Fossile Et Al. (2021) Gulf of Manfredonia (Southern Adriatic Sea)

Marine Pollution Bulletin 163 (2021) 111933
Contents lists available at ScienceDirect
Marine Pollution Bulletin

journal homepage: www.elsevier.com/locate/marpolbul
Sensitivity of foraminiferal-based indices to evaluate the ecological quality

status of marine coastal benthic systems: A case study of the Gulf of
Manfredonia (southern Adriatic Sea)
Eleonora Fossile a, 1, Anna Sabbatini a, *, Federico Spagnoli b, *, Francesca Caridi a,
Antonio Dell’Anno a, Rocco De Marco b, Enrico Dinelli c, Elisa Droghini d, Mario Tramontana d,
Alessandra Negri a
a
Department of Life and Environmental Science, Polytechnic University of Marche, Via Brecce Bianche, 60131 Ancona, Italy
b
Institute of Biological Resources and Marine Biotechnology (IRBIM), National Research Council (CNR), Largo Fiera della Pesca, 2, 60125 Ancona, Italy
c
Department of Biological, Geological, and Environmental Sciences, University of Bologna, Piazza di Porta S.Donato 1, Bologna, Italy
d
Department of Pure and Applied Sciences (DiSPeA), University of Urbino Carlo Bo, Campus Scientifico E. Mattei, 61029 Urbino, Italy
A R T I C L E I N F O A B S T R A C T
Keywords: This paper aims to compare two foraminiferal based biotic indices generally used to evaluate the ecological
Foraminifera quality status (EcoQS): the Foram-AMBI and the Foram Stress Index (FSI). For this purpose, we report the dis
Biomonitoring tribution and diversity of living foraminiferal assemblages and the environmental variables from a bathymetric
Biotic indices
transect in the Southern Adriatic Sea. The two indices agree well with the detected organic enrichment but
Mediterranean
Organic matter
indicate conflicting EcoQS as the Foram-AMBI detects good environmental conditions, whereas the FSI describes
Heavy metals a poor-moderate quality. Many species not assigned (including soft-shelled foraminifera) are to blame for the
different results. Also, both foraminiferal-based indices neglect the heavy metal increase encountered in the
deepest stations. These findings suggest the need for a more in-depth analysis to improve the ecological status
evaluation of marine benthic systems, including other descriptors as chemical pollutants in combination with
biotic indices sensitive to organic matter enrichment.
1. Introduction Framework Directive (WFD, 2000/60/EC) to protect and monitor

coastal and transitional waters. In the WFD, and later in the Marine
Human activities strongly influence marine coastal areas. One of the Strategy Framework Directive (MSFD, 2008/56/EC), was underlined the
major threats is the continental runoff of industrial waste, urban sewage necessity to evaluate the ecological quality status (EcoQS) of those
and farming, leading to eutrophication and deterioration of the coastal ecosystems using efficient and reliable bio-assessment tools. Bio
water quality (e.g., Karydis and Kitsiou, 2012; Khan and Mohammad, indicators (i.e., macrofauna and meiofauna) are useful tools to evaluate
2014; Powley et al., 2016). Nonetheless trace elements, from natural or the environmental quality thanks to their sensitivity to natural and
anthropogenic sources may also determine the contamination of those anthropogenic variations. Among those, benthic foraminifera present
areas. Marine sediment is a repository and sink for many natural and several advantages. They are unicellular organisms part of the meio
anthropogenic contaminants (e.g., Roussiez et al., 2006; Christophoridis fauna, worldwide distributed in all marine and transitional environ
et al., 2019) and can become toxic for benthic faunas, further causing ments, quickly responding to environmental changes thanks to their
ecological changes (e.g., Vilela et al., 2004; Frontalini and Coccioni, short life cycle (Murray, 2006). Moreover, foraminiferal fossilisation
2011). For these reasons, the monitoring and evaluation of marine en potential allows to monitor environmental changes through time
vironments’ “ecological health” requires the integration of chemical and (Frontalini and Coccioni, 2011): foraminifera can be used to define the
biological analyses (e.g., Hylland et al., 2017; Musco et al., 2017). present EcoQS (e.g., Barras et al., 2014; Bouchet et al., 2018; Damak
In this context, the European Commission enacted the Water et al., 2019) and to provide time series back to reference conditions (e.g.,
* Corresponding authors.
E-mail addresses: [email protected] (A. Sabbatini), [email protected] (F. Spagnoli).
1
LPG-BIAF UMR-CNRS 6112, UNIV Angers, CNRS, UFR Sciences, 2 bd Lavoisier 49045, Angers CEDEX 01, France.
https://doi.org/10.1016/j.marpolbul.2020.111933
Received 9 July 2020; Received in revised form 7 December 2020; Accepted 9 December 2020
Available online 20 January 2021
0025-326X/© 2020 Elsevier Ltd. All rights reserved.
E. Fossile et al. Marine Pollution Bulletin 163 (2021) 111933
Alve et al., 2009; Dolven et al., 2013). Foraminiferal distribution and 2. Material and methods
composition are influenced by several environmental factors, including
temperature, salinity, organic matter inputs, oxygen, sediment grain size 2.1. Study area
and composition (Murray, 2006; Celia Magno et al., 2012).
Based on such features, foraminifera are widely used to evaluate The present study was carried out in the Gulf of Manfredonia (South-
different impacts in coastal environments: aquaculture, oil spills, heavy Eastern of the Gargano promontory, SW Adriatic Sea) (Fig. 1). The
metals and urban sewage (see Bouchet et al., 2012 and reference western Adriatic current (W-Ad) determines the sedimentological
therein). However, it is still unclear how to distinguish between natural characteristics of the western Adriatic Sea. It represents the main sup
and anthropogenic stress (Armynot du Châtelet and Debenay, 2010). plier of fine-grained sediments within the Gulf of Manfredonia (Spagnoli
The FOraminiferal BIo-MOnitoring group (FOBIMO) established a et al., 2008). The W-Ad current flows southward offshore the Gargano
standardised protocol for environmental monitoring studies to optimise Promontory. It generates an anticyclonic cell into the central area of the
the use of foraminifera as bioindicators (Schönfeld et al., 2012). After Gulf (Fig. 1), responsible for the partial mixing of the Ofanto river
that, several foraminiferal indices have been proposed to evaluate the sediments with the fine sediments coming from the north (Spagnoli
soft bottom EcoQS (e.g., Alve et al., 2016; Barras et al., 2014; Bouchet et al., 2008). Also, the Ofanto river provides the main continental inputs
et al., 2012; Dimiza et al., 2016; Jorissen et al., 2018; Alve et al., 2019). (Cattaneo et al., 2003).
However, the scientific community is not yet fully coordinated and a As for the reactive organic matter, porewater concentration data
shared routine application to evaluate the environmental quality is showed high inputs in the Gulf of Manfredonia shelf and minor inputs in
missing. the southern Adriatic Sea (Spagnoli et al., 2010). Previous studies
The present study aims to contribute this topic by investigating the (Spagnoli et al., 2010) observed that the basin area presents higher
living foraminiferal assemblages from the surface sediments along a oxygen penetration depth and lesser organic matter degradation prod
bathymetric transect in the Gulf of Manfredonia (southern Adriatic Sea, ucts (NH+ 4 and DIC) than the shelf. Also, in the Gulf of Manfredonia,
Italy) to evaluate the environmental status of the area. First, we analysed organic matter degradation processes led to anoxic conditions within the
foraminiferal distribution and diversity patterns related to several first millimeters of sediments, whereas in the basin the oxic layer is
environmental variables measured in the surface sediment (e.g., sedi thicker (Spagnoli et al., 2010). Finally, Mn and P enrichment, in the
ment organic matter quantity and quality, grain size, temperature, pH, superficial sediment of the Gulf, was attributed to changes in the solid
redox potential, and heavy metals concentrations). Then, we applied discharge from rivers into the Gulf rather than industrial contamination
two different foraminifera-based indices to evaluate the EcoQS, the (Focardi et al., 2009).
Foram-AMBI developed for the Mediterranean (Jorissen et al., 2018)
and the Foram Stress Index (FSI; Dimiza et al., 2016) to evaluate their
sensitivity and highlight the differences in the EcoQS obtained. 2.2. Sampling strategy
Five stations located along a bathymetric transect were sampled by

box-corer (20 * 29 * 49 cm) in September 2016 during the PERTRE
cruise (R/V G. Dallaporta) organised by ISMAR (Istituto di Scienze
Fig. 1. Location of the study area with sampling stations. The blue lines represent the western Adriatic current (W-Ad). Bathymetry obtained from GEBCO 2014
(www.gebco.net) and map elaborated with Qgis (made with Natural Earth). (For interpretation of the references to colour in this figure legend, the reader is referred
to the web version of this article.)
2
Table 1
List of sampling stations with date of sampling, coordinates, water depth and surface sediment parameters (Eh = redox potential, T = temperature).
Sampling date Station Longitude (◦ E) Latitude (◦ N) Depth (m) pH Eh (mV) T(◦ C)
24/09/2016 35 16 05.493
◦
41 32.781
◦
15.4 7.33 − 228.0 23.6
24/09/2016 33 16◦ 19.292 41◦ 35.738 32.5 7.20 − 219.0 21.9
24/09/2016 28 16◦ 28.693 41◦ 38.625 74.4 7.33 − 178.5 15.4
25/09/2016 26 16◦ 39.411 41◦ 41.492 103 7.16 − 160.8 15.3
29/09/2016 25 16◦ 46.459 41◦ 42.737 131 7.61 141.0 14.6
Marine; CNR, Ancona) (Fig. 1). At each station, the surface sediment was as bovine serum albumin, glucose and tripalmitin equivalents, respec
immediately described and photographed, and measurements of tively. Protein, carbohydrate and lipid concentrations were converted
physical-chemical parameters were taken by punch-in electrodes in the into carbon equivalents by using the following conversion factors: 0.49,
uppermost 2 cm (pH by Methrom 826 pH meter with Pt 1000 code n. 0.40 and 0.75 g C g− 1, respectively (Fabiano et al., 1995). The sum of
6.1114.010 and pH microelectrode code n. 6.0234.100; redox potential protein, carbohydrate, and lipid carbon was referred as Biopolymeric
(Eh) by Crison 507 pH meter with Crison redox electrode 5260; T by Carbon (BPC) and the algal fraction of the BPC was calculated as the
Methrom 826 ph meter and Pt 100 code n. 6.1114.010; Table 1). One percentage ratio of C-CPE to BPC (Pusceddu et al., 2009). To highlight
sediment core (3.6 cm inner diameter), dedicated to foraminiferal ana variations among stations in organic matter parameters, one-way
lyses, was collected at each station using a plexiglass liner tube and then ANOVA and Tukey’s HSD test were performed using the Paleontolog
stored at − 20 ◦ C until further processing in the laboratory. Additionally, ical Statistics Data Analysis (PAST) software (version 2.17c; Hammer
extra aliquots of surface sediment were collected from the box-corer et al., 2001).
with a spoon and stored at − 20 ◦ C until processing. These aliquots TOC-VCPH analyser was used to determine the Total Organic Carbon
were destined for grain size and total organic C analysis, biochemical (TOC) sediment content doing two sequential analyses. First, a sediment
composition of organic matter, and trace metals concentration. aliquot was used to measure the Total Carbon (TC) through a combus
tion process at 900 ◦ C. Then another aliquot of sediment was used to
2.3. Grain size analysis determine the Inorganic Carbon (IC) with a combustion process at 200
◦
C (after the addition of concentrated phosphoric acid). The TOC con
A fraction of the surface sediment (0–2 cm) collected at each station tent was calculated as the difference between TC and IC content. For
was oven-dried at 70–80 ◦ C for about 48 h. Dry sediment samples were detailed methods refer to Droghini et al. (2019).
pre-treated with a 16% H2O2 solution (65 vol.) to facilitate separation of
the grain and remove organic matter. The coarser and finer fraction was 2.5. Trace metal analysis
then obtained by wet sieving with a mesh of 62.5 μm; the two fractions
thus obtained were oven-dried at 60–90C◦ for about 48 h. The coarser The total concentration of selected elements (As, Cr, Ni, Pb) of
fraction (>62.5 μm) was separated using sieves (Series A.S.T.M.) piled environmental concern were obtained on bulk sediment from the same
with a decreasing mesh, which allowed the separation of the different stations used for foraminiferal analyses. The analyses were carried out
grain size classes (Wentworth, 1922). Two cycles of vibration, 6 min by means of X-ray Fluorescence spectrometry using a Panalytical
each, were sufficient for the treatment; the fraction retained by every Axios4000 spectrometer at the XRF-Lab of the BiGeA Department. Dried
single sieve was weighed and expressed in percentage with respect to the sediment was milled and homogenised in an agate mortar and prepared
total weight of the sample examined. The pelitic fraction (<62.5 μm) as pressed powder pellets. Matrix corrections followed the methods of
was prepared for further analysis with a Sedigraph (Micromeritics Franzini et al. (1972, 1975), Leoni and Saitta (1976), and Leoni et al.
Sedigraph 5100): 4 g of sediment were treated with a solution of distilled (1982). Accuracy was tested by analysing international reference stan
water and sodium hexametaphosphate 6‰ (with anti-flocculant action) dards: differences with reference values were lower than 5%, except for
for about 24 h, and then ultrasonicated for 5–7 min, for further disin trace elements with concentrations lower than 10 μg g− 1 (10% relative
tegration of any floccules. The samples were then analysed by X-ray difference). The Loss on Ignition was determined gravimetrically after
Sedigraph that measures a grain size range between 0.1 and 300 μm with overnight heating at 950 ◦ C. The total mercury content was determined
2% accuracy. by thermal decomposition amalgamation atomic absorption spectrom
etry using a Direct Mercury Analyser (DMA-1, Milestone, BG, Italy) as
2.4. Organic matter analysis explained in Droghini et al. (2019).
The surface sediment (0–2 cm) collected at each station was used to 2.6. Foraminiferal analysis
assess the organic matter’s quantity and biochemical composition. The
quantification of all parameters (Chlorophyll-a, phaeopigments, total In the laboratory, we extruded every frozen sediment core from the
lipids, carbohydrates and proteins) were performed as three pseudo- plexiglass liner tube, and we sliced the 0–0.5 cm and 0.5–1 cm sediment
replicates, with about 1 g wet sediment per sample. Chlorophyll-a intervals. These were then fixed in a solution of 4% formalin (to preserve
(Chl-a) and phaeopigment analyses were carried out according to the foraminiferal cytoplasm) buffered with sodium borate (to prevent
standard protocols (Lorenzen and Jeffrey, 1980). Pigments were dissolution of foraminiferal calcareous shells) and stained with Rose
extracted with 90% acetone (12 h in the dark at 4 ◦ C). After the Bengal (1 g L− 1) for 48 h to distinguish living faunas. Sediment samples
extraction, the pigments were fluorometrically analysed to estimate the were then sieved through 150 and 63 μm mesh. All the processed samples
quantity of Chl-a and, after acidification (20 s) with 0.1 N HCl (Plante- were then stored in 4% buffered formalin solution with one drop of Rose
Cuny, 1974), to estimate the amount of phaeopigments. Chloroplastic Bengal solution. The described protocol was used to allow the better
pigment equivalents (CPE) were calculated as the sum of Chl-a and preservation of soft-shelled foraminifera (Danovaro et al., 2003), which is
phaeopigments concentration. The carbon associated with CPE (C-CPE) not fully guaranteed with the use of ethanol as recommended in the
was calculated by converting CPE contents into carbon equivalents using FOBIMO protocol (Schönfeld et al., 2012). The residues were kept wet
40 μgC per μg of phytopigment as a conversion factor (de Jonge, 1980). and hand-sorted for living stained benthic foraminifera in water in a Petri
Protein, carbohydrate and lipid sedimentary contents were determined dish using the stereomicroscope (ZEISS Stemi 2000). Hard-shelled
spectrophotometrically (Danovaro, 2009) and concentrations reported calcareous and agglutinated species were sorted in micro-
3
paleontological slides. Instead, soft-shelled monothalamous species were Assigned species, NA hereinafter). According to Borja and Muxika
placed in cavity slides in glycerol and observed under a compound mi (2005), in samples where the NA make up >20% of the assemblage, the
croscope (Nikon Eclipse E 600 POL). For the >150 μm fraction, all living AMBI-values should be evaluated with care and if they make up >50%,
specimens were picked and counted while for the 63–150 μm fraction AMBI should not be used.
several splitted aliquots were analysed and picked for living specimens in The FSI was calculated using the Dimiza et al. (2016) formula and the
order to reach a total of at least 300 individuals; counts from each wet species were classified as “sensitive” (Sen) or “stress tolerant” (Str) using
aliquot were then extrapolated and standardised for the total sample. only the list provided by Dimiza et al. (2016). Following El Kateb et al.
Foraminiferal species were determined using commonly used taxonomic (2020), we added the species Eggerelloides scaber in the Str group. The
reference works (e.g., Cushman, 1950; Loeblich and Tappan, 1987). complete list of the species recognised in the present study with fora
Foraminiferal counts from the two sediment intervals (0–0.5 and 0.5–1 miniferal densities (ind.10 cm− 3) and the correspondent Foram-AMBI
cm) were combined and then standardised to 10 cm3. The total density of and FSI classification can be found in the supplementary materials.
living foraminifera (ind.10 cm− 3 in the >63 μm) in the 0–1 cm interval Both indices do not consider soft-shelled foraminifera, therefore we
was calculated as the sum of the density of the two size fractions (63–150 excluded them from the calculation, and the same we did for the H′ .
μm and > 150 μm). Foraminiferal biodiversity was estimated using However, in order to explore the possible contribution of this group in
different diversity indices: species richness, measured as the number of the evaluation of the EcoQS of the soft bottom area, both indices were re-
species; species diversity, measured by the Shannon-Wiener (H′ ); the calculated including the two most abundant and easily recognisable
equitability (J), known as Pielou’s evenness. The indices were calculated genera of monothalamous soft-shelled foraminifera. The pollution
using PAST (version 2.17c; Hammer et al., 2001). All the biodiversity ranking for each station (i.e. unpolluted, slightly polluted, meanly
indices were calculated considering the coarser fraction (>150 μm) and polluted, heavily polluted and extremely polluted) was obtained
the finer fraction (63–150 μm) separated and combined together (>63 μm following Borja et al. (2003) and Dimiza et al. (2016) for the Foram-
fraction). A heatmap was used to display foraminiferal relative abun AMBI and FSI, respectively. The corresponding EcoQS was classified
dances (for the species contributing more than 5% in at least one sample) as high, good, moderate, poor or bad for both indices. Since there is no
for the coarser (>150 μm) and the finer fraction (63–150 μm). The limit EcoQS performed on foraminifera yet, for the Foram-AMBI we
heatmap was generated using the package ggplot2 (Wickham, 2016) in R tentatively applied the EcoQS limits defined for macrofauna (Borja et al.,
software (version 4.0.0; R core team, 2020). 2003). A recent publication on the same topic (El Kateb et al., 2020) also
refers to EcoQS limits proposed by Barras and Jorissen (2011) when the
2.7. Multivariate analysis foraminiferal TSI-Med index is applied. El Kateb et al. (2020) also used
EcoQS classes developed for the Italian coastal environments by Bouchet
A Canonical Correspondence Analysis (CCA) was used to visualise et al. (2018) based on environmental criteria and diversity (Exp(H’bc))
the relationships between the environmental parameters (water depth, values. We then tested the correlation of the Foram-AMBI and FSI with
sediment T, pH, Eh, grain-size, organic matter composition and heavy TOC % and H′ index (Alve et al., 2016) as it is expected correspondence
metal concentrations) and the faunas (>63 μm, 0–1 cm) of all stations between degraded environment (high values of the Foram-AMBI), high
considering the absolute densities (ind. 10 cm− 3) of the species which TOC % and low diversity. Additionally, we tested the possible correla
contribute with >5% to the assemblage. Values of different environ tion of both indices with the biopolymeric Carbon (BPC).
mental variables and different orders of magnitude were standardised as
follows: (x-mean x)/sd, in which x is the value of the variable in one 2.8.2. Environmental status based on other variables
station, mean x is the mean of the same variable among the stations and We considered several environmental parameters to evaluate the
sd is the corresponding standard deviation. The densities of the fora environmental status along the transect (pH, Eh, sediment grain size, the
miniferal faunas were normalised using the transformation Log10(x + 1) TOC %, the BPC with its composition and the concentrations of selected
(where x is the density expressed in ind. 10 cm− 3). We performed this heavy metals As, Cr, Hg, Ni and Pb). Values of pH and Eh were used to
CCA using PAST (version 2.17c; Hammer et al., 2001). infer the surface sediment oxygenation in comparison with the quantity
of organic matter (TOC % and BPC). The proteins to carbohydrate ratio
2.8. Evaluation of environmental quality (PRT/CHO) were used as descriptors of aging and nutritional quality of
the sediment organic matter (Pusceddu et al., 2000; Tselepides et al.,
2.8.1. Ecological quality status based on benthic foraminifera 2000).
To evaluate the environmental quality, we applied two indices using
the organic enrichment as a driving factor: the Foram-AMBI developed 3. Results
for the Mediterranean (Jorissen et al., 2018) and the Foram Stress Index
(FSI; Dimiza et al., 2016). We calculated both indices considering the 3.1. Environmental variables
foraminiferal assemblages of the larger fraction (>150 μm) and of the
total >63 μm size fraction, in the top first centimetre of the sediment. 3.1.1. Surface sediment characteristics
For the Foram-AMBI, the list of the Mediterranean species assign The temperature at the bottom sediment interface decreases with
ment is given in Jorissen et al. (2018) and the index was calculated using increasing water depth, varying from 23.6 ◦ C at the shallowest station
the Borja et al. (2000) formula. For each station we then calculated the (35) to 14.6 ◦ C at the deepest one (25) (Table 1). Surface sediment pH
percentage of individuals not present in the species assignment list (Not varies between 7.16 (at station 26) and 7.61 (at station 25). The redox
Table 2
Grain size characteristics (percentage of gravel, sand, silt and clay), percentages of total organic carbon (TOC) and protein to carbohydrate ratio (PRT/CHO).
Stations Gravel (%) Sand (%) Silt (%) Clay (%) TOC (%) PRT/CHO
35 0.3 0.3 46.1 53.3 0.29 5.18

33 0.0 0.1 31.1 68.8 0.29 6.92
28 0.0 0.2 21.8 78.1 0.35 3.82
26 0.0 3.3 20.9 75.8 0.25 2.75
25 0.6 38.5 12.0 48.9 0.13 1.49
4
potential (Eh) increases from the coast to the open sea and it displays mg kg− 1 (set by the Environmental Quality Standard Water Framework
negative values (from − 228 mV to − 160 mV, therefore evidencing Directive and generally decrease from the inner to the outer stations (as
reducing conditions) at each station except for the outer station 25 detailed in Droghini et al., 2019). Pb varies from 21 to 27 mg kg− 1.
(+141 mV) (Table 1).
Grain size analyses (Table 2) show that sand contribution is low at all
stations except for the deepest station (38.5%), note that gravel size 3.2. Living foraminiferal assemblages
evidenced in table, corresponds to molluscan shell fragments. The per
centage of silt decreases from the coast to the open sea (from 46.1 to 3.2.1. Abundance, diversity and taxonomic composition
12.0%, from station 35 to 25) while clay increases from station 35 to 26 Considering the >63 μm size fraction the station 26 presents the
(from 53.3 to 75.8%). According to the Shepard classification (1954) the highest foraminiferal abundance (3182 ind. 10 cm− 2) and the station 33
sediment samples collected at the two shallowest stations (35 and 33) the lowest (309 ind. 10 cm− 3; Fig. 3) as well as the 63–150 μm fraction.
consist of silty clay, the stations 28 and 26 are clayey, and the deepest Whereas the coarser size fraction (>150 μm) records the highest abun
station 25 is sandy clay. dance at station 25 (326 ind. 10 cm− 3). The coarser fraction (>150 μm)
gives a low contribution to the total foraminiferal density at all stations
3.1.2. Phytopigments and organic matter composition (7 to 32%). In the >63 μm fraction, the highest species richness occurs at
The complete dataset for biochemical composition of the sediment is the station 25 with 88 identified species, decreasing progressively to
reported in Table S1 of the supplement. The BPC varies significantly wards the shallower stations (Fig. 3a). The H′ index values of the >63
among the stations (one-way ANOVA, F = 15.45, p < 0.001; Fig. 2). The μm fraction varies between 3.10 and 3.53 (Fig. 3b). If we consider the
highest BPC content is found at station 33 (5.61 ± 0.74 mgC g− 1), and it two size fractions separately, the >150 μm compared to the 63–150
shows a general decreasing trend from the coast to the open sea (from fraction shows lower diversity at the station 35 and 33 and higher at
4.44 ± 1.33 to 1.75 ± 0.20 mgC g− 1 at station 35 and 25, respectively; station 25. The equitability is high and similar at all stations with the
Fig. 2). The carbohydrates (CHO) concentration is similar at each station highest value at the station 33 (0.86) decreasing to 0.72 at station 26 and
(Table S1), while the protein (PRT) and lipid (LIP) concentrations show the coarser fraction always shows higher values compared with the finer
significant differences among stations (one-way ANOVA, F = 13.15, p < fraction (65–150 μm; Fig. S1).
0.001 for PRT, and F = 69.71, p < 0.001 for LIP). The BPC mostly Hyaline species dominate the foraminiferal assemblage of the
consists of PRT (60–83%), followed by CHO (10 and 34%) and LIP coarser fraction (>150 μm) at stations 28, 26 and 25 with relative
(<11%; Fig. 2). The PRT/CHO ratio generally decreases with increasing abundance varying from 43 and 52%, followed by agglutinated species
water depth (from 6.92 to 1.49 at station 33 and 25, respectively;
Table 2). The CPE concentrations vary significantly among stations (one-
way ANOVA, F = 88.11, p < 0.05), with the highest values at station 35
(18.19 ± 4.63 μg g− 1). Also, the contribution of the algal fraction to the
BPC (range: 6–19%) varies significantly among stations (one-way
ANOVA, F = 5.14, p < 0.05) but only the station 25 significantly differs
from the station 35 and 28 (Tukey’s HSD, p < 0.05). Total organic
carbon percentages are very similar in the sediments of stations 35 and
33 (0.29%) and slightly increase at station 28 and decrease at the two
deepest stations (Table 2).
3.1.3. Trace metals concentrations

The measured heavy metals concentrations across the transect show
a general increase from the inner to the outer stations (Table 3). Cr
shows values from 102 to 135 mg kg− 1. The same is observed for Ni
(from 49 to 92 mg kg− 1). Hg concentrations are below the limit of 0.3
Fig. 3. (a) Cumulative foraminiferal densities considering the two different size
Fig. 2. Biopolymeric carbon content (BPC, expressed in mgC g− 1 and repre fractions (63–150 μm and >150 μm) and species richness (S) of the >63 μm
sented by the black dots) and its relative composition of lipids (LIP), proteins fraction. (b) Shannon-Wiener index (H′ ) considering the 63–150 and the >150
(PRT) and carbohydrates (CHO). μm fraction separately and together (>63 μm fraction).
5
(29 to 45%) (Table S2). Agglutinated species instead dominate the two Cassidulina carinata, Eiloedra vitrea and M. subrotunda characterise the
shallowest stations (35 and 33) with 39 and 57%, respectively (Table stations 28, 26 and 25. Miliolinella sp. characterised exclusively station
S2). Soft-shelled taxa contribute with the 30% to the assemblage of the 25. Some species shared among all stations are Bolivina seminuda, Boli
large fraction at station 35 and with 4% at station 33 and 25. The finer vina spathulata, Bulimina aculeata and Bulimina marginata.
size fraction is dominated by hyaline taxa (from 73 up to 77%) at all
stations except station 35 where the dominance is broken down among
3.3. Evaluation of environmental quality
hyaline and agglutinated species (39 and 38%, respectively). Soft-
shelled foraminifera contribute with 12% at station 35 and 33 to the
3.3.1. Foram-AMBI
63–150 μm fraction (Table S2).
Applying the Foram-AMBI index on the large size fraction (>150
μm), we obtained values between 1.73 and 3.00 corresponding to a good
3.2.2. Foraminiferal living assemblages of the 63–150 and >150 μm size
environmental status (Table 4) and a slightly polluted classification
fractions
following Borja et al. (2003). However, we can observe some differences
The heatmap highlights similarities and differences in species
among the stations. Indeed, the two deepest stations show lower scores
composition among the stations and between the two size fractions
(1.73 and 1.83 for stations 26 and 25, respectively), meaning higher
(Fig. 4). The agglutinated Eggerelloides scaber dominates the shallower
environmental quality, while the other stations record values higher
stations 35 and 33 in the >150 μm fraction, while the finer size fraction
than 2.50. The percentage of not assigned specimens (NA) is less than
(63–150 μm) presents a more homogenous composition. Station 35 is
50% of the assemblages at each station; however, NA < 20% is observed
also characterised by the presence of Ammonia spp., the agglutinated
only at the stations 35 and 28. As expected, the H′ index calculated for
Lepthoalysis scottii and Reophax sp. and by some soft-shelled species
the coarser size fraction displays the opposite trend observed for the
(Allogromiid spp. and Psammophaga cf cristallifera) unique of this station.
Foram-AMBI, increasing from the coast to the open sea. The value of the
Whereas the soft-shelled Micrometula sp. was found only at station 33.
Foram-AMBI increases when applied on the >63 μm size fraction at all
The coarser size fraction (>150 μm) of the deeper stations (28, 26 and
stations except the 33, highlighting that the environmental quality
25) is dominated by the calcareous Uvigerina mediterranea and the
generally decreases but remains in the same interval of quality (Table 4).
agglutinated Textularia spp.. These three stations share also the presence
The frequency of NA decreases for the stations 33 (20.4%), 26 (12.8%)
of the hyline Bolivina seminuda in the finer size fraction (63–150 μm).
and 25 (33.2%) while for the remaining stations it increases. Although
The finer size fraction (63–150 μm) of stations 26 and 25 are dominated
the NA percentage is <50% at all stations, it is <20% only at station 26.
by Cassidulina carinata and Globocassidulina subglobosa.
The >63 μm fraction’s H′ index does not show a clear trend, but we have
the highest value at the offshore station 25 and the lowest at the
3.2.3. Multivariate analysis
innermost station 35 (3.5 and 2.9, respectively).
The first two axes of the CCA analysis explain around 84% of the total
variance (Fig. 5). The axis 1 separates the two shallowest stations 35 and
3.3.2. Foram stress index (FSI)
33 from the other three stations. Both stations, especially station 33,
The application of the FSI index on the assemblage of the >150 μm
present a positive correlation with the percentage of mud (silt + clay)
size fraction results in three different pollution states (Dimiza et al.,
and high quantities of organic matter (both in terms of TOC % and BPC
2016) and it varies from 1.58 to 6.19 (Table 5). Station 25 classifies as
content). The two deepest stations (25 and 26) positively correlate with
slightly polluted (good EcoQS), stations 35, 33 and 26 as moderately
heavy metal concentrations, percentage of sand and carbohydrate con
polluted (moderate EcoQS) and station 28 as heavily polluted (poor
centrations. Axis 2 separates the two central stations of the transect (28
EcoQS). The NA % is high (>40%) at all stations except for stations 35.
and 33) from the other stations based on lipid percentages. Some com
The FSI applied on the >63 μm fraction varies between 1.28 and 3.81
mon species characterise station 35 and 33: A. parkinsoniana, A. tepida,
and it classifies the stations into two different pollution state: stations
E. scaber, L. scottii, Micrometula spp. and N. turgida. The genus Psam
35, 26 and 25 are classified as moderately polluted (moderate EcoQS)
mophaga spp. and the species Reophax sp. occur exclusively at station 35.
and stations 33 and 28 as heavily polluted (poor EcoQS). The
Fig. 4. Heatmap showing the relative abundances of the species occurring with frequencies >5% considering the finer (63–150 μm) and the coarser (>150 μm) size
fraction separately.
6
Fig. 5. Canonical correspondence analysis based on foraminiferal densities (0–1 cm, > 63 μm, absolute densities of the species with relative abundance >5%) and 17
environmental variables.
percentages of NA are higher than 30% at each station except for station μm and >63 μm size fraction, respectively) (Fig. 6c). The same corre
26 (27.5%). lations were tested using the FSI scores (Fig. 6d, e, f). In this case, the FSI
index shows a strong negative correlation (R2 = 0.80) with the TOC %
3.3.3. Biotic indices correlations when applied on the coarser size fraction (>150 μm) while it decreases
A positive correlation between the Foram-AMBI and TOC % as well (R2 = 0.57) when applied on the entire fraction (>63 μm) (Fig. 6a). We
as between the Foram-AMBI and the BPC considering both size fractions can observe a significant correlation between the FSI and BPC when
is observed (Fig. 6a, b). However, the correlation between the Foram- considering the >63 μm fraction (R2 = 0.57) (Fig. 6e). The FSI index as
AMBI and the BPC (R2 = 0.89 and R2 = 0.62, for the >150 μm and opposed to the Foram-AMBI does not show a strong correlation with
>63 μm size fraction, respectively) is stronger than that with TOC % (R2 Shannon-Wiener Index (R2 = 0.44 for the >150 μm) (Fig. 6f).
= 0.42, for both size fractions). A negative correlation is recorded be
tween Foram-AMBI and H′ index (R2 = 0.74 and R2 = 0.78, for the >150
Fig. 6. Correlation of the two biotic indices (Foram-AMBI in panels a, b, c; FSI in panels d, e, f) and the TOC % (a, d), the BPC content (b, e) and the H′ index (c, d).
7
Fig. 7. Curves indicating the maximum relative frequencies of the two genera Micrometula and Psammophaga found as a function of (a) TOC % and (b) BPC con
centrations. (c) The cumulative relative abundance of all species belonging to each of the 5 ecological groups along an organic enrichment gradient (figure modified
from Jorissen et al., 2018 and Alve et al., 2016). The group Micrometula spp. includes M. hyalostriata and Micrometula sp. and the group Psammophaga spp. includes P.
cf cristallifera, P. cristallifera and P. cristallifera “magnetic”.
3.3.4. Possible assignments of soft-shelled foraminifera 4. Discussion

Fig. 7 shows the trends of the two most abundant genera of soft-
shelled foraminifera recorded in our samples, considering the >63 μm 4.1. Environmental drivers of foraminiferal distribution
fraction in relation to the organic enrichment (either BPC content or
TOC %). The trend based on the BPC enrichment suggests that Psam From the inner to the outer part of the Gulf of Manfredonia, different
mophaga may belong to the “Second-order opportunists” (group IV) and environmental conditions characterise the benthic systems investigated
Micrometula to the “First-order opportunists” (group V). On the other in the present study. In particular, the two shallower stations (station 35
hand, the relationship with TOC enrichment suggests the inclusion of and 33) are characterised by high concentrations of BPC (i.e., >5
both genera in group IV. Although, based on the better correlation be mgC− 1), high PRT/CHO ratio (i.e., the estimate of organic material
tween the Foram-AMBI and the BPC (Fig. 6b) we suggest to assign the aging; Fabiano et al., 1995), extremely negative Eh value (i.e., low ox
two genera following the BPC enrichment and we decided to consider ygen available; Søndergaard, 2009) and silty clay sediment as shown
both genera as stress-tolerant taxa for the FSI. However, these two also in the CCA analyses (Fig. 5). Usually, negative redox potential oc
genera are relatively abundant but not dominant in the assemblage curs at the sediment-water interface because of the consumption of ox
(relative abundances <8%) and the organic enrichment of our dataset ygen and other electron acceptors when organic material undergoes
does not show a gradient (i.e., all TOC values are <0.5%). This suggests decomposition and the supply of oxygen from the water column is
that we need more data to make the correct assignment of both genera, limited.
albeit promising. Nonetheless, these genera are abundant in coastal Our data suggest that the inner part of the Gulf of Manfredonia
areas and easy to identify, so their inclusion in the index would help to experienced an accumulation of biopolymeric carbon which could be, in
evaluate the EcoQS. turn, an additional co-factor potentially responsible for hypoxic or
anoxic events. In fact, the organic matter mineralisation rate is pro
3.3.5. Assessment of indices by including soft-shelled foraminifera portional to oxygen consumption. Instead, the accumulation of organic
The inclusion of the two genera of soft-shelled foraminifera (Micro carbon depends on its reactivity with the available oxygen (Dauwe et al.,
metula and Psammophaga) determines changes in the scores of the 2001). The fine grain size of our sediment samples, with an affinity for
Foram-AMBI and FSI only at the two shallowest stations (35 and 33) organic matter (Kennedy et al., 2002), may further reduce the oxygen
where these species are present. At station 35, the Foram-AMBI score penetration at these stations. Oxygenation and trophic availability are
increases from 2.62 (Table 4) up to 2.76 (Table 6) for the coarser frac the two major factors influencing foraminiferal distribution (e.g., Mur
tion, and from 3.20 (Table 4) up to 3.38 (Table 6) in the >63 μm frac ray, 2006), those, in turn, is also related to sediment grain size (Celia
tion. For this last fraction, this determines a change in the EcoQS of the Magno et al., 2012). The potential stressful environmental conditions at
station 35, passing from good to moderate and consequently the switch both stations 35 and 33 (i.e., low oxygen and high BPC) may explain the
from slightly to meanly polluted classification. Similar behaviour in the low benthic foraminiferal abundances and diversity encountered at
Foram-AMBI score can be observed for the station 33 when considering these stations. Here, a dominant opportunistic species is Eggerelloides
the >63 μm fraction: the value passes from 2.93 (Table 4) to 3.16 scaber, a species generally restricted to shallow water (<30 m) and
(Table 6) although in this case the quality range and the pollution nutrient-rich systems (Donnici and Serandrei Barbero, 2002; Mendes
classification does not change. The FSI value calculated for the station et al., 2004; Murray, 2006; Martins et al., 2015). This species can
35 decreases from 2.04 (Table 5) to 1.96 (Table 6) considering the penetrate deeper into the sediment and is able to exploit sub-surface
coarser size fraction and from 2.93 (Table 5) to 2.66 (Table 6) for the food resources (e.g., Cesbron et al., 2016). Another species occurring
>63 μm fraction, evidencing a slight decrease in the environmental at these stations with lower relative abundances is Ammonia parkin
quality but not changing the EcoQS (moderate). Again, the same is soniana. This species, typical of shallow environments was previously
observed for station 33 considering the >63 μm, passing from 1.28 reported as sensitive to heavy metal and organic matter (Damak et al.,
(Table 5) to 1.26 (Table 6). 2019) and usually restricted to clean to modestly polluted environments
(Frontalini and Coccioni, 2011). Psammophaga spp. and Leptoalysis scottii
characterise the finer (63–150 μm) size fraction at station 35. Sabbatini
et al. (2012) previously recognised that both species show an opportu
nistic behaviour in response to organic matter inputs of high nutrition
quality and our analysis supports this finding.
8
Farther from the coast (stations 28, 26 and 25), benthic foraminiferal of the total assemblage is not assigned to a definite ecological category.
abundance and diversity (H′ index) increase, whereas the BPC in the We observed high percentages of NA in most of the stations: the values
sediment decreases, as well as the PRT/CHO ratio as stated previously. exceed 20% in three stations for the >150 μm size fraction, and in four
This, combined with Eh values higher than in the previous stations, stations when the total fraction >63 μm is considered. In the present
suggests a relatively higher availability of oxygen at the surface sedi work, the majority of the Foram-AMBI values should be evaluated with
ment but it contrasts with the finer grain size (clay) observed at stations care as recommended by Borja and Muxika (2005). Therefore, the need
28 and 26. The high foraminiferal abundance observed in the first to assign more species to their respective ecological groups to reduce the
centimetre of sediment might also reflect the possible reduction of other NA percentage is mandatory.
stressful environmental conditions (i.e., sediment resuspension due to Furthermore, the station showing the lowest number of NA species is
the increased water depth and slower sedimentation). In this regard, the that with the highest density, and this is mainly due to the contribution
coarser size assemblages (>150 μm) of these stations are characterised of the finer size fraction. This highlights the relevant contribution of the
by the agglutinated species Textularia agglutinans, previously observed in 63–150 μm fraction in both ecological and biomonitoring studies, even if
nutrient-poor area, less influenced by rivers inputs (e.g., Donnici and the analysis of the finer fraction is often overlooked because it is time-
Serandrei Barbero, 2002). Another dominant species in these stations is consuming (Schönfeld et al., 2012). As reported in this survey, and by
the calcareous Uvigerina mediterranea. This species has been classified as previous studies (e.g., Diz, 2004; Nardelli et al., 2018), the finest fraction
an “indifferent species” to organic enrichment in the Foram-AMBI list (63–150 μm) includes the highest proportion of living foraminifera.
(Jorissen et al., 2018) and it is a species usually found at deeper water Some ecologically significant species may exclusively occur in the
depth (Murray, 2006). Therefore, the presence of U. mediterranea in the 63–150 μm size fraction and, consequently, studies based only on the
outer part of the Gulf is probably more related to the water depth instead coarser size fraction may lack important information (Lo Giudice Cap
of organic matter decrease or maybe both. pelli and Austin, 2019). Moreover, the 63–150 μm fauna often consists of
juveniles and small opportunistic taxa that quickly respond to eutro
4.2. Foram-AMBI sensitivity phication (e.g., Mojtahid et al., 2006).
Consequently, the opportunistic behaviour or sensitivity of small-
This study is one of the first attempts to apply the recently developed size species to increased organic matter accumulation can only be
Foram-AMBI index (Jorissen et al., 2018) adapted to the Mediterranean observed considering this fraction. Once again, analyses conducted only
faunas to evaluate the Ecological Quality Status (EcoQS) of coastal on the coarser fraction may cause under-representation or even absence
marine environments. This index is based on species sensitivity or of indicative species (Duchemin et al., 2007). The finer fraction better
tolerance to environmentally stressful conditions, primarily determined represents soft-shelled taxa, but these taxa are frequently excluded from
by organic enrichment. All the Foram-AMBI values obtained, fall within biomonitoring programs (Schönfeld et al., 2012) and the evaluation of
the interval 1.73–3.38 (Tables 3, 6) indicative of “slightly polluted” or EcoQS using Foram-AMBI and FSI indices. We suggest a reassessment
“meanly polluted” environment (Borja et al., 2003) and corresponding considering that some soft-shelled opportunistic species (e.g., Psammo
to good or moderate EcoQS, respectively. The scores of the index either phaga spp.; Sabbatini et al., 2012) can provide a precise evaluation of the
considering the different size fractions or including soft-shelled fora environmental quality concerning the organic enrichment.
minifera do not change. The only shift from good to moderate EcoQS is Although we encountered some critical issues in the Foram-AMBI
observed for station 35 when soft-shelled foraminifera are included. The application, especially the high NA percentage (from 13 to 44%) and
limited variation of TOC content along the transect may explain the the use of only the coarser size fraction, our results suggest the sensi
relatively small range of index scores. The correlation found in this study tivity of this index to represent the organic matter distribution. In
between TOC content and the index is consistent with the results ob particular, referring to the observed correlation between the reduction
tained by Alve et al. (2016), further confirming the validity of the spe of sediment organic matter values together with the slightly decreasing
cies assignments based on organic enrichment. However, a stronger trend of Foram-AMBI scores along the studied transect (Fig. 3 and
relationship was found between the index value and BPC concentration. Table 4). However, in the present study, it seems that the Foram-AMBI
This observation, and the fact that the BPC is considered more repre score does not fully reflect the potential environmental stress caused
sentative of the benthic trophic status than the TOC (Pusceddu et al., by the organic enrichment; in fact, our stations result all in a good EcoQS
2009), suggests that this variable better explains the benthic forami beside the high organic matter values of biopolymeric carbon recorded
niferal distribution. The benthic trophic status can be evaluated in terms in the transect. In marine sediment, our BPC values (4–6 mgC g− 1) are
of TOC supply rate to the sea bottom (as gC m− 2 yr− 1; Nixon, 1995). associated at highly productive systems (such as estuaries, ponds, and
However, this is difficult to assess since the magnitude of the organic fish farm sediments) in coastal eutrophic environments (Pusceddu et al.,
carbon fluxes is not always directly linked to the primary production in 2009). El Kateb et al. (2020) already highlighted that the Foram-AMBI
the water column, and the assessment of all of the possible inputs of just reflects the organic matter sedimentary distribution (considering
organic carbon is difficult to achieve on large spatial and temporal scales the TOC), further confirming our findings and they underlined that this
(Lee et al., 1988). BPC is significantly related to TOC. However, while index underestimates the ecological conditions along the Tunisian coast
the biopolymeric fraction undergoes rapid changes in quantity and affected by intense anthropogenic pollution. Besides, they confirm also
composition during early diagenesis, TOC generally exhibits a more that the application of the Foram-AMBI is presently not appropriate to
conservative nature (Fabiano et al., 1995). This fact suggests that assess the EcoQS since a large percentage of the present species are not
changes in the BPC quantity might respond to changes and/or differ assigned to ecological groups. Finally, our results confirm also that the
ences in the systems’ productivity more promptly than TOC. TOC con
tent was selected as a proxy for the stress level on benthic communities
Table 3
because it is one of the most used environmental variables in forami
Sediment heavy metal concentrations (expressed in mg kg− 1) for each station.
niferal studies (Alve et al., 2016). Nevertheless, our data suggest that the
foraminiferal species assignment into the ecological groups can be Stations Heavy metals concentrations (mg kg− 1)
improved using the BPC as a more sensitive proxy for benthic trophic 35 33 28 26 25
status in further studies (Pusceddu et al., 2009). As 14 16 24 23 22
The major issue in applying the Foram-AMBI is the high number of Cr 102 109 112 126 135
Not Assigned specimens (NA). Indeed, Jorissen et al. (2018) assigned Hg 0.05 0.07 0.08 0.05 0.03
only 199 common Mediterranean benthic foraminiferal taxa to the five Ni 49 59 65 79 92
Pb 21 23 26 27 27
ecological categories considered. Our analysis highlights that 13 to 44%
9
Table 4
From left to right: the five ecological quality status (EcoQS) classes, the correspondent Foram-AMBI intervals and the pollution clas
sification following Borja et al. (2003). The percentages of not assigned specimens (NA), Foram-AMBI values, Shannon- Wiener index
(H′ ) calculated excluding soft-shelled foraminifera for the larger size fraction (>150 μm) and for the small plus large size fraction (>63
μm). Dot colour corresponds to the EcoQS code.
Foram-AMBI Pollution > 150 µm > 63 µm

EcoQS Stations
score classification NA (%) Foram-AMBI H' NA (%) Foram-AMBI H'
High x ≤ 1.2 Unpolluted 35 17.6 2.62 2.2 43.6 3.20 2.9
Good 1.2 < x ≤ 3.3 Slightly polluted 33 36.4 3.00 2.3 20.4 2.93 3.2
Moderate 3.3 < x ≤ 4.3 Meanly polluted 28 13.5 2.54 2.9 20.7 2.77 3.1
Poor 4.3 < x ≤ 5.5 Heavily polluted 26 21.3 1.73 3.1 12.8 2.71 3.1
Bad 5.5 < x ≤ 6.0 Extremely polluted 25 44.3 1.83 3.6 33.2 2.46 3.5
Table 5
The five ecological quality status (EcoQS) classes, the correspondent FSI intervals and the pollution classification
following Dimiza et al. (2016). The percentages of not assigned individuals (NA), FSI values, for the larger size fraction
(>150 μm) and for the small plus large size fraction (>63 μm). Dot colour corresponds to the EcoQS code.
Pollution > 150 µm > 63 µm

EcoQS FSI score Stations
classification NA (%) FSI NA (%) FSI
High 9.0 ≤ x ≤ 10.0 Normal/Pristine 35 17.5 2.04 40.7 2.93
Good 5.5 ≤ x < 9.0 Slightly polluted 33 45.5 4.00 31.8 1.28
Moderate 2.0 ≤ x < 5.5 Moderately polluted 28 51.0 1.58 52.7 1.42
Poor 1.0 ≤ x < 2.0 Heavily polluted 26 45.8 4.99 27.5 3.61
Bad x < 1.0 Azoic 25 44.3 6.19 35.3 3.81
Foram-AMBI does not effectively reflect EcoQS as the AMBI of Borja between 1.26 and 6.19 (Tables 5, 6). The EcoQS obtained using the
et al. (2000) does for macrofauna. Moreover, Bouchet et al. (2018) coarser size fraction of the assemblage, results good at station 25,
compared EcoQS obtained with benthic foraminifera to previous studies moderate at station 35, 33 and 26 and poor at station 28 highlighting a
that assessed EcoQS in the same areas using indices based on benthic variable score for the FSI along the transect. A different result is obtained
macrofauna (Borja et al., 2000). By comparing EcoQS assessment ob when we consider the total assemblage (>63 μm): the EcoQS results
tained using the foraminiferal method with those calculated with mac moderate at station 35, 26 and 25, while it becomes poor at stations 33
rofaunal methods, they demonstrated that benthic foraminifera might and 28 in the inner part of the Gulf of Manfredonia. The inclusion in the
be more appropriate than benthic macrofauna to evaluate the health of FSI index of the 63–150 μm assemblage, lower all the scores (except for
Italian transition waters accurately. So, foraminifera are candidates, station 35) and the consequent classification in a worse EcoQS class at
better than macrofauna, to be very promising bioindicators but there is station 33. However, this apparent impoverishment of the environ
not a clear discrepancy between EcoQS limits defined by macrofauna mental quality obtained for the >63 μm size fraction should be evalu
and foraminifera. ated with care. In fact, the abundance of the species considered to
calculate the FSI index at each station is lower than 53% of the total
4.3. Foram stress index (FSI) sensitivity assemblage both considering the total >63 μm or only the coarser size
fraction. Nevertheless, the scores obtained depend on the fact that we
The biotic index called Foram Stress Index (FSI) is based on the calculated the index using only the species or genera included by Dimiza
assignment of foraminiferal species to two ecological groups based on et al. (2016) (with the addition of E. scaber following El Kateb et al.,
their tolerance or sensitivity to organic enrichment (Dimiza et al., 2016). 2020) whose assignments to the sensitive or stress-tolerant group are
The values we obtained from the application of the FSI index falls based on the literature. This fact determines the low relative abundances
of the assemblage used to calculate the FSI index. Furthermore, when
Table 6 the two soft-shelled foraminifera genera are included as a stress-tolerant
Comparison between Foram-AMBI and FSI scores considering soft-shelled group in the FSI index, we observe a slight decrease in the index score for
foraminifera for both >150 μm and >63 μm size fractions. Values station 35 and 33. However, the inclusion of these two taxa does not
affected by the inclusion of soft-shelled foraminifera in the indices are change the EcoQS of these two stations.
marked in bold. Dot colours correspond to the EcoQS code. As for the Foram-AMBI, the FSI index reflects the organic enrich
Foram-AMBI FSI ment: a negative correlation is observed between the FSI scores and the
Stations TOC content (Fig. 6d). The correlation is weaker between the FSI and the
> 150 µm > 63 µm > 150 µm > 63 µm
BPC (Fig. 6e). Moreover, the obtained FSI scores show a correlation with
35 2.76 3.38 1.96 2.66 the H′ index only when the coarser fraction is used. Summarising the
33 3.00 3.16 4.00 1.26 findings, if we consider the percentage of species assignments, it is
28 2.54 2.77 1.58 1.42 evident that also in this case there is a methodological limitation due to
26 1.73 2.71 4.99 3.61 the species included in the list of Dimiza et al. (2016).
25 1.83 2.46 6.19 3.81
10
4.4. Indices comparison and heavy metals concentrations Credit authorship contribution statement
The Foram-AMBI and the FSI indices are based on two different spe Eleonora Fossile: Conceptualization, Methodology, Validation,
cies classification in ecological groups and two different formula, but both Formal analysis, Investigation, Writing - Original Draft. Anna Sabba
species assignments are based on their sensitivity to organic enrichment tini: Conceptualization, Methodology, Validation, Investigation, Re
(Alve et al., 2016; Dimiza et al., 2016; Jorissen et al., 2018). Thus, from sources, Writing - Review & Editing, Supervision. Federico Spagnoli:
the application of these two indices, similar EcoQS are expected. On the reference person for geochemistry and sedimentology. Methodoloy,
contrary, we observe an impoverishment of the environmental quality Investigation, Resource, Writing - Review & Editing. Francesca Caridi:
when we apply the FSI index. In this study, we used two different vari Methodology, Interpretation Analysis. Antonio Dell’Anno: Methodol
ables to assess organic enrichment: TOC and BPC concentrations. As ogy, Writing- Review & Editing. Rocco De Marco: Methodology. Enrico
shown in Fig. 6, both variables show a correlation with the Foram-AMBI Dinelli: Methodology. Elisa Droghini: Methodology. Mario Tra
and the FSI scores. This correlation is stronger between the Foram-AMBI montana: Methodology. Alessandra Negri: Conceptualization, Writing
and the BPC and between the FSI and the TOC content. The difference - Review & Editing, Supervision.
between the two indices may depend on the different species assignments,
the percentage of the assemblage considered in the calculation or the Declaration of competing interest
different formula used. As mentioned earlier, the major issue in applying
both indices is the high percentages of foraminifera not included in the The authors declare that they have no known competing financial
evaluation of the EcoQS. Our results suggest that both the Foram-AMBI interests or personal relationships that could have appeared to influence
and the FSI are good tools to evaluate the EcoQS in the Mediterranean the work reported in this paper.
Sea because they seem to reflect the organic enrichment. However, there
is the need to extend the list of the species assigned to both indices and it Acknowledgements
may be necessary to adapt the coefficients in the Foram-AMBI formula as
previously suggested by El Kateb et al. (2020). We are grateful to Giuseppe Caccamo, Simone Baldelli, Elisa Man
The heavy metal concentration slightly increases from the coast to the zotti, Andrea Castelli, Massimo Leonetti and the crew of the R/V Dal
open sea, but it seems to not influence the foraminiferal distribution along laporta for their precious help in the cruise activities. We thank Marco
the transect. Foraminiferal responses to heavy metal pollution are still Lo Martire and Giuseppe Toscano for the help in organic matter analyses
unclear. Experimental studies have shown ultrastructural changes and and Anna Annibaldi for Hg analysis. We thank the two anonymous re
intracellular modification in foraminifera exposed to heavy metals (e.g., viewers for their constructive and useful comments.
Frontalini et al., 2016, 2018a), while others have shown effects at the
ecological level (e.g., Frontalini et al., 2018b). Miliolids, for instance, Appendix A. Supplementary data
have shown contradictory responses to heavy metal pollution (Nardelli
et al., 2016 and reference therein). Frontalini and Coccioni (2008) Supplementary data to this article can be found online at doi:https://
underlined a possible control of heavy metals on benthic foraminiferal doi.org/10.1016/j.marpolbul.2020.111933.
assemblages and test malformation development. Our study did not
observe test malformations and foraminiferal diversity seems to increase References
in the outer part of the transect even if heavy metals concentrations
progressively increase. These observations highlight that a thorough Alve, E., Lepland, A., Magnusson, J., Backer-Owe, K., 2009. Monitoring strategies for re-
environmental quality evaluation needs to be assessed using biological establishment of ecological reference conditions: possibilities and limitations. Mar.
Pollut. Bull. 59, 297–310. https://doi.org/10.1016/j.marpolbul.2009.08.011.
elements supported by abiotic variables. Furthermore, the use of multiple
Alve, E., Korsun, S., Schönfeld, J., Dijkstra, N., Golikova, E., Hess, S., Husum, K.,
bioindicators at different trophic levels (e.g., foraminifera and macro Panieri, G., 2016. Foram-AMBI: a sensitivity index based on benthic foraminiferal
fauna) can give a complete evaluation of the EcoQS. faunas from North-East Atlantic and Arctic fjords, continental shelves and slopes.
Mar. Micropaleontol. 122, 1–12. https://doi.org/10.1016/j.marmicro.2015.11.001.
Alve, E., Hess, S., Bouchet, V.M.P., Dolven, J.K., Rygg, B., 2019. Intercalibration of
benthic foraminiferal and macrofaunal biotic indices: an example from the
5. Conclusions Norwegian Skagerrak coast (NE North Sea). Ecol. Indic. 96, 107–115. https://doi.
org/10.1016/j.ecolind.2018.08.037.
Armynot du Châtelet, É., Debenay, J.P., 2010. The anthropogenic impact on the western
The application of two foraminifera-based indices, the Foram-AMBI French coasts as revealed by foraminifera: a review. Rev. Micropaleontol. 53,
(Jorissen et al., 2018) and the FSI (Dimiza et al., 2016) to evaluate the 129–137. https://doi.org/10.1016/j.revmic.2009.11.002.
Barras, C., Jorissen, F.J., 2011. Étude des faunes de foraminifères benthiques de la côte
EcoQS in the Gulf of Manfredonia (Southern Adriatic Sea, Italy), led to
méditerranéenne française : mise en place d’un nouvel indice biotique dans le cadre
different outcomes. The study area results in good EcoQS when the de 41 Directive Cadre Eau - Campagne DCE 2009. In: Laboratoire des Bio-Indicateurs
Foram-AMBI is applied, while a general impoverishment of the EcoQS Actuels et Fossiles (BIAF) Université d’Angers, Angers, France.
(moderate or poor) is obtained from the application of the FSI. Both Barras, C., Jorissen, F.J., Labrune, C., Andral, B., Boissery, P., 2014. Live benthic
foraminiferal faunas from the French Mediterranean coast: towards a new biotic
indices correlate well with the organic matter distribution but the per index of environmental quality. Ecol. Indic. 36, 719–743. https://doi.org/10.1016/j.
centages of Not Assigned specimens is still too high to allow a correct ecolind.2013.09.028.
interpretation of the EcoQS. Thus, an improvement of the species as Borja, A., Muxika, I., 2005. Guidelines for the use of AMBI (AZTI’s marine biotic index)
in the assessment of the benthic ecological quality. Mar. Pollut. Bull. 50, 787–789.
signments for both indices is critical to guarantee an effective evaluation https://doi.org/10.1016/j.marpolbul.2005.04.040.
of the EcoQS in biomonitoring surveys. Additionally, the observed con Borja, A., Franco, J., Pérez, V., 2000. A marine biotic index to establish the ecological
centrations of heavy metals seem to not affect the foraminiferal assem quality of soft-bottom benthos within European estuarine and coastal environments.
Mar. Pollut. Bull. 40, 1100–1114. https://doi.org/10.1016/S0025-326X(00)00061-
blages, especially in the most external stations. Consequently, for a 8.
complete overview of the area’s environmental status, we suggest the Borja, A., Muxika, I., Franco, J., 2003. The application of a marine biotic index to
application of biotic indices together with the evaluation of environ different impact sources affecting soft-bottom benthic communities along European
coasts. Mar. Pollut. Bull. 46, 835–845. https://doi.org/10.1016/S0025-326X(03)
mental parameters, including organic matter composition (i.e. BPC) and
00090-0.
heavy metals. Bouchet, V.M.P., Alve, E., Rygg, B., Telford, R.J., 2012. Benthic foraminifera provide a
promising tool for ecological quality assessment of marine waters. Ecol. Indic. 23,
66–75. https://doi.org/10.1016/j.ecolind.2012.03.011.
Bouchet, V.M.P., Goberville, E., Frontalini, F., 2018. Benthic foraminifera to assess
ecological quality statuses in Italian transitional waters. Ecol. Indic. 84, 130–139.
https://doi.org/10.1016/j.ecolind.2017.07.055.
11
Cattaneo, A., Correggiari, A., Langone, L., Trincardi, F., 2003. The late-Holocene foraminifer ammonia parkinsoniana. PLoS ONE 11. https://doi.org/10.1371/
Gargano subaqueous delta, Adriatic shelf: sediment pathways and supply journal.pone.0162401.
fluctuations. Mar. Geol. 193, 61–91. https://doi.org/10.1016/S0025-3227(02) Frontalini, F., Nardelli, M.P., Curzi, D., Sabbatini, A., Negri, A., Losada, M.T., Gobbi, P.,
00614-X. Coccioni, R., Bernhard, J.M., 2018a. Benthic foraminiferal ultrastructural alteration
Celia Magno, M., Bergamin, L., Finoia, M.G., Pierfranceschi, G., Venti, F., Romano, E., induced by heavy metals. Mar. Micropaleontol. 138, 83–89. https://doi.org/
2012. Correlation between textural characteristics of marine sediments and benthic 10.1016/j.marmicro.2017.10.009.
foraminifera in highly anthropogenically-altered coastal areas. Mar. Geol. 315–318, Frontalini, F., Semprucci, F., Bella, D., Caruso, A., Cosentino, C., Maccotta, A.,
143–161. https://doi.org/10.1016/j.margeo.2012.04.002. Coccioni, R., 2018b. The response of cultured Meiofaunal and benthic Foraminiferal
Cesbron, F., Geslin, E., Jorissen, F.J., Delgard, M.L., Charrieau, L., Deflandre, B., communities to Lead exposure : results from Mesocosm experiments. Environ.
Jézéquel, D., Anschutz, P., Metzger, E., 2016. Vertical distribution and respiration Toxicol. Chemestry 37, 2439–2447. https://doi.org/10.1002/etc.4207.
rates of benthic foraminifera: contribution to aerobic remineralisation in intertidal Hammer, Ø., Harper, D., Ryan, P.D., 2001. PAST: palaeontologi- cal statistics software
mudflats covered by Zostera noltei meadows. Estuar. Coast. Shelf Sci. 179, 23–38. package for education and data analysis. Palaeontol. Electron. 4, 1–9.
https://doi.org/10.1016/j.ecss.2015.12.005. Hylland, K., Robinson, C.D., Burgeot, T., Martínez-Gómez, C., Lang, T., Svavarsson, J.,
Christophoridis, C., Bourliva, A., Evgenakis, E., Papadopoulou, L., Fytianos, K., 2019. Thain, J.E., Vethaak, A.D., Gubbins, M.J., 2017. Integrated chemical and biological
Effects of anthropogenic activities on the levels of heavy metals in marine surface assessment of contaminant impacts in selected European coastal and offshore marine
sediments of the Thessaloniki Bay, northern Greece: spatial distribution, sources and areas. Mar. Environ. Res. 124, 130–138. https://doi.org/10.1016/j.
contamination assessment. Microchem. J. 149, 104001. https://doi.org/10.1016/j. marenvres.2016.05.014.
microc.2019.104001. Jorissen, F., Nardelli, M.P., Almogi-Labin, A., Barras, C., Bergamin, L., Bicchi, E., El
Cushman, J.A., 1950. Foraminifera. Their Classification and Economic Use. Harvard Kateb, A., Ferraro, L., McGann, M., Morigi, C., Romano, E., Sabbatini, A.,
University Press, Cambridge, MA (605 pp). Schweizer, M., Spezzaferri, S., 2018. Developing Foram-AMBI for biomonitoring in
Damak, M., Frontalini, F., Elleuch, B., Kallel, M., 2019. Benthic foraminiferal the Mediterranean: species assignments to ecological categories. Mar.
assemblages as pollution proxies along the coastal fringe of the Monastir Bay Micropaleontol. 140, 33–45. https://doi.org/10.1016/j.marmicro.2017.12.006.
(Tunisia). J. African Earth Sci. 150, 379–388. https://doi.org/10.1016/j. Karydis, M., Kitsiou, D., 2012. Eutrophication and environmental policy in the
jafrearsci.2018.11.013. Mediterranean Sea: a review. Environ. Monit. Assess. 184, 4931–4984. https://doi.
Danovaro, R., 2009. Methods for the Study of Deep-Sea Sediments, Their Functioning org/10.1007/s10661-011-2313-2.
and Biodiversity. CRC Press, Boca Raton. Kennedy, M.J., Pevear, D.R., Hill, J.R., 2002. Mineral surface control of organic carbon in
Danovaro, R., Gambi, C., Mirto, S., Sandulli, R., Ceccherelli, V.U., 2003. Meiofauna. In: black shale. Science 295, 657–660. https://doi.org/10.1126/science.1066611.
Manuale di Metodologie di campionamento e studio del benthos marino Khan, M., Mohammad, F., 2014. Eutrophication: challenges and solutions. In: Ansari, A.,
mediterraneo. Eds. Gambi M.C., Dappiano M. Biol. Mar. Mediterr. 10, 61–108. Gill, S. (Eds.), Eutrophication: Causes, Consequences and Control. Springer,
Dauwe, B., Middelburg, J.J., Herman, P.M.J., 2001. Effect of oxygen on the degradability Dordrecht. https://doi.org/10.1007/978-94-007-7814-6_1.
of organic matter in subtidal and intertidal sediments of the North Sea area. Mar. Lee, C., Wakeham, S.G., Hedges, J., 1988. The measurement of oceanic particle flux - are
Ecol. Prog. Ser. 215, 13–22. https://doi.org/10.3354/meps215013. “swimmers” a problem? Oceanography 1 (2), 34–36. https://doi.org/10.5670/
De Jonge, V.N., 1980. Fluctuations in the organic carbon to chlorophyll a ratios for oceanog.1988.06.
estuarine benthic diatom populations. Mar. Ecol. Prog. Ser. 2, 345–353. https://doi. Leoni, L., Saitta, M., 1976. X-ray fluorescence analysis of 29 trace elements in rock and
org/10.3354/meps002345. mineral standard. Rend. Soc. Ital. Mineral. Petrol. 32, 497–510.
Dimiza, M.D., Triantaphyllou, M.V., Koukousioura, O., Hallock, P., Simboura, N., Leoni, L., Menichini, M., Saitta, M., 1982. Determination of S, Cl and F in silicate rocks by
Karageorgis, A.P., Papathanasiou, E., 2016. The Foram Stress Index: a new tool for X-ray fluorescence analyses. X-Ray Spectrom. 11, 156–158. https://doi.org/
environmental assessment of soft-bottom environments using benthic foraminifera. 10.1002/xrs.1300110404.
A case study from the Saronikos Gulf, Greece, Eastern Mediterranean. Ecol. Indic. 60, Lo Giudice Cappelli, E., Austin, W.E.N., 2019. Size matters: analyses of benthic
611–621. https://doi.org/10.1016/j.ecolind.2015.07.030. foraminiferal assemblages across differing size fractions. Front. Mar. Sci. 6
Diz, P., 2004. Distribution of benthic foraminifera in coarse sediments, Ria De Vigo, Nw (December), 1–8. https://doi.org/10.3389/fmars.2019.00752.
Iberian margin. J. Foraminifer. Res. 34, 258–275. https://doi.org/10.2113/ Loeblich, A.R., Tappan, H., 1987. Foraminiferal geNera and Their Classification, 2. Van
34.4.258. Nostrand Reinhold Co., New York (970 pp. (v. 1) + 847 pls (v. 2)).
Dolven, J.K., Alve, E., Rygg, B., Magnusson, J., 2013. Defining past ecological status and Lorenzen, C.J., Jeffrey, S.W., 1980. Determination of chlorophyll in seawater. UNESCO
in situ reference conditions using benthic foraminifera: a case study from the Tech. Pap. Mar. Sci. 35, 1–20.
Oslofjord, Norway. Ecol. Indic. 29 (2013), 219–233. https://doi.org/10.1016/j. Martins, M.V.A., Silva, F., Laut, L.L.M., Frontalini, F., Clemente, I.M.M.M., Miranda, P.,
ecolind.2012.12.031. Figueira, R., Sousa, S.H.M., Dias, J.M.A., 2015. Response of benthic foraminifera to
Donnici, S., Serandrei Barbero, R., 2002. The benthic foraminiferal communities of the organic matter quantity and quality and bioavailable concentrations of metals in
northern Adriatic continental shelf. Mar. Micropaleontol. 44, 93–123. https://doi. Aveiro Lagoon (Portugal). PLoS One 10, 1–23. https://doi.org/10.1371/journal.
org/10.1016/S0377-8398(01)00043-3. pone.0118077.
Droghini, E., Annibaldi, A., Prezioso, E., Tramontana, M., Frapiccini, E., De Marco, R., Mendes, I., Gonzalez, R., Dias, J.M.A., Lobo, F., Martins, V., 2004. Factors influencing
Illuminati, S., Truzzi, C., Spagnoli, F., 2019. Mercury content in central and southern recent benthic foraminifera distribution on the Guadiana shelf (Southwestern
Adriatic Sea sediments in relation to seafloor geochemistry and sedimentology. Iberia). Mar. Micropaleontol. 51, 171–192. https://doi.org/10.1016/j.
Molecules 24, 1–16. https://doi.org/10.3390/molecules24244467. marmicro.2003.11.001.
Duchemin, G., Fontanier, C., Jorissen, F.J., Barras, C., Griveaud, C., 2007. Living small- Mojtahid, M., Jorissen, F., Durrieu, J., Galgani, F., Howa, H., Redois, F., Camps, R., 2006.
sized (63–150 μm) foraminifera from mid-shelf to mid-slope environments in the Bay Benthic foraminifera as bio-indicators of drill cutting disposal in tropical East
of Biscay. J. Foraminifer. Res. 37 (1), 12–32. https://doi.org/10.2113/gsjfr.37.1.12. Atlantic outer shelf environments. Mar. Micropaleontol. 61, 58–75. https://doi.org/
El Kateb, A., Stalder, C., Martínez-Colón, M., Mateu-Vicens, G., Francescangeli, F., 10.1016/j.marmicro.2006.05.004.
Coletti, G., Stainbank, S., Spezzaferri, S., 2020. Foraminiferal-based biotic indices to Murray, J.W., 2006. Ecology and Application of Benthic Foraminifera. Cambridge
assess the ecological quality status of the Gulf of Gabes (Tunisia): present limitations University Press, Cambridge, New York. https://doi.org/10.1017/
and future perspectives. Ecol. Indic. 111, 105962. https://doi.org/10.1016/j. CBO9780511535529.
ecolind.2019.105962. Musco, M., Cuttitta, A., Bicchi, E., Quinci, E.M., Sprovieri, M., Tranchida, G.,
Fabiano, M., Danovaro, R., Fraschetti, S., 1995. A three-year time series of elemental and Giaramita, L., Traina, A., Salvagio Manta, D., Gherardi, S., Mercurio, P., Siragusa, A.,
biochemical composition of organic matter in subtidal sandy sediments of the Mazzola, S., 2017. Benthic foraminifera as bio-indicators of anthropogenic impacts
Ligurian Sea (northwestern Mediterranean). Cont. Shelf Res. 15, 1453–1469. in coastal environments: Acqua dei Corsari area case study (Palermo, Italy). Mar.
https://doi.org/10.1016/0278-4343(94)00088-5. Pollut. Bull. 117, 75–87. https://doi.org/10.1016/j.marpolbul.2017.01.032.
Focardi, S., Specchiulli, A., Spagnoli, F., Fiesoletti, F., Rossi, C., 2009. A combinated Nardelli, M.P., Malferrari, D., Ferretti, A., Bartolini, A., Sabbatini, A., Negri, A., 2016.
approach to investigate the biochemistry and hydrography of a shallow bay in the Zinc incorporation in the miliolid foraminifer Pseudotriloculina rotunda under
South Adriatic Sea: The Gulf of Manfredonia (Italy). Environmental Monitoring and laboratory conditions. Mar. Micropaleontol. 126, 42–49. https://doi.org/10.1016/j.
Assessment 153, 209–220. https://doi.org/10.1007/s10661-008-0350-2. marmicro.2016.06.001.
Franzini, M., Leoni, L., Saitta, M., 1972. A simple method to evaluate the matrix effects in Nardelli, M.P., Sabbatini, A., Bonnot, E., Mea, M., Pusceddu, A., Danovaro, R., Durrieu de
X-ray fluorescence analysis. X-Ray Spectrom. 1, 151–154. https://doi.org/10.1002/ Madron, X., Negri, A., Bicchi, E., 2018. Benthic foraminiferal assemblages in the Cap
xrs.1300010406. de Creus canyon and adjacent open slope: Potential influence of dense shelf water
Franzini, M., Leoni, L., Saitta, M., 1975. Revisione di una metodologia analitica per cascading and open-ocean convection. Deep. Res. Part I Oceanogr. Res. Pap. 136,
fluorescenza-X, basata sulla correzione completa degli effetti di matrice. Rend. Soc. 31–43. https://doi.org/10.1016/j.dsr.2018.04.010.
Ital. Mineral. Petrol. 31 (365–378), 1975. Nixon, S.W., 1995. Coastal marine eutrophication: a definition, social causes, and future
Frontalini, F., Coccioni, R., 2008. Benthic foraminifera for heavy metal pollution concerns. Ophelia 41, 199–219.
monitoring: a case study from the Central Adriatic Sea coast of Italy. Estuar. Coast. Plante-Cuny, M.R., 1974. Evaluation par spectrophotométrie des teneurs en chlorophylle
Shelf Sci. 76, 404–417. https://doi.org/10.1016/j.ecss.2007.07.024. “a” fonctionnelle et en phéopigments des substrats meubles marins, Doc. Sci. la
Frontalini, F., Coccioni, R., 2011. Benthic foraminifera as bioindicators of pollution: a Mission l’O.R.S.T.O.M. à Nosy-Bé, 45, p. 76.
review of Italian research over the last three decades. Rev. Micropaleontol. 54, Powley, H.R., Dürr, H.H., Lima, A.T., Krom, M.D., Van Cappellen, P., 2016. Direct
115–127. https://doi.org/10.1016/j.revmic.2011.03.001. discharges of domestic wastewater are a major source of phosphorus and nitrogen to
Frontalini, F., Curzi, D., Cesarini, E., Canonico, B., Giordano, F.M., De Matteis, R., the Mediterranean Sea. Environ. Sci. Technol. 50 (16), 8722–8730. https://doi.org/
Bernhard, J.M., Pieretti, N., Gu, B., Eskelsen, J.R., Jubb, A.M., Zhao, L., Pierce, E.M., 10.1021/acs.est.6b01742.
Gobbi, P., Papa, S., Coccioni, R., 2016. Mercury-pollution induction of intracellular
lipid accumulation and lysosomal compartment amplification in the benthic
12
Pusceddu, A., Dell’Anno, A., Fabiano, M., 2000. Organic matter composition in coastal Søndergaard, M., 2009. Redox potential. In: Likens, Gene E. (Ed.), Encyclopedia of Inland
sediments at Terra Nova Bay (Ross Sea) during summer 1995. Polar Biol. 23, Waters. Academic Press, pp. 852–859. https://doi.org/10.1016/B978-012370626-
288–293. https://doi.org/10.1007/s003000050446. 3.00115-0.
Pusceddu, A., Dell’Anno, A., Fabiano, M., Danovaro, R., 2009. Quantity and Spagnoli, F., Bartholini, G., Dinelli, E., Giordano, P., 2008. Geochemistry and particle
bioavailability of sediment organic matter as signatures of benthic trophic status. size of surface sediments of gulf of Manfredonia (southern Adriatic Sea). Estuar.
Mar. Ecol. Prog. Ser. 375, 41–52. https://doi.org/10.3354/meps07735. Coast. Shelf Sci. 80, 21–30. https://doi.org/10.1016/j.ecss.2008.07.008.
R Core Team, 2020. R: A Language and Environment for Statistical Computing. R Spagnoli, F., Dell’Anno, A., de Marco, A., Dinelli, E., Fabiano, M., Gadaleta, M.V.,
Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Ianni, C., Loiacono, F., Manini, E., Marini, M., Mongelli, G., Rampazzo, G.,
Roussiez, V., Ludwig, W., Monaco, A., Probst, J.L., Bouloubassi, I., Buscail, R., Rivaro, P., Vezzulli, L., 2010. Biogeochemistry, grain size and mineralogy of the
Saragoni, G., 2006. Sources and sinks of sediment-bound contaminants in the Gulf of central and southern Adriatic sea sediments: a review. Chem. Ecol. 26, 19–44.
lions (NW Mediterranean Sea): a multi-tracer approach. Cont. Shelf Res. 26 (16), https://doi.org/10.1080/02757541003689829.
1843–1857. https://doi.org/10.1016/j.csr.2006.04.010. Tselepides, A., Polychronaki, T., Marrale, D., Akoumianaki, I., Dell’Anno, A.,
Sabbatini, A., Bonatto, S., Bianchelli, S., Pusceddu, A., Danovaro, R., Negri, A., 2012. Pusceddu, A., Danovaro, R., 2000. Organic matter composition of the continental
Foraminiferal assemblages and trophic state in coastal sediments of the Adriatic Sea. shelf and bathyal sediments of the Cretan Sea (NE Mediterranean). Prog. Oceanogr.
J. Mar. Syst. 105, 163–174. https://doi.org/10.1016/j.jmarsys.2012.07.009. 46 (2–4), 311–344. https://doi.org/10.1016/S0079-6611(00)00024-0.
Schönfeld, J., Alve, E., Geslin, E., Jorissen, F., Korsun, S., Spezzaferri, S., Abramovich, S., Vilela, C.G., Batista, D.S., Baptista-Neto, J.A., Crapez, M., McAllister, J.J., 2004. Benthic
Almogi-Labin, A., du Chatelet, E.A., Barras, C., Bergamin, L., Bicchi, E., Bouchet, V., foraminifera distribution in high polluted sediments from Niterói Harbor
Cearreta, A., Di Bella, L., Dijkstra, N., Disaro, S.T., Ferraro, L., Frontalini, F., (Guanabara Bay), Rio de Janeiro, Brazil. An. Acad. Bras. Cienc. 76 (1), 161–171.
Gennari, G., Golikova, E., Haynert, K., Hess, S., Husum, K., Martins, V., McGann, M., https://doi.org/10.1590/S0001-37652004000100014.
Oron, S., Romano, E., Sousa, S.M., Tsujimoto, A., 2012. The FOBIMO (FOraminiferal Wentworth, C.K., 1922. A scale of grade and class terms for clastic sediments. J. Geol. 30,
BIo-MOnitoring) initiative-Towards a standardised protocol for soft-bottom benthic 377–392. https://doi.org/10.1086/622910.
foraminiferal monitoring studies. Mar. Micropaleontol. 94–95, 1–13. https://doi. Wickham, H., 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New
org/10.1016/j.marmicro.2012.06.001. York (ISBN 978-3-319-24277-4). https://ggplot2.tidyverse.org.
13

Fossile Et Al. (2021) Gulf of Manfredonia (Southern Adriatic Sea)

Uploaded by

Copyright:

Available Formats

Fossile Et Al. (2021) Gulf of Manfredonia (Southern Adriatic Sea)

Uploaded by

Document Information

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Fossile Et Al. (2021) Gulf of Manfredonia (Southern Adriatic Sea)

Uploaded by

Copyright:

Available Formats

Marine Pollution Bulletin 163 (2021) 111933

Contents lists available at ScienceDirect

Marine Pollution Bulletin

Sensitivity of foraminiferal-based indices to evaluate the ecological quality

1. Introduction Framework Directive (WFD, 2000/60/EC) to protect and monitor

Five stations located along a bathymetric transect were sampled by

35 0.3 0.3 46.1 53.3 0.29 5.18

3.1.3. Trace metals concentrations

3.3.4. Possible assignments of soft-shelled foraminifera 4. Discussion

Foram-AMBI Pollution > 150 µm > 63 µm

Pollution > 150 µm > 63 µm

You might also like