Elphidium advena reached 16% in the top sample, but were less than 5% in the three lowermost samples (21–24; 24–27; 27–30). The inorganic fraction of sediment was less rich in antrophic iron and coal compared to the other cores.

Discussion

Since the Q-mode CA singled out clusters mainly corresponding to a single core, it may be inferred that foraminiferan assemblage variability is associated with spatial changes, rather than temporal changes of the environmental parameters. It is likely that, the sediment content in fine fractions is the most important factor determining the assemblage composition. Cores G4 and H4 (grouped in the same cluster, Figure 3), contained a significant percentage of fine sediments (Figure 2), while core T3, fairly distant from the other cores in the CA, was almost exclusively constituted of sand. With respect to temporal changes of the benthic assemblage, core H4 showed a rather constant composition; core G4 did not show distinct trends in faunal changes, and core T3 showed slight differences between the lower and the upper portion. Consequently, HCA does not show the important faunal shift that could result from a supposed environmental transition from natural to polluted conditions (Alve, 1991a, b). Such a deduction is confirmed by analyses of pollutants. Heavy metals, PCB and PAHs did not reveal a clear decreasing trend with increasing depth. The high concentrations of PAHs, localised in some levels of core F3, may not be correlated with the modifications on foraminiferal assemblages because in this core foraminifers were not present. The recorded PCBs concentrations (up to about 120 ng g−1 d.w.) did not seem to affect foraminiferal abundance. The low faunal abundance or the complete absence of foraminifera in some cores could be attributed to high metals pollution (Alve, 1991a, b; Yanko et al., 1994; Samir and El Din, 2001) if natural causes could be excluded. The high sedimentation rate recorded in the study area by Sharp and Nardi (1987) could have caused a dilution of tests in the sediments, corresponding to a decrease of the BN. In spite of this, it is reasonable to suppose that the high differences in foraminiferal abundance recorded in cores G4, H4 and T3 may not be explained by large differences in the sedimentation rate in the study area, because it is smaller than 1 km2. It is likely that the combined high concentrations of more than one metal (particularly Cu and Fe) are responsible for the absence of foraminifera in F1, F3, R1 and T1 cores. However, high Zn contamination (up to 2300 mg kg−1 d.w.) recorded in core H4 did not seem to influence foraminiferal abundance.

The presence of irregular tests may have natural causes, that is, environmental stress due to hypo/hyper salinity or strong hydro dynamism (Geslin et al., 2000). We can exclude that the significant presence of irregular Miliolinella subrotunda and Elphidium advena found in this work is naturally driven, because there is no fresh-water contribution in the study area and no widespread signs of mechanical trauma were observed on the tests. Alve (1991a) noted that the normal rate of abnormal specimens in a non-stressed population is about 1% (calculated on the entire assemblage). In laboratory cultures of Ammonia under normal conditions, 1% of abnormalities was observed (Stouff et al., 1999). Consequently, since the percentage of irregular Miliolinella subrotunda was significantly high in H4 core and that of Elphidiumadvena was high in G4 and T3 cores, the cause of this phenomenon could be attributed to one of the analysed heavy metals.

The percentages of irregular Miliolinella subrotunda were compared with the concentrations of Cu in H4 core. Although the range in Cu concentrations was small, it is evident from Figure 4 that trends of the two graphs are similar even though the intervals sampled for chemical and foraminifers analyses are different. It was not possible to perform a similar comparison with the G4 core because only two intervals were analysed for trace metals. Likewise, the abundance of irregular specimens of Elphidium advena in core T3 shows the same trend with respect to Cr, Mn and Zn concentrations (Figure 5).

Acknowledgments

The authors thank Dr. S. Focardi for determination of PCBs, Dr. A. Schiavetti and R. Spaziani for trace metals analyses, Dr. S. Rossi and G. Ciuffa for PAHs determination. The authors are grateful to Dr. G. Cavarretta, Director of IGAG (CNR), for the use of SEM and to Mr. A. Mancini for the technical assistance in SEM photographs.

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