Suitable sediment fraction for paleoenvironmental reconstruction and assessment of contaminated coastal areas based on benthic foraminifera: A case study from Augusta Harbour (Eastern Sicily, Italy)

Ecological Indicators 71 (2016) 66–78

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Suitable sediment fraction for paleoenvironmental reconstruction and assessment of contaminated coastal areas based on benthic foraminifera: A case study from Augusta Harbour (Eastern Sicily, Italy) Luisa Bergamin, Elena Romano ∗ ISPRA, Institute for Environmental Protection and Research, Via di Castel Romano, 100, 00128 Rome, Italy

a r t i c l e

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Article history: Received 12 February 2016 Received in revised form 14 June 2016 Accepted 15 June 2016 Keywords: Benthic foraminifera Sediment core Foraminiferal size Contaminated sediments Environmental assessment

a b s t r a c t Since the 1990s several studies noticed that, along coastal marine areas, the mean size of benthic foraminifera may be reduced due to heavy metal pollution, even if no biometric studies were carried out to quantify this aspect. The Augusta harbour (Sicily, Italy), is characterized by a strong contamination due to several anthropogenic activities, the most important of which are a petrochemical pole and an important industrial harbour. Taking into account the previous studies carried out in the area, which recorded small-sized foraminifera, the present study compared assemblage composition and faunal parameters in the >125 ␮m and >63 ␮m fractions of a sediment core collected in the most polluted sector of Augusta harbour. The aim was to understand if the two fractions have comparable environmental significance providing reliable information on the environmental status. In order to quantify the amount of smaller foraminifera in a community and to determine species loss between size fractions, two new indices are used: the Foraminiferal Size Index (FSI) and the Lost Species Index (LSI). Species richness, diversity and composition of the two assemblages were determined to characterize their structure. The results highlighted great depletion and different composition of the >125 ␮m assemblage with respect to the >63 ␮m one, showing a selective loss of particular ecological groups (stress-tolerant infaunal taxa). Also the better correlation of Foraminiferal Number (FN) and H’ index of >63 ␮m fraction with Polychlorobiphenyls (PCBs), Polycyclic Aromatic Hydrocarbons (PAHs), Barium (Ba) and Mercury (Hg), demonstrated the higher reliability of this size fraction for environmental assessment purposes. © 2016 Elsevier Ltd. All rights reserved.

1. Introduction Benthic foraminifera are widely considered for paleoenvironmental and environmental purposes, and recent foraminifera have been increasingly used as environmental indicators for the assessment and monitoring of marine environments (Nigam et al., 2006; Frontalini and Coccioni, 2011). They are particularly suitable for this application due to the high number of specimens present in a small volume of sediment, which allows a solid statistical data processing. Besides, they respond to natural and anthropogenic environmental changes with a rapid faunal turnover, which may be highlighted by the change of quantitative faunal parameters. Another important aspect to be considered is the size of tests in the studied assemblages, because they may be affected by adverse

∗ Corresponding author. E-mail address: [email protected] (E. Romano). http://dx.doi.org/10.1016/j.ecolind.2016.06.030 1470-160X/© 2016 Elsevier Ltd. All rights reserved.

effects of contamination in the sediments, which may determine the presence of stunted specimens. The matter of the size fraction in the analyses of benthic foraminiferal assemblages is essential to achieve reliable results, because the ecological significance of the studied assemblages should reflect as much as possible the environmental conditions in which they lived. At present, it is not clear which are the main environmental factors influencing the size of benthic foraminifera and apparently conflicting indications are available from literature. According to some studies, small size may be indicative of early reproduction under favourable conditions such as abundant food (Diz et al., 2006). Nevertheless, also unfavourable conditions, such as lowoxygen availability (Nagy et al., 2010) or anthropogenic pollution (Yanko et al., 1994; Samir and El Din, 2001; Romano et al., 2008), may produce undersized assemblages. In order to verify which are the size fractions, generally used by researchers in the ecological studies, a survey of ISPRA database, including 165 articles published since 1991, was car-

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Fig. 1. Studied foraminiferal size fraction according to the Foraminiferal Method Database (http://www.bonifiche.isprambiente.it/forams/index.php). N.I. = Not Indicated.

ried out (www.bonifiche.isprambiente.it/forams/index.php). The review highlighted that, although most researchers use the >63 ␮m fraction (59%), also coarser size fractions, such as >125 ␮m and >150 ␮m, are considered in the 18% and 8% of articles, respectively (Fig. 1). In this study, the two most commonly used fractions (> 125 ␮m and >63 ␮m) were considered. There are both advantages and disadvantages in using each of these size fractions. The >63 ␮m one includes nearly the totality of foraminiferal tests (Schröder et al., 1987), although the foraminiferal analysis takes considerable time in the classification of small species and juvenile specimens (Duchemin et al., 2007; Foster et al., 2012). This aspect is important while processing a lot of samples with close deadlines. On the other hand, the >125 ␮m fraction should generally include most individuals, because smaller benthic foraminifera size commonly range from 100 to 500 ␮m. The preference of researchers for this fraction is generally due to the time saved for handling and classifying larger specimens. However, Scott et al. (2001) reported cases of deep-water samples in which up to 99% of the individuals may be lost by studying the >125 ␮m fraction instead of the >63 ␮m one. Schröder et al. (1987) found that the use of fractions >125 ␮m implied a considerable loss of specimens which determined “artificially barren zones in sequences dominated by small-sized species”. Sen Gupta et al. (1987), who studied both Caribbean and Arctic deep-water samples, found that the use of the >250 ␮m fraction changed considerably the proportion of dominant species and, consequently, the ecological significance of the assemblages. In the perspective of environmental studies, the different size fraction used is really important because it influences the number of species, the foraminiferal density and the assemblage composition, all indicative features of environmental quality. In particular, the assemblage composition and its ecological significance may be influenced by the size fraction because the opportunistic species can be more abundant in the finer fractions (Kitazato et al., 2000; Duchemin et al., 2007). Some studies compared quantitative results of different size fractions in recent foraminiferal assemblages, from areas not affected by specific anthropogenic impact. Bouchet et al. (2012) considered diversity indices obtained from the >125 ␮m fraction and the one comprised between 63 and 125 ␮m, as equally representative of the ecological status, because both correlated with

dissolved oxygen at bottom-water interface. However, Schönfeld et al. (2013) recognized that diversity indices showed a considerable decrease with increasing mesh size and that only half of the living specimens were retained in the >125 ␮m fraction. No similar studies are known in areas affected by intense industrial contamination where there is a higher chance to find small benthic foraminifera than in unpolluted sites (Yanko et al., 1994; Coccioni et al., 1997; Samir and El Din, 2001; Romano et al., 2008). Biotic indices, based on ecological groups of benthic macrofauna with different tolerance degree, and finalized to the quantification of marine ecological status, have been developed since 2000 (Borja et al., 2000; Simboura and Zenetos, 2002; Borja et al., 2009). Pollution index, based on the abundance of indicative stress-tolerant species, have been provisionally used also for benthic foraminifera (Mojtahid et al., 2006; Jorissen et al., 2009; Barras et al., 2014; Dimiza et al., 2016). This conceptual model is being approached also by the FOBIMO initiative for biomonitoring marine coastal zone by means of living benthic foraminifera (Schönfeld et al., 2012). The use of biotic indexes may be applied not only for living foraminifera, but also for temporal reconstruction of environmental quality changes in core sediments, due to anthropogenic impact. In recent years, the study of foraminifera from sediment cores collected in contaminated areas, was widely applied to reconstruct level and changes of environmental status during the last decades (Cearreta et al., 2002, 2008; Hayward et al., 2004; Scott et al., 2005; Caruso et al., 2011; Dolven et al., 2013; Francescangeli et al., 2016; among the others). The advantage of using these organisms as ecological indicators in the environmental reconstruction is that, differently, for example, from benthic macrofauna, a high number of specimens may be present in a thin level of core, providing quantitative data suitable for statistical approach. Moreover, due to their mineralized tests, the assemblage may be preserved in the sedimentary record, although post-mortem processes altering the original biocenosis must be taken into account. Consequently, deeper core levels may include assemblages referable to pre-impact conditions. The identification of reference conditions is essential because quality assessment is based on the degree of deviation of current environmental status from the reference one. The environmental recovery after remediation action is also detectable in sediment cores by means of benthic foraminifera (Alve et al., 2009). Although most studies on sediment cores, aimed to environmental reconstruction, used the >63 ␮m fraction, also finer (Debenay

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and Fernandez, 2009) and coarser fractions (Elberling et al., 2003; Nomura and Kawano, 2011; Dijkstra et al., 2013), were considered. However, a reasoned explanation for this choice was not given. The present study considers benthic foraminifera from a sediment core, collected in the Augusta harbour, where a large petrochemical pole is working and a strong sediment pollution, mainly due to Mercury (Hg) and Polychlorobiphenyls (PCBs), was recorded (Sprovieri et al., 2011; Romano et al., 2013; Croudace et al., 2015). A previous research on recent foraminifera from the same area, highlighted the presence of specimens smaller than normal, but no quantitative approach was applied (Romano et al., 2009). For this reason, before starting a research on the same core finalized to paleoenvironmental assessment (Romano et al., 2015), a preliminary study about the best sediment fraction to use in the ecological characterisation was carried out and it is the object of the present paper. The study of benthic foraminifera from the >63 ␮m fraction allowed to recognize three distinct ecozones along the core, strictly correlated with Barium (Ba), Hg and PCBs, especially in terms of faunal diversity and abundance (Romano et al., 2015). Aim of the present research is to evaluate the differences of the foraminiferal assemblage obtained from the >63 ␮m and >125 ␮m fraction regarding diversity, density and composition and, consequently, ecological significance. The finer fraction was considered as conservative, with respect to ecological information, because it contains nearly all the specimens effectively present in the sediment. The >63 ␮m fraction was considered by Alve and Goldstein (2002, 2010) as the suitable fraction to detect the development of foraminiferal specimens from the propagule stage. In order to quantify this comparison in terms of different number of specimens contained in the two fractions, the Foraminiferal Size Index (FSI), which is the rate between smaller (63–125 ␮m) and larger (> 125 ␮m) foraminifera, introduced by Romano et al. (2015) was determined. Moreover, the Lost Species Index (LSI), which is descriptive of the number of species not present in the >125 mm fraction due to smaller size, was applied for the first time in this study. In this study, a quantitative and comparative analysis of benthic foraminifera from the coarser fraction and the finer one will look for a correspondence of environmental features. If such correspondence would be observed, then the coarse fraction could offer consistent information regarding the environmental status, with the advantage of faster and easier quantitative analysis. The ultimate goal is to offer reliable indications to the researchers interested in investigating temporal changes of environmental status in sediment cores (fossil assemblages) from chemically polluted areas, characterized by small-sized benthic foraminifera.

2. Study area The Augusta harbour is part of a natural bay, located in the eastern coast of Sicily (Italy), closed by dams in the early 1960s and connected with the open sea by the western and southern inlet (Fig. 2). The sheltered area is about 24 km2 and the average water depth is about 15 m, with the maximum depth, of around 40 m, located in correspondence of the western inlet, while it is less of 20 m from the piers to the coast (Feola et al., 2016). The NW sector of the harbour is influenced by the seasonal outflows of the Mulinello, Marcellino and Cantera streams. Their contributions are generally poor and with very localized hydrodynamic effects (Lisi et al., 2009). Romano et al. (2013), who studied the distribution of recent benthic foraminifera in the whole harbour, recognized foraminiferal assemblages referable to freshwater contributions, only localized very close to the stream mouths. The mean current speed at the bottom layer is lower than 0.05 m/s in the most part of the harbour,

while the highest values, above 0.5 m/s, were recorded during the winter season, close to the dams and the coast (Feola et al., 2016). The harbour is affected by high degree of contamination due to the presence of a large petrochemical pole, which started up in the early 1950s, including mainly oil refineries, petrochemical industries and electric power plants, which affected the environmental quality of the marine area. During the 1960s a fast industrial development made it the largest industrial petrochemical site in Europe. Even though some activities have ceased their production since the 1970s, several important plants are still operative. Sediment contamination has become the most important element of environmental concern since 1970s, when high content of industrial pollutants, such as hydrocarbons and heavy metals, were found in the harbour sediment (Sciacca and Fallico, 1978). Recent studies, finalized to recognize vertical and spatial distribution of heavy metals and organic compounds, highlighted exceptionally high concentrations of Hg (up to 191 mg/kg d.w.) and PCBs (up to 0.8 mg/kg d.w.) in the in the superficial sediments of southern coastal area and higher concentrations in the deeper ones (ICRAM, 2008; Romano et al., 2013; Croudace et al., 2015). Such contamination was mainly attributed to the activity of a chlor-alkali plant, which was operative from 1958 to 2003 using a mercury cell technology. Romano et al. (2015) found in the sediment core, used for the present study, very high concentrations of Ba, Hg and PCBs, up to 5708, 680 and 22.9 mg/kg d.w., respectively. The highest concentrations correspond to the period of the highest activity of the factory, between 1960s and 1980s. The most remarkable decrease of contamination level was recorded in the upper 15 cm of the core, corresponding to the 2002–2008 time interval, after the closure of the chlor-alkali plant. The area was also demonstrated to be an important contributor for Hg in the Mediterranean Sea basin, with an Hg output of 0.162 kmol/y to coastal and offshore waters (Sprovieri et al., 2011).

3. Material and methods A sediment core (AU10) of 127 cm length was collected in July 2008 at 10 m water depth in the southern part of the harbour, close to the coast and the industrial area (Fig. 2), using a gravity corer (mod. SW104). A total of 20 samples having 3 cm thick were subsampled: the first 10 were collected in the upper 30 cm of the core, to guarantee the highest resolution of more recent times; more 10 samples were taken below this depth with an interval of 9 cm, to detect the main environmental changes in previous times. Sediment samples were used for the analysis of benthic foraminifera and for grain size and chemical analyses, which results are described in Romano et al. (2015). In addition, for this study, sediment samples were wet-sieved using two different sieves (63 ␮m and 125 ␮m) in order to obtain the two size fractions (> 125 ␮m and >63 ␮m, including the >125 ␮m fraction), and then oven dried at 40 ◦ C. The quantitative analysis was carried out separately on the two fractions and all the foraminifera of each sample (or in a representative split) were counted and classified. Only well-preserved tests, with no breakages or abrasion signs indicating transport or reworking, were picked, counted and classified. Microfaunal analysis was conducted by means of stereomicroscope Leica mod. M165C. Classification, at genus level, was made according Loeblich and Tappan (1987), while species were determined according to major studies relative to the Mediterranean area (Jorissen, 1988; Cimerman and Langer, 1991; Sgarrella and Moncharmont-Zei, 1993) and to the World Modern Foraminifera Database (Hayward et al., 2011). The Foraminiferal Number (FN) was calculated as the number of specimens per gram of dry sediment (specimens/g) according to

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Fig. 2. The Augusta harbour (Eastern Sicily): sampling site.

Schott (1935). The species diversity was measured considering the species richness (S), the Fisher ␣-index (Fisher et al., 1943; Murray, 1991) and the Shannon index (H’) (Shannon, 1948), as well as the dominance D = 1-Simpson index (Hammer et al., 2001; Hammer and Harper, 2006). The number of specimens used for the deter-

mination of diversity indices were always above 100 (up to 554) in the >63 ␮m fraction, according to the indications of Fatela and Taborda (2002), while they were less abundant in the >125 ␮m one, where only samples with more than 50 specimens were considered for statistical purposes, according to Barras et al. (2014). In

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Fig. 3. Box-plot of absolute abundance of the 20 most numerous species for the >63 ␮m and >125 ␮m fraction.

order to compare species diversity and dominance in the >63 ␮m and >125 ␮m fraction, the rate between the values of H’-index (H’rate), ␣-index (␣-rate) and D (D-rate) were determined. The Principal Component Analysis (PCA) was applied to the two assemblages, using a matrix including species >5% in at least one sample, in order to highlight different species distribution. All statistical analyses and diversity indices calculations were carried out by means of PAlaeontological STatistics – PAST ver. 2.17 (Hammer and Harper, 2006). In order to quantify the abundance of small foraminifera and the effects of the size on assemblage features, a Foraminiferal Size Index (FSI) and Lost Species Index (LSI) were proposed and determined. The FSI is considered as the rate of smaller foraminifera with respect to the larger ones in a sample (FSI = N63-125 /N > 125 ; N63-125 = number of specimens with a size between 63 and 125 ␮m; N > 125 = number of specimens with a size above 125 ␮m). The LSI is considered as the % of species exclusive of the >63 ␮m fraction.

4. Results 4.1. Assemblage composition and structure A total of 121 species was found in the assemblage >63 ␮m (hereinafter cited as 63-assemblage), while 102 species were recognized in the assemblage >125 ␮m (hereinafter cited as 125assemblage), with an overall percentage of lost species in the coarser fraction of 18%. Juvenile specimens were practically absent not only in the 125-assemblage, but also in the finer one. Excluding very sporadic taxa, which showed no more than 5 specimens, some rather abundant species were found exclusively in the 63assemblage: Gavelinopsis praegeri (88 specimens), Epistominella vitrea (54 specimens), Globocassidulina subglobosa and Hopkinsina pacifica (18 specimens) and Lagena striata (17 specimens). The 20 most abundant species in the >63 ␮m and >125 ␮m fractions were considered and box-plot diagrams, illustrating basic statistics of their absolute abundance, were drawn (Fig. 3). It may be observed that in both cases, considering median values, the most abundant species is Miliolinella subrotunda, an herbivore epifaunal taxon (Murray, 2006) which was recognized as tolerant for heavy metal polluted sediments (Romano et al., 2008, 2009). Five herbivore epifaunal species (Neoconorbina posidonicola, Triloculina plicata, Elphidium granosum, Planorbulina mediterranensis and Quinqueloculina seminulum), living on plants or sediments (Murray,

Table 1 Basic statistics of species richness (S), ␣-index, H’-index and dominance (D) in the 63 and 125-assemblage.

Taxa S 125 Taxa S 63 Fisher ␣ 125 Fisher ␣ 63 Shannon H’ 125 Shannon H’ 63 Dominance D 125 Dominance D 63

Min

Max

Mean

SD

10 35 9.7 11.6 2.3 3.1 0.05 0.04

45 59 53.3 19.6 3.4 3.5 0.12 0.08

26 47 19.5 15.0 2.9 3.3 0.07 0.05

9 6 10.0 2.4 0.3 0.1 0.02 0.01

2006), are exclusive of the 125-assemblage. On the other hand, six species (Bolivina earlandi, B. aenariensis, B. pseudoplicata, Quinqueloculina stelligera, Q. subpolygona and Elphidium advenum), mostly detritivore infaunal species, are exclusive of the 63-assemblage. Bolivina species are nearly absent in the coarser fraction, while they represent the most abundant genus in the finer one. A considerable number of species was recorded in both assemblages even if the higher S value was recorded in the 63-assemblage, because this fraction includes the 125-one. High values of the H’ index, not significantly different between them, were recorded in both assemblages (Table 1). Conversely, the ␣-index shows lower mean values in the finer assemblage than in the coarser one (mean 19.5), even if a considerable standard deviation is present in the 125-assemblage. Dominance, which is generally low, is rather similar in the two assemblages. The FN is characterized by very different values for the 63 and 125-assemblages, ranging between 0 and 1930, and 0 and 729, respectively. The pattern of FN values along core-depth is, in general, similar for the two fractions: considerably high values in the upper part of the core, equal or close to 0 in the intermediate interval, very low values in the samples close to the bottom. However, in the upper part of the core, the FN recorded considerably higher values in the 63-assemblage than in the 125one. In the intermediate barren interval, the thickness is smaller for the fine fraction (82.5–85.5 cm) and larger for the coarse one (64.5–91.5 cm) (Fig. 4). As an example, the plot along the core-depth of the absolute abundance of the most frequent species, M. subrotunda, considering different size fractions, was drawn (Fig. 5). It may be observed that the great majority of specimens have a size comprised between 63 and 125 ␮m in all the samples.

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Fig. 4. Foraminiferal Number (FN = specimens/g dry sediment) in the >63 ␮m and >125 ␮m fraction plotted along core-depth.

4.2. Faunal parameters for size evaluation The FSI shows a wide range of values, comprised between 1.3 and 13.5, to indicate that smaller foraminifera always prevail on the larger ones and that, sometimes, they are nearly exclusive. Similarly, LSI has a wide range of values (19.6%–71.4%) showing that a large number of species is lost in the 125-assemblage. The core profiles of FSI and LSI display highly similar patterns, characterized by low values in the lower part of the core (Fig. 6). The highest values are recorded between 28.5 and 46.5 cm, while a decreasing trend is recognizable in the upper levels. The H’-rate shows values ranging from 1.03 to 1.42, indicating a slightly more diverse 63assemblage than the 125-assemblage, with a similar profile to the FSI and LSI ones. The value range of ␣-rate is wider and comprised between 0.27 and 1.26. Most samples show values <1 indicating that higher values are more frequent in the 125-assemblage. This means that, in most cases, the 125-assemblage is characterized by a higher number of species in relation to the number of counted specimens. The pattern of ␣-rate is opposite to H’-rate one from 28.5 and 55.5 cm, while above the two profiles are very similar. The D-rate has a vertical profile with an opposite pattern with respect to H’-rate. It ranges between 0.41 and 1.07 and values are <1 in almost

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Fig. 5. Plot along core-depth of the most abundant species, M. subrotunda. Absolute abundance in the 63-assemblage is reported together with the abundance in the two size categories (63–125 ␮m and >125 ␮m).

all levels to point out higher values in the coarser assemblage. This points out that a worse distribution of individual among species is recognizable in the 125-assemblage. 4.3. Principal component analysis Scatter plots of PCA, applied to 63 and 125-assemblage, are shown in Figs. 7–8. In both cases three distinct groups are recognizable. Group 1 loads on the negative side of the first axis and includes samples of the lower part of the core (up to 99–102 cm). About the 63-assemblage, this group includes also two samples above the barren interval, up to the level 36–39 cm. These samples are characterized by the same taxa in the two assemblages: Asterigerinata mamilla, Rosalina spp., Lobatula lobatula and Sigmoilinita costata. Group 2 loads mainly on the positive side of the second axis and includes samples belonging to the intermediate part of the core, above the barren interval. In the 63-assemblage the interval includes levels from 54–57 cm to 18–21 cm, while the 125one displays a shorter interval, ranging from 24 to 18 cm. Species referable to this group are, in the 63-assemblage, Cornuspira involvens, Miliolinella spp. Quinqueloculina lata and Q. Stelligera, while Q. seminulum characterizes the 125-assemblage. Moreover, Spiril-

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Fig. 6. Size parameters (FSI, LSI, H’-rate, ␣-rate and D-rate) plotted along core-depth.

Fig. 7. Principal Component Analysis on >63 ␮m fraction. Component 1 and 2 account for 32% and 27%, respectively.

lina vivipara strongly characterizes samples of group 2 only in the 63-assemblage. Finally, the upper core levels (from 18 cm to the top) load on the negative side of the second axis in both assemblages (group 3). Taxa characterizing this core interval are almost the same for the two assemblages (Ammonia spp., Bulimina spp. and Haynesina depressula) with the exception of Bolivina species which are absent in the 125-assemblage. Q. lata characterizes samples of this interval only in the 125-assemblage. 5. Discussion In this study, it was necessary to select a core that would reflect a gradient of historical environmental degradation, caused mainly

by chemical pollution, where identifying the best size fraction for environmental reconstruction and assessment based on benthic foraminiferal assemblages. Core AU10 represented the best choice because it was located in the most polluted sector of the harbour, where the highest abundance of small-sized foraminifera was highlighted by Romano et al. (2009, 2013). These studies, mostly the last one, demonstrated that inside the harbour there is an increasing gradient of contamination levels, from the North to the South, in relation to the increasing of impact due to industrial activities. The integrated environmental reconstruction and assessment, based on benthic foraminiferal assemblages and abiotic sediment parameters of core AU10, like as grain size, Ba, Hg, PAHs and PCBs, was carried out by Romano et al. (2015), using the >63 ␮m fraction for

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Fig. 8. Principal Component Analysis on >125 ␮m fraction. Component 1 and 2 account for 46% and 21%, respectively.

Fig. 9. Plot along a double scale, core-depth, and age of PAHs, PCBs, Ba, and Hg concentrations and foraminiferal number (FN). The distribution along the core of ecological zones is also given (Romano et al., 2015).

foraminiferal study. The information obtained by the integrated reading of foraminiferal and abiotic parameters may be helpful for interpreting the features of foraminiferal assemblages of the different fractions, object of the present research. Sediment texture does not show dramatic changes along depth, and silt is the prevailing fraction, with a mean value of 53%, while clay and sand have a mean of 22 and 25%, respectively. Exceptionally high contamination levels, mostly due to Hg, but also to PCBs and Ba, were recorded in all the levels of the core, with the highest concentrations from 35 cm to the core bottom; this interval correspond to the timing range from early 1960s to about 1995, the period of maximum activity of the chlor-alkali plant (Fig. 9). A foraminiferal assemblage with low diversity and very low density, dominated by

Rosalina spp. and M. Subrotunda, was found in this interval, that is characterized by very high concentration of Hg and PCBs and it is interrupted by a barren section (60–95 cm), where the highest concentrations were recorded (Hg > 500 mg/kg d.w.; PCBs > 7.5 mg/kg d.w.). Successively, contaminant levels started to decrease in correspondence of an assemblage with increased diversity and density, characterized by M. subrotunda and S. vivipara. The decrease of contamination levels was more evident in the 2000s, after the enclosure of the chlor-alkali plant, when an assemblage with the very high foraminiferal density and high species diversity, characterized by Bolivina seminuda (B. earlandi in this paper) and M. Subrotunda, is present. The FN was found negatively correlated (Spearman ␳) to all the main contaminants as well as the H’ index, to

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confirm the reliability of foraminifera from the >63 ␮m fraction, as environmental indicators in core AU10. The good correspondence of faunal and abiotic sediment data, indicates that post-mortem processes did not modify significantly the foraminiferal assemblages which consequently may be considered as reliable indicators of the environmental status. This study considered the limits of 63 ␮m and 125 ␮m for foraminiferal size because these are the most commonly used in the study of benthic foraminifera. The absence of juvenile specimens in the 63-assemblage of studied core, let us suppose that they were lost in the sieving phase. According to Alve and Goldstein (2002, 2010), the <63 ␮m fraction includes propagules which may be dispersed due to physical processes and, for this reason, it is not significant for environmental assessment. Consequently, the size of 63 ␮m may be considered the best choice for these purposes. The comparison of foraminiferal data with the >125 ␮m one is finalized to understand if the study of the coarser fraction is adequate to obtain reliable information on environmental status. Significant differences were observed in the composition of the 63 and 125-assemblage. The Bolivina genus strongly characterizes the 63-assemblage because it is the most represented, while it is absent from the 20 most abundant species of the 125-assemblage (Fig. 3) due to their small size (Schröder et al., 1987). They are detritivore infaunal taxa and are traditionally considered as opportunist species (Jorissen et al., 2009; Martins et al., 2013). Also most species, exclusive of the 63-assemblage (E. vitrea, G. subglobosa, H. pacifica and L. striata), are detritivore infaunal species associated to fine, organically-enriched sediments (Murray, 2006). Consequently, the use of 125-assemblage implies the loss of the ecological information given by the infaunal stress-tolerant taxa. These results highlight how the loss of detritivore opportunistic taxa, deriving from the use of coarse fraction, would led to higher values for biotic indices based on relative abundance of stress-tolerant/sensitive taxa and, consequently, to higher evaluation of environmental status of the Augusta sediments. Foraminiferal density may be considered as another descriptor of environmental quality. In case of organic matter pollution, the number of specimens mainly represented by opportunistic taxa may considerably increase due to the consequent raise of food availability. At the same time, the consumption of organic matter may determine persisting anoxic conditions with consequent foraminiferal desertion (Alve, 1995). Differently, strong chemical pollution leads to a decrease of foraminiferal abundance until their total disappearance (Bergamin et al., 2005; Ferraro et al., 2006). The correlation between foraminiferal abundance and contaminant concentration was recognized for superficial sediments of the Augusta area, using the >63 ␮m fraction, demonstrating its reliability as environmental indicator (Romano et al., 2013). This correlation was confirmed also for core AU10, where the Foraminiferal Number was found negatively correlated to all the contaminants, with an high correlation coefficient (␳ = −0.936) with respect to Hg (Romano et al., 2015). From these results we may deduce that contamination levels are the main factor influencing foraminiferal density, while other environmental factors may be supposed to have null or minor importance. Consequently, low FN values indicate low environmental status due to chemical contamination. Assuming that the FN 63 is always higher than FN 125, because the finer fraction is inclusive of the coarser one, the first conclusion is that, as regards faunal density, the 63-assemblage is indicative of a better environmental quality. Observing the FN values along the core-depth (Fig. 4), despite the similarity of the two profiles, it is clear how the dead zone of 125-assemblage is wider than the 63-one, due to the loss of smaller specimens. The significant environmental improvement, recorded by FN 63 in the range between 20 cm and 40 cm, is not pointed out by FN 125, which testifies the further improvement of environmental conditions only in

the upper 20 cm. This demonstrates how, in the Augusta sediments, the FN 125 is unreliable descriptor of environmental quality and also not enough sensitive to the environmental changes. Another tool, generally used for environmental assessment for living (Vilela et al., 2011) and fossil assemblages (Alve et al., 2009), is the species diversity. Considering the species richness S, a great difference was found in this study between the two considered fractions with the high % of lost species in the 125-assemblage (LSI: 20–71%). Nevertheless, values of ␣-rate generally lower than 1 indicate that the ␣-index was mostly higher in the coarser fraction (Fig. 6). This may be explained by the ␣-index formula, which takes into account the number of species, including the rare ones, with respect to the total number of specimens counted (Murray, 1991). For this reason, it may happen that the number of species vs the number of individuals in a sample, may be higher in the coarser fraction where foraminifera are less abundant. On the other side, Schönfeld et al. (2013) observed that ␣-index was strongly influenced by size fraction because it was lower by a half in the >125 ␮m and >150 ␮m fractions as compared to the >63 ␮m one. Differently, values of H’-rate always higher than 1 indicate that the H’-index was always higher in the 63-assemblage. It generally varies from 0, for communities with only a single taxon, to higher values for communities with many taxa, when individuals are equally distributed among taxa (Murray, 1991). High values of LSI indicate that 125assemblage contain a considerably lower number of species with respect to the 63-one. Nevertheless, because the H’ is determined in a logarithmic algorithm, the variability due to the different number of species in the two fractions is reduced. This implies that H’ is the less influenced index by the foraminiferal size and, consequently, by different foraminiferal density of the two assemblages. The good response of the H’ index to different foraminiferal density was also recognized by Barras et al. (2014). A correlation matrix (Pearson Correlation), including size parameters determined in our study (FSI, LSI, ␣-rate, H’-rate and Drate) and the foraminiferal indices, describing species diversity and density in the two considered size fractions (␣ 63 and ␣ 125; H’ 63 and H’ 125; FN 63 and FN 125), together with the abiotic sediment parameters from Romano et al. (2015) was applied (Table 2). The correlation between chemical and grain size parameters will not be discussed because it was the topic of Romano et al. (2015). Some relevant correlations were recognized, pointing out the differences between the 63 and 125-assemblages. The high positive correlation between FSI and LSI means that the larger is the number of foraminifera having a size between 63 and 125 ␮m, and the higher is the number of species lost in the >125 ␮m fraction. Consequently, small specimens are distributed among most species. Besides, the positive correlation of FSI and LSI with the H’-rate, indicates that higher H’ values are found in the 63-assemblage with increasing number of smaller foraminifera and increasing species lost in the coarser fraction. Differently, the ␣-rate shows significant (negative) correlation only with FSI, and D-rate has negative correlation both with FSI and LSI. It may be deduced that ␣-rate is directly influenced only by proportion of smaller specimens with respect to the larger ones, while D-rate is also conditioned by the number of species lost in the 125-assemblage. In spite of great loss of specimens and species of 125-assemblage, it seems that H’ index has narrow variation considering the two assemblages and that such variation is predictable because directly proportional to the number of missing specimens and species in the coarser one. These features make the H’ index preferable when artificial loss, due to coarse sieving, may not be avoided. The negative correlation of FSI and LSI with PCBs and sand, and the positive correlation with clay let us suppose that both sediment texture and PCBs concentration may be factors conditioning foraminiferal size. The negative correlation of FN with clay in both 63 and 125 assemblages is a significant feature of the studied core. Because organic carbon is generally associated to the fine sed-

sand sand silt clay PAHs PCBs Ba Hg FN 63 FN 125 H’ 63 H’ 125 ␣ 63 ␣ 125 FSI LSI H’ rate ␣ rate D rate

−0.775 −0.78438 −0.4731 −0.66231 −0.0023411 −0.34223 0.65128 0.63171 0.28399 0.55074 0.31787 −0.35459 −0.48223 −0.53208 −0.54055 0.33966 0.52822

silt

clay

PAHs

PCBs

Ba

Hg

FN 63

FN 125

H’ 63

H’ 125

␣ 63

␣ 125

FSI

LSI

H’ rate

␣ rate

D rate

0.00042157

0.00032143 0.42183

0.064192 0.26484 0.085854

0.0051835 0.078341 0.018457 0.088602

0.99313 0.56518 0.58355 0.24607 0.033396

0.19447 0.19539 0.47342 0.091141 0.0032556 0.00012788

0.0062776 0.036902 0.053085 0.052423 0.0002095 0.0052249 0.00017546

0.0086654 0.054354 0.050151 0.21097 0.0025596 0.094267 0.010892 3.18E-06

0.28644 0.42382 0.39054 0.18722 0.046999 0.11279 0.006671 0.010129 0.0059191

0.027045 0.56413 0.0025187 0.043819 0.046001 0.88247 0.25835 0.034179 0.015277 0.0024381

0.23022 0.90861 0.037261 0.94508 0.26614 0.50295 0.5151 0.3147 0.037946 0.042852 0.021343

0.17779 0.28969 0.30504 6.68E-05 0.57393 0.92106 0.83999 0.55552 0.67987 0.94971 0.32753 0.65428

0.058531 0.39322 0.037966 0.12658 0.091387 0.46234 0.55372 0.19735 0.040129 0.054074 0.00079691 0.015182 0.061487

0.033878 0.58226 0.003971 0.11986 0.095188 0.62678 0.31446 0.047102 0.0091084 0.0091908 4.78E-07 0.015219 0.25914 2.41E-05

0.030632 0.7049 0.0011393 0.02346 0.079279 0.43679 0.5744 0.19045 0.16163 0.075159 2.52E-07 0.071772 0.14714 0.00091065 4.57E-05

0.19806 0.14319 0.57602 0.10046 0.57591 0.41322 0.75589 0.98185 0.62883 0.74436 0.77775 0.63677 0.00036953 0.012567 0.44019 0.47362

0.035439 0.44569 0.01111 0.36691 0.33693 0.098672 0.42188 0.69922 0.54787 0.62815 0.0026116 0.4243 0.64711 0.093395 0.031792 0.0002976 0.93952

0.21594 0.29648 0.45261 0.15553 0.34157 −0.52473 −0.4894 −0.21504 −0.15594 0.031224 0.28216 0.22918 0.14882 0.10276 −0.38294 −0.20526

0.44281 0.58023 −0.14832 0.1932 −0.49165 −0.49703 −0.23044 −0.70032 −0.52388 0.27368 0.52225 0.67697 0.73648 −0.15126 −0.61571

0.43938 0.30785 0.43627 −0.49285 −0.33066 −0.34752 −0.50948 0.018741 0.83098 0.39823 0.40481 0.56202 −0.42538 −0.24181

0.5333 0.68741 −0.79833 −0.69953 −0.50307 −0.50504 −0.29571 0.15208 0.43598 0.43145 0.45135 −0.15131 −0.25684

0.81319 −0.66186 −0.43253 −0.41202 0.040207 0.18074 −0.026958 −0.19798 −0.13172 −0.20921 0.21988 0.42741

−0.80381 −0.61702 −0.64769 −0.30035 −0.17571 0.054892 0.16007 0.26861 0.1519 0.084432 0.21592

0.89327 0.62176 0.53133 0.26848 −0.15936 −0.34016 −0.50286 −0.34514 0.0061907 0.10483

0.65471 0.59391 0.52229 −0.11191 −0.51736 −0.62857 −0.36733 0.13094 0.16241

0.70191 0.51149 −0.017159 −0.48989 −0.628 −0.45697 −0.088542 0.1312

0.56932 −0.2617 −0.75112 −0.91939 −0.92664 0.076678 0.69853

0.12139 −0.59435 −0.59418 −0.46176 0.12795 0.21482

0.47739 0.29988 0.37949 −0.77961 −0.12406

0.85527 0.74577 −0.60746 −0.43357

0.84049 −0.2077 −0.53745

−0.19312 −0.78697

0.020641

L. Bergamin, E. Romano / Ecological Indicators 71 (2016) 66–78

Table 2 Correlation matrix (Pearson index\p value) of faunal parameters and abiotic sediment parameters from Romano et al. (2015). ␣-index, H’-index in the 63 and 125-assemblages were included. FSI, LSI, H’-rate, ␣-rate and D-rate. Significant correlations and corresponding p values are in bold.

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iment fraction, the present result confirms that organic enrichment does not play a significant role with respect to foraminiferal density in core AU10. Both FN 63 and FN 125 are negatively correlated with Hg and PCBs, but correlation shown by FN 63 is considerably higher. Moreover, FN 63 is also negatively correlated with Ba. Also considering the H’ index, the H’ 63 is negatively correlated with Ba, Hg and PCBs, while H’ 125 shows significant negative correlations with PCBs. From these results it may be deduced that faunal parameters of the 63-assemblage are better descriptive of the environmental status. Recently the expH’bc , derived from the H’ index, has been used as an indicator for defining Ecological Quality Status (EcoQS), based on different class ranges of some biotic and abiotic parameters (Bouchet et al., 2012; Dolven et al., 2013). In their study on sediments from silled basins of the Norwegian Skagerrak coast, Bouchet et al. (2012) found that diversity both of the 63 and 125 assemblages had significant correlation with bottom-water oxygen. Consequently, they indicated that >125 ␮m fraction is preferable for the assessment of ecological status because of the small information lost and of the minor effort required for the analysis. However, for the chemically polluted sediments from the Augusta harbour, a classification tool like as EcoQS, based on lower H’ values from the 125-assemblage, could led to a classification corresponding to worse conditions than those described by the 63-assemblage. Because this study demonstrated the better correlation of H’ index of the finer fraction with chemical contaminants, it may be deduced that it is a more reliable descriptor of actual ecological status. The PCA is one of the most commonly statistical descriptive methods used to characterize foraminiferal assemblages (Carboni et al., 2009; Coccioni et al., 2009; Martins et al., 2013) also if this study is not aimed to this purpose. The comparison of PCA of 63and 125-assemblages is finalized to understand if they supply the same ecological information. The same general information may be obtained from the two scatter plots on samples grouping and species characterizing each groups, but some significant differences are recognizable (Fig. 7, Fig. 8). The main evidence is that the >63 ␮m plot shows a more clear partition of species groups. The core interval directly above the barren one (group 2) is well characterized only in this fraction, because of the exclusion from the matrix of samples with few individuals, not offering a solid statistical census in the coarse fraction. The species mostly characterizing group 2 in the 63-assemblage, S. vivipara, is not recognizable in the 125-one. Because this group corresponds to a first environmental improvement, indicated by the increase of the FN in the 63-assemblage at about 40 cm, it may be deduced that important ecological information on the assemblage of this core interval is lost by the 125-assemblage. Moreover, Q. lata is attributable to group 2 in the 63-assemblage and to group 3 in the 125-assemblage. This species was defined in Romano et al. (2008, 2009) as tolerant for heavy metal polluted sediments and this feature is confirmed only in the 63-assemblage (Fig. 7). As a consequence, a contradictory information is obtained from the PCA based on the 125-assemblage. All the above considerations indicate that, for Augusta sediments, reliable information useful for the definition of environmental status may be obtained only from the faunal census of the >63 ␮m sediment fraction.

6. Conclusions From the comparison of the 125-assemblage with the 63-one, which was considered more conservative as regards the ecological information, a great depletion of the first one was recorded in terms of number of specimens and species. Although this loss affects mostly small detritivore infaunal species, which may be nearly absent in the 125-assemblage, it was demonstrated that it

involves a considerable number of species. Species diversity and dominance were found to be directly correlated to the proportion of small-sized foraminifera and/or to the % of species lost in the coarse fraction. All foraminiferal parameters, generally considered as indicative of environmental quality, such as assemblage composition, species diversity and density, are modified in the 125-assemblage. However, from the comparison of the two assemblages, it was demonstrated the H’ index was the one with smaller variability. The most common foraminiferal indices used for the definition of the environmental status, based both on species composition and diversity, lead to unreliable results if applied using the 125-assemblage. The better correlation of FN and H’ of the 63-assemblage with contaminant concentrations strongly indicate the better performance of the finer fraction for environmental assessment purposes. Because smaller specimens are more abundant above the barren core interval, characterized by the highest contamination levels, the finer size fraction detects earlier and more effectively the first signs of recovery of the foraminifera community. Even the use of statistical techniques aimed to characterize distinct foraminiferal assemblages, each one corresponding to a specific environment, was found negatively affected by the depletion of the 125-assemblage. These results indicate that, when benthic foraminifera are studied in sediment cores for environmental reconstruction and assessment of chemically polluted areas, the use of the >63 ␮m fraction should be strongly considered in spite of the higher effort necessary for the analysis.

Acknowledgments We are very grateful to two anonymous reviewers who helped us to improve the manuscript with constructive criticism and helpful suggestions.

Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ecolind.2016. 06.030.

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