SSRN Id4412792

1 A first study on the use of Rhyssoplax olivacea (Mediterranean Polyplacophora) to biomonitor trace metal
2 contamination.
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4 1) Nacima MESLI1,*
5 2) Omar ROUANE-HACENE2
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6 3) Zoheir BOUCHIKHI-TANI1
7 4) Jonathan RICHIR3,4,*
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9 1 University of Tlemcen Abou Bekr Belkaid, Laboratoire Valorisation des actions de l’Homme pour la
10 protection de l’environnement et application en santé publique (VAHPEASP), Department of Biology, BP
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11 119, 13000 Tlemcen, Algérie ;
12 2 University of Oran 1 Ahmed Ben Bella, Department of Biology, 31000 Oran, Algeria;
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13 3 Station de Recherches Sous-marines et Océanographiques, Punta Revellata, BP33, 20260 Calvi, France
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14 4 SciSca, 5330 Maillen, Belgium.
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16 * Corresponding authors’ e-mail: meslinacima74@gmail.com, jonathan.richir@gmail.com
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18 Abstract
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19 The study involved the first use of Rhyssoplax olivacea (Mediterranean Polyplacophora) for the trace metal
20 contamination assessment (Fe, Cu, Co, Cr and Cd) in shell and soft tissues at five sites along the Algerian west
21 coast during the cold and hot seasons of 2019. The condition index provided information on habitat quality, the
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22 organisms' reproductive performance and physiological status. For the first time, a database compiled all available
23 data on trace element contamination in polyplacophorans. The trace metal contamination status was assessed using
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24 a range of indices; the metal shell weight indices determined the bioavailability of TMs at the sites. The trace
25 element pollution index used alongside the quartile method allowed the assignment of contamination levels to
26 sites. Trace element spatial variation index ranked Cd and Cr as TMs of primary environmental concern based on
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27 overall spatial variability. The study validated R. olivacea as a good bioindicator of TM contamination.
This preprint research paper has not been peer reviewed. Electronic copy available at: https://ssrn.com/abstract=4412792
28 Keywords: Rhyssoplax olivacea; Bioindicator; Trace metal contamination; Mediterranean; Condition index;
29 Pollution indices.
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31 1. Introduction
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32 Over 80% of marine pollution (macro-waste, microplastics, chemicals, etc.) originating from land, urban areas or
33 industrial and agricultural activities, transported by rivers, air, coastal drainage or discharged by sewage treatment
34 plants, ends up in seas and oceans, the ultimate receptacle of anthropogenic pollution (United Nations, 2004; World
35 Wide Fund for Nature, 2015). The complex nature and topography of the semi-enclosed Mediterranean Sea,
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36 leading to unique physiographic and ecological features (Ali et al., 2022), makes it particularly sensitive to
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37 pollution (Ducrocq et al., 2016). About 45% of the population of Algeria (southwestern Mediterranean) lives in
38 coastal areas where more than 50% of the industrial units (petrochemical, chemical, steel and agro-food activities)
39 are concentrated. This population density and industrialisation generates a high level of multiform and multisource
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40 pollution (organic, chemical, thermal, bacterial, etc.) (Grimes, 2010), including because of wastewater discharges
41 into the sea without prior treatment (Benali et al., 2016) and through outfalls.
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42 Coastal pollution causes malfunctions of abiotic and biotic compartments of the coastal environment (Grimes,
43 2010). Contaminants accumulate in sediments and along trophic chains (Thompson et al., 2004; Amiard, 2017),
44 can lead to the long-term decline of aquatic populations and can increase their vulnerability to natural and
45 anthropogenic stressors (Michel et al., 2013). Most Trace Elements (TEs) can be considered as environmental
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46 contaminants (Richir and Gobert, 2013). Because they are considered non-degradable (Navratil and Minarik, 2011;
47 Pan and Wang, 2012), their persistence may alter their natural biogeochemical balance in contaminated
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48 environments (Doney, 2010). Essential Trace Metals (TMs) can be either deficient in too small quantities or toxic
49 when absorbed in high concentrations, whereas only a threshold of toxicity exists for non-essential TMs (Amiard,
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50 2017). Non-essential TMs such as Cd play no physiological role and are often toxic even in very small quantities
51 (Nordberg et al., 2007). With regard to the essential micronutrients Cu and Zn, they are among the most toxic TMs
52 at certain levels (Phillips and Rainbow, 1993). Metal ions can cause toxic effects by substituting for each other in
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53 metabolically important molecules (Prejanò et al, 2020). Because of their toxicity to living organisms and
54 biological processes, the environmental occurrence of TMs must be appropriately monitored. The monitoring of
55 chemicals in the environment can be performed using bioindicator species (Markert et al., 2003; Richir and Gobert,
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56 2013; Costa and Teixeira, 2014). Martin and Coughtrey (1982) define biomonitors as “organisms that provide the
57 means for regular monitoring, and can also be used to quantify a pollutant present in a particular environment”.
58 Biomonitors are thus collected and analysed to measure the amount and bioavailability of contaminants
59 accumulated from the environment in their tissues (Phillips and Rainbow, 1993). Macrozoobenthic communities
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60 are considered as excellent structural bioindicators (Bellan, 1967; Hily, 1984; Bakalem and Romano, 1989; Singh
61 and Sinha, 1993; Grimes, 1998; Richir and Gobert, 2013; Benali et al., 2016; Rouane-Hacene, 2015;2018), as they
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62 reflect the local environmental conditions through their ubiquity and are considered intermediate links between
63 trophic levels (Nieto et al., 2017). The published literature contains high amount of data on TM concentrations in
64 marine invertebrates collected in different areas and at different times of the year, and measured using various
65 analytical methods (Blackmore, 2001). However, few papers studied the bioaccumulation of TMs in
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66 polyplacophorans (Table 1), while none investigated it in Rhyssoplax olivacea (Spengler, 1797) (accepted name
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67 for Chiton olivaceus Spengler, 1797; see World Register of Marine Species) so far.
68 Chitons (Mollusca Polyplacophora), whose shell is an assembly of eight dorsal plates (valves) composed of
69 aragonite (Connors et al., 2012) and surrounded by the girdle (Van Der Wal et al., 1989), a feature not found in
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any other phylogenetic group among molluscs (Fischer, 1988), have the characteristics of a good bioindicator.
71 They live on hard substrates feeding on endo- and epi-lithic algae, scraped and excavated from the substrate with
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72 their radula (Van Der Wal et al., 1989), and have a variety of predators, including fish, lobsters, crabs, octopuses,
73 snails, starfish and birds (Connors, 2014). R. olivacea is ecologically important including as an endemic chiton to
74 the Mediterranean and Algerian coastal waters. Its trophic position allows it to describe the state of coastal
75 ecosystems in time and space, which gives this organism a key role in their protection and management.
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76 The main objective of the present work is to study the bioaccumulation of TMs in R. olivacea and to assess its use
77 as bioindicator species to monitor the contamination status of west Algeria. The specific objectives are: (i) to
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78 study the accumulation and compartmentalization of Fe, Cu, Co, Cr and Cd in the shell and the soft tissues of R.
79 olivacea purchased from 5 coastal locations in west Algeria ; (ii) to investigate the use of the condition index of
80 chitons to evaluate the environmental status of sampled sites and the impact of TM contamination on the
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81 physiology of individuals; (iii) to calculate indices that assess the contamination status of the west Algerian coastal
82 environment, i.e. the metal/shell weight index for the bioavailability of TMs, the trace element pollution index for
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the global contamination of sampled sites by TMs, and the trace element spatial variation index for the spatial
84 variability of TM environmental levels; (iv) to discuss the use of chitons as sentinel species in biomonitoring
85 programmes of coastal chemical contamination.

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87 2. Material and methods
88 2. 1. Sampling sites
89 The study area extends along the west coast of Algeria, including three major maritime cities in the provinces with
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90 the same names: Mostaganem, Oran and Ain Temouchent (Fig. 1). Five sampling sites were selected with respect
91 to the main identified contamination sources to follow a presumed contamination gradient. Westwards sites (S1
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92 and S2), namely Stidia and Sidi Mansour, are located in Mostaganem province, a coastal area where the wadis
93 Macta and Kramis are drained by the Cheliff, the largest river in Algeria (Mostari et al., 2020). Stidia is a site of
94 economic importance (agriculture, fishing, tourism, etc.) and is home to the Macta wetland classified as a Ramsar
95 site in 2001 (DGF, 2005). Stidia has a growing population and generates large amount of urban and industrial
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96 wastewater discharge with no prior treatment. The discharge of untreated wastewater contaminates coastal and
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97 groundwater, affects the environment and public health, and compromises any sustainable development (Taleb et
98 al., 2015). Sidi Mansour, located between Stidia and Marsat El Hadjadj, 18 km west of Mostaganem city, is a
99 seaside resort without urbanisation and frequented by tourists (Taibi et al., 2016). This relatively preserved site is
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the reference site of the study area. Sites St Michel (S3) and Cap Carbon (S4) are located in the province of Oran
101 whose coastline represents about 1/10 of the national littoral (Kacemi, 2011); more precisely in the Gulf of Arzew,
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102 one of the most important Algerian gulfs and home to the largest platform of the North African oil and gas industry
103 (Sahnoun et al., 2010). Many urban and industrial discharges occur along the coastal area of Oran, including
104 Cheliff wadi which carries wastewater of several cities (Bouchentouf et al., 2013), and El Mohgoun wadi which
105 drains the effluent of El Mohgoun Hospital (Grimes, 2010). St Michel is located near a hydrocarbon terminal, and
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106 is characterized by a consequent marine traffic and important fishing activities (Kerfouf et al., 2007; Dermeche et
107 al., 2009; Dermeche, 2010). Cap Carbon is an urban area not connected to the sewage network, as most of the
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108 constructions are listed illicit or contrary to the current regulations. It is characterised by the presence of septic
109 tanks and direct discharges into the coastal environment. The site Sidi Boucif (S5) is located in Ain Temouchent,
110 a province located at the crossroads of three large western cities (Oran, Tlemcen and Sidi Bel Abbes). Sidi Boucif,
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111 situated nearby the mouth of river Tafna, is home to several tourist resorts and hotels and large port infrastructures
112 (formerly for the iron ore trade), and to one of the most important cement factories in Algeria. The area is further
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known for its fishing and naval construction activities. Sidi Boucif is a seaside resort near Beni Saf harbor and is
114 considered polluted by the local authorities. The beach of Sidi Boucif is a black spot in terms of the discharge of
115 wastewater from the surrounding areas, hence the ban on bathing there for years but defied by vacationers.
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117 1. 2. Collection and preparation of samples
118 One hundred specimens of the Mediterranean Polyplacophora R. olivacea were collected from the inter-tidal zone
119 in each of the five sites during the cold (January to March) and the hot (June to September) seasons of year 2019.
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120 Collected chitons were washed with seawater on site and were immediately transported to the laboratory in an
121 isothermal box at a temperature of +5 °C. Chitons were left in seawater from their respective sampling sites for 24
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122 to 36 h. After depuration and prior dissection, the individual total wet weight was measured. Each individual was
123 dissected with stainless steel instruments, and soft tissues and shell were sampled and weighed, then dried in an
124 oven at 70 °C for 48 h and weighed for dry weight. All weighings were performed to an accuracy of 0.01 g.
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126 2. 3. Trace metal analysis
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127 The digestion of samples prior metal analysis was performed according to the method of Aminot and Chaussepied
128 (1983). Dry samples were digested at 95 °C for 1 hour using 1 ml of 65% concentrated HNO3 (Merck Suprapur
129 grade) for the soft tissues and 2 ml for the shell. Digestates were filtered through Whatman GF/F filters (0.45 μm
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pore size) after cooling and diluted to 50 ml with deionised water. TM concentrations (Fe, Cu, Co, Cr and Cd)
131 were measured using an Aurora Al 1200 atomic absorption spectrophotometer. TM concentrations are expressed
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132 in μg per g of dry tissue (μg g-1dw). Quality assurance and quality control were assessed by processing blank samples
133 and reference standard material (Biota, IAEA-MEL-2012-02 PT). TM concentrations obtained for standard
134 reference materials were always within the 95% confidence interval of certified values. Data are presented as mean
135 ± standard deviation of the mean (mean ± SD; n = 5). In order to compare bioaccumulation in R. olivacea with
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136 other polyplacophorans previously studied for TM bioaccumulation, and using the chiton soft tissues and/or the
137 shell as bioindicator tissues, an exhaustive review of the data available in the literature was carried out (Table 1).
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138 The data includes eight studies (including the present one) on TM concentrations in chitons from different
139 geographical regions.
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141 1. 4. Physiological index
142 The assessment of the environmental quality of monitoring sites requires the verification of the physiological status
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of the organisms included in the study (EPA, 2019); that verification was done using the Condition Index (CI). CI
144 was calculated as the ratio of the soft tissue drained wet weight to the total wet weight of chitons multiplied by
145 100 (n = 50 by site and season), according to the recommendation of the French Association for Standardization
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146 (AFNOR, 1985; Amiard et al., 1998):
147 CI = 100 × (soft tissue drained wet weight / total wet weight)
148 CI represents the first indicator of occupancy rate of valves by soft tissues. This reliable index (Bodoy et al. 1986)
149 is generally used to evaluate the seasonal variations in the nutrient reserves or quality of tissues, as well as to
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150 monitor the deleterious effects of various contaminants and/or diseases (Crosby et Gale, 1990).
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152 2. 5. Trace metal contamination indices
153 The Metal/Shell-Weight Index (MSWI) has been recommended to determine metal bioavailability in seawater
154 (Fischer, 1984; Soto et al., 2000; Rouane-Hacene et al., 2015; 2018; Guendouzi et al., 2020). In a recent study
155 conducted on the west coast of Algeria, Rouane-Hacene et al. (2018) calculated for the first time MSWI by
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156 normalising the concentrations of TMs according to the test weight of sea urchins (Paracentrotus lividus). The
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157 results obtained showed a good correlation between TM concentrations and MSWI. These authors validated the
158 normalised MSWI as a reliable tool for assessing the bioavailability of TMs. The MSWI for chitons was calculated
159 by normalising TM concentrations in soft tissues by the shell weight according to the following equation:
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MSWI =TMCST x [DWST / DWS]
161 where, TMCSB is the trace metal concentration in soft tissues (µg of TM/g of soft tissues), DWST is the dry
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162 weight of soft tissues (g), and DSW is the dry weight of the shell (g).
163 The level of TM contamination for each site in both seasons was calculated using the Trace Element Pollution
164 Index (TEPI) of Richir and Gobert (2014), a weighted version of the Metal Pollution Index (MPI) of Usero et al.
165 (1997). A high TEPI value is indicative of a potentially polluted site. The TEPI was calculated according to the
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166 following equation:
167 TEPI = (Cf1 x Cf2 . . .Cfn)1/n

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168 Where, Cfn is the mean normalised soft tissue concentration of TM n of the monitored site and season. Unlike
169 the MPI, the TEPI allows a reliable comparison of study sites and seasons regardless of the list of monitored
170 contaminants or the bioindicator species used (Richir and Gobert, 2014). The higher the TEPI value, the more
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171 contaminated the sample is. Based on TEPI values from the five sites over both seasons, the quartiles were
172 calculated to determine the class limits of a 3-level water quality scale (Richir et al., 2015). TEPI values were
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arranged in ascending order prior to quartile calculation. Quartile data were then averaged to determine the class
174 limits of the 3-level water quality scale. The class limits corresponded to the lower and upper quartile means: (i)
175 low contamination level (LCL, TEPI values below the 1st quartile mean), (ii) medium contamination level
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176 (MCL, TEPI values between the 1st and 3rd quartile means), and (iii) high contamination level (HCL, TEPI
177 values above the 3rd quartile mean) (Richir et al., 2015; Morrison et al., 2017; Ternengo et al., 2018; El Idrissi et
178 al., 2020).
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179 To order and to compare TMs according to the overall spatial variability of their environmental levels through the
180 whole of the study area, the Trace Element Spatial Variation Index (TESVI) of Richir and Gobert (2014) was
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181 calculated using soft tissues TM concentrations according to the following equation:
182 TESVI = [(xmax/xmin) / (∑(xmax/xi)/n)] x SD
183 where: xmax and xmin are the maximum and minimum mean concentrations recorded among the n sites, xi is mean
184 concentrations recorded in each of the n sites, and SD is the standard deviation of the weighted sum ∑(xmax/xi)/n.
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185 The higher the index value for a given TM, the more its environmental levels globally vary throughout the whole
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186 of west coast of Algerian (punctual contaminations and overall coastal spatial heterogeneity of TM levels
187 considered). The ranking of TMs in ascending order according to their TESVI values highlight the TMs of primary
188 environmental concern (Marengo et al., 2018).
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190 2. 6. Statistical analysis
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191 Results concerning the CI (n = 10) and TM concentrations (Fe, Cu, Co, Cr and Cd; n = 5) are expressed as mean
192 ± standard deviation (mean ± SD). Analyses of variance (ANOVA) were used to compare means of the measured
193 parameters (TM concentrations in the soft tissues and the shell and CI) among sites (5 levels) and seasons (2 levels)
194 after testing for normality and homoscedasticity. When ANOVA was significant (p < 0.05), a post-hoc comparison
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195 of means was made using Fisher's LSD test. Principal component analysis (PCA) was used to define possible
196 correlations between the eleven variables (TM concentrations in the soft tissues or the shell and CI). Missing
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197 concentrations below detection limits were substituted by 0 before statistical analysis (Helsel, 2004).
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199 3. Results
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200 3. 1. Trace metal analysis
201 TM concentrations in the soft tissues and the shell of R. olivacea and ANOVA results are presented in Tables 2
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and 3, respectively. The ANOVA results showed a very highly significant site effect (p < 0.001) for Fe, Cu and
203 Co in both the soft tissues and the shell, and for Cr and Cd in the soft tissues. A very highly significant seasonal
204 effect (p < 0.001) occurred for Fe, Co and Cd in both compartments and for Cu in the soft tissues. The site x season
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205 interaction was very highly significant (p < 0.001) for Fe, Cu and Co in the shell, and for Cu and Cd in the soft
206 tissues; it was significant (p < 0.05) for Cd in the shell. No site x season interaction effect was recorded for Cr in
207 the shell.
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208 Among all analysed TMs, in all the sites and for both seasons, Fe concentrations were higher in both the soft
209 tissues and the shell in comparison to the other monitored TMs. Fe concentrations in the soft tissues showed the
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210 same pattern in all sites, with higher values in the cold season ranging from 2471 ± 730 μg g-1dw in site S1 to 1415
211 ± 281 μg g-1dw in site S5. Levels varied from 1811 ± 678 μg g-1dw in site S1 to 923 ± 454 μg g-1dw in site S3 in the
212 hot season. Fe concentrations in the shell were higher in sites S1, S2 and S5 in the hot season than in the cold
213 season, and lower in sites S3 (< DL) and S4. Fe concentrations in the soft tissues and the shell thus followed
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214 opposite seasonal patterns in sites S1, S2 and S5. Cd concentrations were lower in both compartments in
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215 comparison to the other TMs. Cd concentrations were lower in the cold season, with site S4 showing the maximum
216 concentrations of 23.94 ± 5.25 μg g-1dw in the soft tissues and of 14.42 ± 4.50 μg g-1dw in the shell. In the hot season,
217 S5 showed the maximum concentrations in both the soft tissues (53.66 ± 14.42 μg g-1dw) and the shell (19.04 ±
218 8.48 μg g-1dw).

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219 Soft tissue Cu concentrations were higher in the cold season compared to the hot season, except for site S5 where
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220 soft tissue Cu concentrations were similar in between the two seasons (21.90 ± 10.51 μg g-1dw in the cold season
221 and 23.02 ± 8.30 μg g-1dw in the hot season, respectively). The highest Cu concentrations was measured in site S1
222 during the cold season in both compartments (78.70 ± 30. 83 μg g-1dw in the soft tissues and 23.22 ± 9.39 μg g-1dw
223 in the shell, respectively). Co concentrations in the soft tissues were higher in the cold season than in the hot season
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224 (< LD in sites S1 and S3), except for the most contaminated site S5 (116.10 ± 19.04 μg g-1dw in the cold season
225 and 80.37 ± 52.60 μg g-1dw in the hot season, respectively). In contrast, Co concentrations in the shell were higher
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226 in the hot season, except in site S4. Cr concentrations in the soft tissues varied among sites, and were higher in the
227 hot season in sites S3, S4 and S5. Shell Cr concentrations showed different seasonal pattern between sites, with
228 distinct inter-seasonal concentrations in sites S1 and S3 (e.g. 50.02 ± SD μg g-1dw in the cold season and 45.44 μg
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229 g-1dw in the hot season, respectively, for site S3), and similar inter-seasonal concentrations in sites S2, S4 and S5
230 (e.g. 38.28 ± SD μg g-1dw in the cold season and 63.14 ± SD μg g-1dw in the hot season, respectively, for site S5).
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231 All TMs considered, their concentrations in the soft tissues were higher than in the shell, particularly for the
232 essential TMs Fe, Cu and Co and this for both seasons. Fe, Cu and Co concentrations followed opposite seasonal
233 trends between compartments, with higher soft tissue concentrations in the cold season and higher shell
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234 concentrations in the hot season. TM concentrations varied between sampling sites.
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236 3. 2. Physiological index
237 The CI showed similar trends across all sites with higher values in the cold season compared to the hot season,
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238 except for site S1 (Fig 2). The ANOVA revealed a very highly significant site effect (p < 0.001). However, there
239 was no significant season effect, nor significant site x season interaction effect (p > 0.05; Table 3).
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241 3. 3. Trace metal bioavailability
242 TM bioavailability, i.e. MSWI values in R. olivacea from the five sites is given in Table 4. Fe was the most
243 bioavailable metal in the study area for both seasons, with site S1 showing the highest MswI values (434.8 ± 67.2
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244 in the cold season and 409.6 ± 128.1 in the hot season, respectively). Co was highly bioavailable in site S5 in both
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245 seasons. Cr and Cd bioavailability were higher in the hot season in all monitored sites, unlike Fe and Cu whose
246 bioavailability was higher in the cold season. Cu was also most bioavailable in site S1 in both seasons (13.78 ±
247 4.33 in the cold season and 3.86 ± 2.36 in the hot season, respectively).
248
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249 3. 4. Principal component analysis
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250 Results of the PCA showed that for the cold season (Fig. 3, A), the two first components PC1 and PC2 represented
251 56.53 % and 28.65 % of the total variance, respectively. For the hot season (Fig. 3, B), the two first components
252 PC1 and PC2 represented 56.46 % and 24.76 % of the total variance, respectively. During the cold season, positive
253 correlations were observed between soft tissues (acronym st) Cr (st), Cd (st), shell (acronym s) Cu (s) and Co (s)
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254 with r = 0.99, 0.88 and 0.91, respectively and between Cu (s), Cd (st), Cd (s) and Co (s) with r = 0.88, 0.86 and
255 0.85 respectively. Cu (st) was positively correlated with Fe (st) and CI with r = 0.91 and 0.75, respectively.
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256 Negative correlations were recorded between CI and Co (s), Cu (s) and Cd (s) with r = -0.76, -0.97 and -0.95,
257 respectively, with Cd (st) and Cr (st) with r = -0.76 and with Cd (s) and Cu (st) with r = -0.72. In the case of
258 essential TMs, a negative correlation was observed between Fe (st) and Fe (s) with r = -0.89 and between Cu (st)
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259 and Cu (s) with r = -0.77. During the hot season, positive correlations were observed between CI and essential
260 soft tissues TMs Fe (st) and Cu (st) with r = 0.72, Co (st), and Cd (st) and Cr (st) with r = 0.84 and 0.86, respectively,
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and Cu (s) and Cd (s) with r = 0.91.
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263 3. 5. Global contamination levels

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264 According to the 3-level water quality scale based on TEPI values calculated from soft tissues TM mean
265 normalised concentrations (Table 5), two samplings (site and season considered) showed MCL (Fig. 4): Stidia
266 (S1) both in the cold season (TEPI = 1.48) and in the hot season (TEPI = 0.28), and Cap Carbon (S4) both in the
267 cold season (TEPI = 0.85) and in the hot season (TEPI = 0.17). Saint Michel (S3) showed LCL in the cold season
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268 (TEPI = 0.12), but switched to a HCL in the hot season (TEPI = 2.15). Sidi Mansour (S2) was the reference site
269 with LCL and the lowest TEPI values both in the cold season (TEPI = 0.03) and in the hot season (TEPI = 0.04).
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270 Conversely, Sidi Boucif (S5) was the most contaminated site, with the highest TEPI value (TEPI = 7.99) in the
271 hot season.
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273 3. 6. Spatial variation of trace metal levels
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274 The TESVI calculated from TM mean concentrations in R. olivacea soft tissues ranged from 0.90 to 27.11 (Table
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275 6). Cd showed the highest spatial variation between sites and seasons (TESVI = 27.11) and Cr was the second TM
276 whose concentrations varied the most (TESVI = 11.14). Site S5 was the site with the highest mean concentration
277 for Cd (53.66 ± 14.42 μg g-1 dw) and Cr (137. 56 ± 60. 02 μg g-1 dw) during the hot season. Cu, Co and Fe showed
278
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low TESVI values (< 5). Fe presented the lowest spatial and seasonal variation of its concentrations in R.
279 olivacea soft tissues (0.90). For each TM, the xmin site of the TESVI matched the minimum value of the respective
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280 MSWI, and the xmax sites matched the maximum value of the respective MSWI. The TESVI values were ordered in
281 ascending sequence as follows: Fe<Co<Cu<Cr<Cd.
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283 4. Discussion
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284 This study aimed to assess the contamination status of the west coast of Algeria by TMs using R. olivacea as
285 bioindicator species and several indices, i.e. CI, MswI, TEPI and TESVI. It also aimed to study the
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286 compartmentalization of TMs in that species. R. olivacea showed its sensitivity to environmental TM
287 contamination, as revealed through the spatial and seasonal dynamics of bioaccumulated levels of TMs in its
288 tissues. Herbivorous chitons, primary consumers in the marine food chain (Van Der Wal et al., 1989),
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289 bioconcentrate TMs from their surrounding environment (Ali and Bahroon, 2000; Simon-Hettich et al., 2001;
290 Otchere, 2003; Shaw et al., 2009). Szefer et al. (1999), Blackmore (2001), Touahri and Abdel-Baset (2004), Fowler
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et al. (2007), Jacinto and Aguilar (2007), Swaleh et al. (2016), Ziyaadini et al. (2017), and Mercado-Molares et al.
292 (2022) reported that chitons were good bioindicators, reflecting the contamination status of the coastal marine
293 environment there were sampled from (Table 1). The present study revealed higher TM concentrations in the soft
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294 tissues than in the shell. Several factors contribute to contaminant accumulation after passage through biological
295 structures, such as the stability of the contaminant's links with organs, the structure and properties of the numerous
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296 cell barriers, the density and accessibility of potential binding sites and the turnover of tissue structures (Casas,
297 2005). The contaminant distribution in the different compartments reveals a "typology" for specific exposure
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298 conditions possibly attributed to organotropism (Ribeyre et al., 1980; Boudou et al., 1982; Casas, 2005).
299 Along the coast of west Algeria, among the five studied sites in both the cold and hot seasons, the highest TM
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300 concentrations were measured for Fe in R. olivacea soft tissues. High Fe levels in the soft tissues could be attributed
301 to the presence of magnetite (iron oxide), the main mineral formed in the cusps of chiton radula teeth (Van Der
302 Wal et al., 1989; Kim et al., 1989; Lowenstam and Weiner, 1989; Macey et al., 1994; Lee et al., 2003 a, b), which
303 are subject to a high abrasion degree, given the daily feeding process, and need to be replaced every two to three
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304 days (Shaw et al., 2002; 2008). Because free Fe induces oxidative stress, its continuous biomineralisation presents
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305 a physiological challenge for chitons (Dixon and Stockwell 2014), as they continuously sequester Fe and circulate
306 high concentrations in their haemolymph (Shaw et al., 2002; 2010). They use ferritin, a protein that allows its safe
307 transport, making them an emergent model for studies of both iron biomineralisation and homeostasis (Varney et
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al. 2021). Regarding Fe in the shell, concentrations were lower than in the soft tissues. Fe important distribution
309 disparities between compartments could reveal a relatively specific organotropism explained by physiological
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310 factors in the whole organism (Casas, 2005).
311 Cu concentrations < LD at St Michel (S3) in the soft tissues and the shell during the hot season and at Sidi Mansour
312 (S2) in the soft tissues during the cold season could be the result of several factors. In aquatic environments,
313 dissolved organic carbon affects Cu ecotoxicity (Ellingsen et al., 2015). Cu uptake by molluscs seems also to be
ot
314 influenced by available concentrations of Zn, Cd, and Pb salts (Phillips, 1976; Eisler, 2010); it appears that high
315 Zn intakes induce inhibition of Cu and Fe uptake (Ellingsen et al., 2015). Environmental physicochemical
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316 conditions (temperature, pH, electrolytes, etc.) and the bioavailability of the TM are other factors (Yung et al.,
317 2017). Fe, as Cu, are components of metalloenzymes and non-enzymatic metalloproteins in the mollusc shell
318 (Camprasse and Camprasse, 1999). Spatial variability and seasonal differences in Cu concentrations in the shell
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319 could result from numerous biotic and abiotic factors affecting its uptake and storage. Recognition of their
320 importance and interactions is essential for understanding Cu dynamics in marine systems (Eisler, 2010). Indeed,
321
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marine molluscs obtain the precursor ions to shell biomineralisation, Ca and bicarbonate from water and food
322 (Marin et al., 2008). They store Ca as amorphous granules in their connective tissues (Istin, 1970; Roinel et al.,
323 1973; Joubert et al., 2010); these granules contribute to the cellular detoxification processes by trapping toxic TMs
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324 (Simkiss, 1977). Furthermore, the negative correlation during the cold season between Cu in the soft tissues and
325 in the shell and between Fe in the soft tissues and in the shell may correspond, according to Avila-Poveda (2013)
11
326 from a study on Chiton articulatus, to the possibility of a short-term transfer of somatic reserves to the reproductive
327 organs in the soft tissues to meet the nutrient and energy needs for reproduction.
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328 Co concentrations were high in the soft tissues during the cold season and in the shell during the hot season. Co
329 plays a vital function in most animal species as a constituent of vitamin B12 (Smith, 1962; 1965; Underwood,
iew
330 1971) necessary for DNA synthesis and cell division (Leroy, 1994), and as a constituent of metalloproteins (Ptak,
331 1971). Co uptake depends on the diet (Amiard-Triquet and Amiard, 1976). Soluble Co uptake is preferred to
332 particulate Co uptake (Lowman and Ting, 1973; Pentreath, 1973; Eisler, 1981), but accumulation from water is
333 only minor because dissolved Co is readily adsorbed by particles whether organic (plankton micro-constituents,
v
334 organic debris, bacteria, molecular aggregates) or mineral. Many parameters influence Co adsorption, like redox
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335 potential, salinity, temperature, pH, the nature and amount of suspended matter (Elteren et al., 1996; Gaudaire,
336 1999), the seasons (Bryan, 1973; Patel et al., 1973, Marimoutou et al., 2022), and the number and types of protein-
337 binding materials (Shimizu et al., 1971). However, Marimoutou et al. (2022) stated that mollusc shells were good
338
er
accumulators of Co via water after experiments on the gastropod Radix balthica.
339 Although Fe, Cu and Co are essential for biological processes, they can be contaminants when their concentration
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340 exceeds a threshold, itself a function of the element's speciation (Casas, 2005, Seignette and Lafontan, 2010),
341 which directly controls its bioavaibility (Gaudaire, 1999); the environmental and ecotoxicological interest for
342 essential TMs lies in the tight limit between their essentiality and toxicity (Mishra et al., 2023). Regarding the
343 concentrations of Fe, Cu and Co in each compartment, weight loss periods due to physiological conditions in
ot
344 molluscs (e.g. reproduction, growth, etc.) have the effect of concentrating the contaminants in the flesh (Casas,
345 2005). The present study showed significant differences in TM concentrations between seasons with higher levels
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346 in the hot season for Cr and Cd in the soft tissues and for Fe, Co and Cd in the shell. Seasonal differences in TM
347 concentrations in chiton compartments could also reflect the increased anthropogenic activities, including fishing
348 and shipping, and the use of the sampling sites by vacationers in the hot season. Direct discharges into the west
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349 coast of Algeria increase considerably during the summer with the growth in the population (Belhoucine et al.,
350 2014; Tabeche et al., 2021). Cr is readily transferred to invertebrates through food (Moore and Ramamoorthy,
351
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1984), which is probably a more important source in most species than water. Its uptake often depends on
352 temperature and is thus seasonal in natural populations (Karbe et al., 1977). Cr contamination of coastal
353 ecosystems, mainly due to the dumping of untreated or poorly treated industrial waste, is highly toxic, presenting
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354 various levels of risk for coastal ecosystems (Chiarelli and Roccheri, 2014). In molluscs and other marine
355 organisms, Cr bioaccumulation is high in the vicinity of tanneries, electroplating plants, oil drilling operations,
12
356 sewage dumps, ocean dumping sites and other sources of Cr-containing wastes (Eisler, 2000; Maanan, 2007;
357 Kumar et al., 2023).
ed
358 Cd has no known biological function in living organisms (Sankar et al., 2006; Julshamn et al., 2008). Its
359 accumulation could be attributed to its bioavailability in ambient seawater (Peden et al., 1973; Stenner and
iew
360 Nickless, 1974), to vertical concentration gradients (Nielsen, 1974; Podgurskaya and Kavun, 2006), to diet
361 (Thorsson et al., 2008), to seasonal changes and to Ca concentrations in the shell (Belcheva et al., 2006). The Cd
362 availability in mollusc shell depends on its binding to biogenic CaCO3 (readily available) or precipitated CaCO3
363 (poorly available) (Cooke et al., 1979). TM uptake rates increase with external dissolved concentrations (Rainbow.
v
364 1985; Rainbow and White., 1990; Wang and Fisher 1996), which are considered a passive process (Phillips and
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365 Rainbow, 1993). However, Ca-pumps could be an active pathway for Cd uptake (Simkiss, 1998). Indeed, non-
366 essential TMs such as Cr and Cd can take over the specific transport of essential TMs such as Ca, Fe or Zn by
367 ionic or molecular mimicry (Luckey and Venugopal, 1977; Bridges and Zalups, 2010; Martinez Finley et al.,
368
er
2012). Cd was measured in high levels in mollusc tissues in the vicinity of highly urbanised areas, especially where
369 electroplating and mining take place (Graham, 1972; Fowler and Oregioni, 1976; Eisler, 1981, 2000; Maanan,
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370 2007), industries that use it as a catalyst for organic synthesis (Benadda, 2002), smelters and discharges from
371 abandoned mines (Garceau et al, 2010), in addition to phosphate rock fertilizers, municipal waste and sewage
372 sludge (Järup and Åkesson, 2009; Pan et al., 2010). The bioavailability of Cd, as for Zn and Pb, seems to influence
373 the absorption of Cu in molluscs (Phillips, 1976), which could explain the positive correlation during the cold
ot
374 season between Cu (s) and Cd (s), matching the negative correlation between Cu (st) with Cu (s) and Cd (s) and
375 the strong correlation during the hot season between Cu (s) and Cd (s) when concentrations were the highest.
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376 Chiton shell appeared to be a good tool for monitoring Cd contamination, in line with the findings of Swaleh et al.
377 (2016).
378 The first, to our best knowledge, comparative review in the present study of existing data on TE bioaccumulation
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379 in other polyplacophorans indicated that TE concentrations varied considerably between species and regions. Fe
380 concentrations in the soft tissues of R. olivacea were close to those of Acanthopleura gemmata collected near a
381
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municipal sewage outfall which discharged into coastal waters (Swaleh et al., 2016), but lower than those
382 of Acanthopleura haddoni from the Gulf of Aden, Yemen (Szefer et al., 1999). Cu concentrations in the soft tissues
383 of R. olivacea were similar to levels observed in other chiton species. R. olivacea showed much higher levels of
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384 Co and Cr (more than 20 times) than A. haddoni (Szefer et al., 1999). Cd concentrations in R. olivacea were similar
385 to those of Acanthopleura japonica (Blackmore, 2001), Acanthopleura vaillantii (Fowler et al., 1983) and A.
13
386 gemmata (Swaleh et al., 2016), but much higher than Cd concentrations in A. haddoni (Szefer et al., 1999)
387 and Chiton lamyi (Ziyaadini et al., 2017). Szefer et al. (1999) by comparing data obtained for chiton A. haddoni
ed
388 from the Gulf of Aden, with those reported for chiton Liolophura japonica from intertidal rocky shore of the east
389 of Kyushu Island, Japan (Fujita, 1994; Ikuta, 1999) reported that A. haddoni contained five and three times more
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390 Cd and Pb, respectively. Blackmore (2001), Fowler et al. (2007) and Jacinto and Aguilar (2007) reported by
391 comparing the accumulative potential of several benthic species, including polyplacophorans, that chitons
392 accumulated the highest concentrations of toxic TEs, such as Cd, compared to other invertebrates. Blackmore
393 (2001) attributed the interspecific variation in body concentrations to the accumulation strategy of the organisms
v
394 analysed and the physiological requirements for essential TMs and suggested that the high concentrations of toxic
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395 TEs may reflect the less advanced physiology of polyplacophorans. The shell Fe concentrations reported by
396 Swaleh et al. (2016) in A. gemmata were twice as high as those obtained in R. olivacea in the present study, while
397 Cu concentrations were higher in R. olivacea than in A. gemmata. According to Blackmore (2001) "other
398
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variations that will affect absolute accumulated levels of TMs include interspecific differences in feeding efficiency
399 and gut passage times and differences in absorption from solution, respiration, life cycle, longevity and growth
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400 rate". All cited authors agree that polyplacophorans are good bioaccumulators of TEs. Blackmore (2001), Fowler
401 et al. (2007), Jacinto and Aguilar (2007), and Swaleh et al. (2016) are unanimous that chitons are a good
402 bioindicator for Cd.
403 Integrated physiological measures of stress can be estimated by determining the CI (Oehlmann and Schulte-
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404 Oehlmann, 2003). The CI provides predictive information on habitat quality and reproductive performance
405 (Stevenson and Woods, 2006) and allows determining pollution signal, as a physiological state indicator of
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406 animals, through its correlation with contaminant concentrations (Margus, 1985; Hariati, 1986; Okumus and
407 Stirling, 1998; Orban et al., 2002; Cossa and Sanjuan, 2002). CI values were higher at sites at Stidia (site S1), Sidi
408 Mansour (site S2) and Sidi Boucif (site S5) compared to St Michel Harbour and Cap Carbon (sites S3 and S4,
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409 respectively). The physiological state of chitons at Stidia (site S1) and Sidi Boucif (site S5) could be related to the
410 presence of organic matter, since the increase in CI is often associated with inputs of organic matter from
411
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anthropized areas and notably domestic wastewater discharges (Schiedek et al., 2006). Not only the quality of the
412 water body, but also the characteristics of the habitat can drive CI values. Indeed, according to our field
413 observations, the five sites have distinct substrates, hydrodynamic regimes and estuarine influence. Thus, at Stidia
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414 (site S1), the chitons lived on rocks rich in macrophytes and different algal communities, which they fed on, and
415 were in a very favourable environment. At Sidi Mansour (site S2), the substratum is soft, and the chitons live
14
416 attached to the few rocks covered with a thin layer of algae but sheltered from anthropic activities, notably during
417 the cold season. At St Michel Harbour (site S3), where chitons were attached to rocks covered with a few species
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418 of algae, and at Cap Carbon (S4), where they lived in crevices in the bedrock where the plant cover was sparse
419 and composed of seasonal algae, the populations were in an unfavourable environment where food resources were
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420 more limited and less readily available. The wide variation in food availability and quality in different habitats can
421 significantly affect the morphology and physiology of molluscs (Kovačić et al., 2023). This result underlined the
422 high adaptability of R. olivacea to environmental conditions, both trophically and physiologically.
423 The high soft tissues Fe and Cu concentrations measured during the cold season could correspond to the
v
424 reproductive period. These two metals as essential micronutrient involved in many essential physiological
re
425 processes including reproduction (Ponka et al., 2015); their bioaccumulation is, therefore, maximal before
426 spawning and minimal after spawning, with nutritional reserves depleted during gametogenesis (Radenac et al.,
427 1997). The positive correlation between soft tissues Cu concentrations and CI values, which also indicated high
428
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values during the cold season, could support this hypothesis for R. olivacea. A positive correlation between Cu
429 levels in the soft tissues and increased body weight was reported for other mollusc species (Boyden, 1974), the
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430 reproductive period being associated with higher feeding activity (Rouane Hacene et al., 2018); reproductive and
431 nutritional status, glycogen utilisation and metal-poor gamete loss are parameters that affect weight variation
432 (Cartier et al., 2004). Indeed, Avila-Poveda (2013) estimated from a study on Chiton articulatus that weight
433 development during reproductive seasons was directly fueled by energy and nutrients from food intake. In addition,
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434 the evident correlation between weight loss and increased Cd and Cr concentrations during the hot season indicated
435 a disturbance of the bioaccumulation process caused by the life cycle of the bioindicator organism. Generally, an
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436 inverse correlation exists between contaminant concentrations and soft body weight through a
437 dilution/concentration effect (Casas, 2005). Indeed, weight changes related to the reproductive cycle of the
438 bioindicator organism dominate seasonality and contribute to most of the temporal variability in bioaccumulation
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439 (Bryan 1973; Boyden, 1974; Cossa, 1980; Amiard et al., 1986; Phillips and Rainbow, 1994; Langston and Spence
440 1995; Wang and Fisher, 1997; Mourgaud et al., 2002; Rouane Hacene et al., 2015), with diet, turbidity, salinity
441
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and water depth being other driving environmental factors (Young, 1975 ; Watling and Watling, 1976).
442 Malav et al. (2023) considered the determination of toxic TM concentrations to be insufficient for an integrated
443 ecosystem assessment, and using pollution indices is the key to effectively assess metal contamination. Among
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444 driving factors involved in TM bioaccumulation are the trophic conditions (quality, quantity), the bioavailability
445 and speciation of TMs present in the environment, and the biological factors including the contamination pathways
15
446 and the biologic cycles of organisms (Casas, 2005). In addition, Rainbow (2018) stated that: "The factors affecting
447 assimilation efficiency, and hence the bioavailability of TMs from the diet, include the TM concentration in the
ed
448 diet, its chemical form in the food, the digestive processes releasing TMs from the ingested meal, the chemical
449 form of TM released by digestion and it’s taken up by a gut epithelial cell". On the west coast of Algeria, Rouane
iew
450 Hacene et al. (2018) confirmed the relevance of normalizing TM concentrations to the test weight of sea urchins
451 when calculating the metal weight/shell index MSWI, an approach similar to the normalisation of TM concentration
452 to the shell weight of bivalves (Fischer, 1984; Soto et al., 2000; Rouane-Hacene et al., 2015; Guendouzi et al.,
453 2020). This approach was considered adequate and useful to assess the bioavailability of TMs to invertebrate’s
v
454 species (e.g. sea urchins and mussels) in the coastal marine environment. The TM bioavailability expressed as
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455 MWSI values in R. olivacea from the five sites showed that Cd, Cr and Co were more bioavailable in Sidi Boucif
456 (site S5), while Fe and Cu were most bioavailable in Stidia (site S1). Average bioavailability values for chitons
457 indicated that Sidi Mansour (site S2) was the least problematic site with respect to TM bioaccumulation, which is
458 in agreement with TEPI values.

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459 The TEPI revealed spatial and seasonal differences in global contamination among sites. Stidia (site S2), with
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460 LCL, was confirmed to be the reference site of the area under study compared to the other four sites. In both
461 seasons, the urban sites Stidia (site S1) and Cap Carbon (site S4) showed MCL, while Sidi Boucif (Site S5)
462 appeared as a contamination hotspot with HCL. The site is considered as polluted by the authorities, and suffers
463 sewage discharges from the surrounding areas in addition to fishing and naval construction industries. The port St
ot
464 Michel (site S3) bordering the Arzew hydrocarbon port switched from an MCL in the cold season to an HCL in
465 the hot season, probably due to the increase of maritime traffic, fishing and other anthropogenic activities during
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466 this season. Bouiba et al. (2023) also reported higher global contamination levels on the west coast of Algeria
467 using P. lividus as bioindicator species in the hot season. The TESVI values sorted TMs in ascending order as
468 Fe<Co<Cu<Cr<Cd, highlighting the distribution of Cd and Cr listed as potentially problematic over the study area
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469 (Richir et al., 2021). In Bouiba et al. (2023), Fe had the highest TESVI value for P. lividus from the west coast of
470 Algeria, followed by Cd and then Cu. In line with TEPI, Sidi Boucif (site S5) was the site with the maximum
471
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concentration (xmax) of Co in the cold season and Cd and Cr in the hot season. Consequently, it was the most
472 impacted site by TM contamination. During the cold season, the maximum Cu and Fe concentrations at Stidia (site
473 S1) could be attributed to the richness of algae at the site or to local contamination (Fowler and Oregioni, 1976).
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474 TM mobility, especially in environments with frequent condition changes is known to cause a toxicological impact
475 on aquatic organisms and ecosystems (Nabelkova and Kominkova, 2012), as in Sidi Boucif (site S5), Stidia (site
16
476 S1) and Cap Carbon (site S4) where sewage networks were absent and urban drainage could considerably modify
477 physicochemical conditions of water, involving the remobilisation of TMs from sediments to water and,
ed
478 consequently, increasing their bioavailability. Accumulation in sediments which serve as storage sites affect
479 benthic invertebrates either directly or through food chain transfer (Chiffoleau, 1994; Badr et al., 2009; Nabelkova
iew
480 and Kominkova, 2012; Meng Chuan and Yunus, 2019; Zhang et al., 2022; Kumar et al., 2023).
481 To assess the TM contamination dynamic on the west coast of Algeria, comparison between results of the present
482 study and previous research in the area was established. The results of the present study were in agreement with
483 those of Remili and Kerfouf (2013) who reported mean Cd concentrations in water samples exceeding the
v
484 normative limit (Tabeche et al., 2021) in Solea solea, and with results of Bouiba et al. (2023) who reported higher
re
485 Cd levels in P. lividus from Algeria than in other Mediterranean and Atlantic countries. According to Belhoucine
486 et al. (2014) and Guendouzi et al. (2020), Cd concentrations in Trachinus araneus and Mytilus galloprovincialis
487 did not exceed the permissible limits. While the essential TMs Fe and Cu displayed the highest concentrations
488
er
during the cold season in R. olivacea, an opposite pattern was observed for Cu in P. lividus (Rouane Hacene et al.,
489 2018) and in S. solea (Tabeche et al., 2021), and for Fe and Cu in P. lividus in the recent study of Bouiba et al.
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490 (2023). The concentrations of Cd, Fe and Cu recorded in R. olivacea were higher than in all the organisms sus-
491 mentioned. Under similar physicochemical conditions, interspecific biological differences in TM accumulation
492 are related to the number of membrane uptake sites; this reflects species differences in their functional ecology,
493 particularly physiological, anatomical, and life history characteristics (Rainbow, 2018). Co and Cr concentrations
ot
494 could not be compared with previous studies in the surveyed area, as there are few publications on their
495 bioaccumulation in marine organisms (Reeves et al., 2022).

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496
497 5. Conclusion
498 The TM concentrations measured in the soft tissues and the shell of the chiton R. olivacea, and the comparison
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499 with available scientific literature on the use of chiton spp. as bioindicators, highlight the potential use of this
500 species to monitor coastal TM contamination in Algeria and in its area of distribution, the Mediterranean. Using
ep
501 the two compartments provided complementary information on TM dynamics. The shell is proposed as a suitable
502 indicator of Cd exposure. The roles and effects of TMs in chitons, including R. olivacea needs to be investigated
503 further to understand their dynamics within the organisms and the potential consequences on their fitness. R.
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504 olivacea reflects the contamination status of the marine environment it is sampled from; it is an efficient
505 bioindicator, given its high potential to accumulate TMs, which confirms its use as an environmental early warning
17
506 system of coastal contamination. Furthermore, the present study shows that the condition index of R. olivacea
507 under field conditions is related to the concentrations of TM accumulated in the soft tissues and their environmental
ed
508 bioavailability. As a first study on the bioaccumulation of TMs in R. olivacea, and from the bibliographic synthesis
509 work carried out, it can be considered as a reference for future work using chiton spp. as an accumulation model.
iew
510 Using a range of contamination indices such as MSWI, TEPI and TESVI provided a panoramic view of TM
511 contamination. The MSWI is an efficient tool to assess the bioavailability of TMs to chitons, which confirms the
512 observations of Rouane-Hacene et al. for M. galloprovincialis (2015) and P. lividus (2018). The TEPI is a reliable
513 tool to compare global TM contamination at local scale, i.e. in space and over the seasons in west Algeria. TEPI
v
514 is internationally implemented, regardless of the number of TMs or the biological model used (Richir and Gobert,
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515 2014; Wilkes et al., 2017; Ternengo et al., 2018). TM bioaccumulation and CI, MSWI and TEPI values are
516 complemented by the TESVI that highlighted the dispersion of Cd and Cr and their involvement in the
517 contamination of the study area, which should be closely monitored at least for these two metals. Sidi Mansour
518
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(site S2) was confirmed as a reference site for the area under study, while Sidi Boucif (site S5) appeared to be the
519 most contaminated by TMs. The concordance and complementarity of the results validates the ecotoxicological
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520 approach based on concentration measurements and physiological and contamination index determination in
521 biomonitoring programmes. Such programmes should be implemented along the Algerian coast, and functional
522 wastewater treatment plants should be installed. The application of restrictive measures for polluting discharges
523 into the environment must be concretely implemented by the concerned authorities.
ot
524
525 Acknowledgements
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526 This article is dedicated to Professor Zitouni Boutiba, who left us in November 2016. The authors would like to
527 thank Mrs Meguebar Ouided and the technical staff of the physicochemical analysis laboratory of (ALZINC,
528
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Ghazaouet) and Pr Omar Kharoubi, Director of the Laboratory of Experimental Biotoxicology, Biodepollution
529 and Phytoremediation from the University of Oran 1 Ahmed Ben Bella (Algeria), for providing helpful advice
530 during periods of experimental study and data processing.

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531
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1 A first study on the use of Rhyssoplax olivacea (Mediterranean Polyplacophora) to biomonitor trace metal

10 protection de l’environnement et application en santé publique (VAHPEASP), Department of Biology, BP

85 programmes of coastal chemical contamination.

87 2. Material and methods

117 1. 2. Collection and preparation of samples

139 geographical regions.

141 1. 4. Physiological index

146 (AFNOR, 1985; Amiard et al., 1998):

166 following equation:

167 TEPI = (Cf1 x Cf2 . . .Cfn)1/n

178 al., 2020).

182 TESVI = [(xmax/xmin) / (∑(xmax/xi)/n)] x SD

188 environmental concern (Marengo et al., 2018).

200 3. 1. Trace metal analysis

207 the shell.

218 8.48 μg g-1dw).

241 3. 3. Trace metal bioavailability

and Cu (s) and Cd (s) with r = 0.91.

263 3. 5. Global contamination levels

271 hot season.

273 3. 6. Spatial variation of trace metal levels

281 ascending sequence as follows: Fe<Co<Cu<Cr<Cd.

357 Kumar et al., 2023).

402 bioindicator for Cd.

458 in agreement with TEPI values.

495 bioaccumulation in marine organisms (Reeves et al., 2022).

530 during periods of experimental study and data processing.

560 Centre. Océano. Pêche. PELAGOS, VII (1), pp. 41–48.

563 Marine Environmental Research, 61(4), pp. 396–409. Available at:

654 Elsevier. Available at: https://doi.org/10.1016/C2009-1-28483-8.

335–346. Available at: https://doi.org/10.1098/rspb.1989.0052.

815 Evolution, 7(14), pp. 5502–5513. Available at: https://doi.org/10.1002/ece3.3101.

Marine Biology, 53(4), pp. 353–360. Available at: https://doi.org/10.1007/BF00391618.

904 149(February), p. 106362. Available at: https://doi.org/10.1016/j.envint.2020.106362.

914 Sahnoun, F, Bendraoua, A and Hadjel, M. (2010) ‘CONTROLE DE LA POLLUTION MARINE DU

925 Seignette, O. and Lafontan, M. (2010) Cobalt 60 et environnement. INRS.

945 Organization. https://apps.who.int/iris/handle/10665/42337.

950 Smith, E.L. (1965) ‘Vitamin B12, London, Methuen, 1965.’

1034 Assessment’, Processes, 10(5), p. 837. Available at: https://doi.org/10.3390/pr10050837.

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