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Journal ArticleDOI

A multitracer approach to assess the spatial contamination pattern of hake (Merluccius merluccius) in the French Mediterranean.

TL;DR: The use of combined ecotracers was revealed as a powerful tool to discriminate between fish populations at large and small spatial scale, and to enable understanding of the environmental and biological influences on contamination patterns.
About: This article is published in Science of The Total Environment.The article was published on 2015-11-01 and is currently open access. It has received 25 citations till now. The article focuses on the topics: Merluccius merluccius & Hake.

Summary (5 min read)

1. Introduction

  • Chemical contaminants emerged recently as useful ecotracers of trophic patterns or environmental parameters when used in combination with other tools, mostly stable isotope analyses (Fisk et al., 2002; Chouvelon et al., 2014; Cresson et al., 2014; Brown et al., 2015; Lavoie et al., 2015).
  • At a fine scale, within-species variation of the shape can reveal the influence of environmental parameters such as temperature and/or food availability (Lombarte and Lleonart, 1993; Gagliano and McCormick, 2004; Mérigot et al., 2007; Morat et al., 2012b).
  • More than 90 % of the French Mediterranean fisheries are located in the Gulf of Lions, with European hake (Merluccius merluccius Linnaeus, 1758) being the most important species (Aldebert et al., 1993; Bănaru et al., 2013).

2.1. Sampling sites

  • European hake (Merluccius merluccius) individuals were collected by professional trawlers at three sites of the French Mediterranean (Fig. 1), two in the western part of the Gulf of Lions (Port la Nouvelle and Le Grau du Roi) and one in northeastern Corsica .
  • These sites were chosen on the basis of the hypothesis that they reflect different contamination levels.
  • The Bastia site in Corsica is located beyond the influence of the Gulf of Lions, with low urban and industrial development, and might consequently be expected to be a semi-pristine area (Porte et al., 2002; Galgani et al., 2006; Serrano et al., 2013).
  • Actual sampling size was lower due to technical constraint in the field and is detailed in Table S1.
  • After sampling, fish were stored frozen until dissection.

2.2. Sample preparation and dissection

  • In the lab, individuals were thawed, measured (total length, to the nearest mm) and weighed (eviscerated mass, to the nearest 0.1 g).
  • Males and females were separated on the basis of macroscopic observation of the gonads.
  • Fish body condition was determined using relative condition factor Kr (Le Cren, 1951), with Kr = Me/Me’.
  • Three muscle samples without skin were collected for analyses, dorsal white muscle for stable isotope analyses, muscle from the caudal peduncle for Hg determination, and the whole remaining muscle for PCBs determination, as a large amount of matter is needed for this analysis.
  • Sagittal otoliths were extracted from the cranial cavity to perform otolith shape analysis.

2.3. Isotopic and contaminant analyses

  • C and N stable isotope ratios were determined with a continuous flow mass spectrometer (Delta V Advantage, Thermo Scientific, Bremen, Germany) coupled with an elemental analyzer (Flash EA 1112 Thermo Scientific, Milan, Italy).
  • One determination of δ13C and δ15N was performed for each individual.
  • This technique allows the determination of the total Hg but not the methylmercury (MeHg).
  • Measurement accuracy was checked by the analysis of certified samples, with standard deviations of ~20 % for all congeners.

2.4. Otolith shape analysis

  • Prior to shape analysis, otoliths were oriented in the same direction and digitalized with a digital camera coupled with a stereomicroscope.
  • Briefly, this technique allows the transformation of the complex shape of the otolith into a set of numerical descriptors, called harmonics.
  • Each harmonic is characterized by 4 coefficients, resulting from the projection of each point of the outline on axes (x) and (y).
  • The lowest needed number of harmonics was determined by calculating the Fourier Power (FP) spectrum.
  • The cumulated power percentage FPc is calculated as the sum of the powers of the n harmonics.

2.5. Numerical analyses

  • The variability of biometry, isotopic ratios and contamination levels were analyzed independently across sex and origin using a univariate PERMANOVA (Anderson, 2001).
  • Total length, Hg and CB153 concentrations were log (X+1) transformed prior to analyses.
  • Analyses were performed using the PRIMER 6 software and the PERMANOVA add-on (Clarke and Warwick, 2001).
  • Distances between groups on the CDA representation were assessed calculating Euclidean distances between the barycenter of each group.
  • A priori groups were based on sex (juvenile, male or female) and on origin.

3.1. Sample size, sex ratio and morphological indices

  • The sex ratio was largely imbalanced, with predominance of juvenile individuals in the smallest size-classes, and of females for larger individuals, consistently with the biology of the species.
  • Mean length of males and females from Port la Nouvelle and Bastia did not significantly differ (~ 300 mm TL for both sexes), whereas females from Le Grau du Roi were significantly larger than males (335 mm for females vs. 259 mm for males).
  • Since males’ growth rate is slower, males were older than females in Port la Nouvelle and Bastia, whereas males and females were of similar age in Le Grau du Roi (PERMANOVA F = 4.75, p = 0.0001).
  • Fish condition factor varied also with site (lowest condition indices at Bastia, highest at Le Grau du Roi) and sex (highest condition factor for juveniles, no differences between adults of both sexes; Table 1).

3.2. Carbon and nitrogen stable isotope ratios

  • When considering sites separately, the difference between minimum and maximum δ15N values was close to 2 ‰.
  • Origin and sex had an effect on stable isotope ratios (Fig. 2).
  • In addition, isotopic ratios measured for adults sampled at Bastia were not markedly different from those of juveniles but significantly lower than those of adults collected in the Gulf of Lions.

3.3. Mercury concentrations

  • A higher value (14.04 µg g-1 dm) was measured for a large female (> 850 mm TL) collected at Le Grau du Roi, but this individual was not included in the study due to its lack of representativeness.
  • The most striking feature observed for Hg was the wide spatial difference (PERMANOVA F = 319.40, p < 0.0001), driven mostly by the high concentrations measured in Corsica.
  • Mean Differences between Corsica and Gulf of Lions were observed whatever the fish size but were more pronounced for larger individuals (Fig. 3).
  • As a consequence, significant correlations were observed between length or trophic level and Hg concentrations, with the exponential model being the best fit in all cases except for the correlation between length and Hg at Port la Nouvelle (Fig. 3, Table S3).

3.4. PCB concentrations

  • The predominant part of the PCB contamination was represented by highly chlorinated compounds, whatever the sex and the origin of the fish.
  • In contrast, tri- and tetra-chlorinated congener were quite absent, with all CB 28 concentrations below detection limits, and CB 53 representing always less than 2 % of the total PCB burden.
  • Regarding the sex, concentrations followed an increasing order: juveniles < females < males when all sites were combined.
  • When sex and sites are considered, this pattern was conserved at Port la Nouvelle and Bastia, but females exhibited higher CB 153 concentrations than males at le Grau du Roi.

3.5. Otolith shape

  • The first plan of the CDA on Fourier coefficients explained 57 % of the variability, with ~75 % of good reclassification (Cohen’s kappa test).
  • Results highlighted discrepancies between individuals from Corsica and the Gulf of Lions on the one hand, and between juveniles and adults on the other hand (Fig. S2).
  • Wide differences (average value of Euclidean distances between barycenter of groups: 1.90 ± 0.46) were observed between individuals from Corsica and from the Gulf of Lions.
  • The lowest Euclidean distance measured in the dataset was calculated between the barycenter of the groups formed by adults from both sites in the Gulf of Lions (d = 0.73).
  • Finally, it is of interest to note that juveniles from Le Grau du Roi are very distant from other sites (Euclidean distances ranging between 2.09 and 2.59).

3.6. Canonical discriminant analysis on combined parameters

  • The general CDA based on all variables explained nearly 70 % of the variability, and discriminated well the individuals, on the basis of their sex and their origin, since 67 % were well-classified within the predefined group (Fig. 4).
  • The most efficient 10 reclassification was observed for juveniles of both sites in the Gulf of Lions and for females from Port la Nouvelle (percentage of good reclassification > 70 %), whereas males from the Gulf of Lions were poorly reclassified.
  • The first axis was based on the opposition between Hg and δ15N values and discriminated individuals from Bastia vs. individuals from the Port la Nouvelle and Le Grau du Roi.
  • The second axis was mostly based on the otolith shape parameters, and separated juveniles from adults at all sites, with a marked pattern in the Gulf of Lions.

4. Discussion

  • Stable isotope ratios, contamination levels and otolith shape allowed a clear discrimination between hake in the Gulf of Lions and in Corsica.
  • Since contamination is mainly driven by the diet (Hall et al., 1997; Cresson et al., 2014) and as Hg and PCB are biomagnified through the trophic network, determining accurately the diet and trophic position of fish is crucial to understanding contamination patters.
  • Additionally, contamination patterns are also driven by local contamination sources, the biology of the species, and environmental specificities (Bodiguel et al., 2009a; Cossa et al., 2012; Brown et al., 2015; Cresson et al., 2015).
  • Assessing a site-specific contamination pattern thus requires a good understanding of all these parameters.

4.1. The Rhône River, main driver of the pattern in the Gulf of Lions

  • The Rhône River is the major organic matter (OM) and contaminant source for the Gulf of Lions.
  • Considering isotopic ratios, juveniles exhibited lower values than adults.
  • Such an influence of riverine inputs on hake juveniles was previously observed at the mouth of the Rhône River, as juveniles collected closer to the river mouth exhibit lower δ13C values than individuals collected further offshore (Ferraton et al., 2007).
  • At Port la Nouvelle, three coastal lagoons and several flash-flooding rivers could also represent important sources of land-derived OM (Kim et al., 2007).
  • Values measured in 2013 were three to five times lower than values measured a decade ago (Table 3), consistently with the expected reduction of burdens in biota ~25 years after the ban on PCB use (e.g. Aguilar and Borrell, 2005).

4.2. The “Corsican mercury anomaly”, an effect of oligotrophy?

  • Earlier studies on mercury concentrations in the Mediterranean documented a “Mediterranean mercury anomaly”, i.e. higher Hg concentrations in Mediterranean individuals when compared with other oceans, even if concentrations in water or sediment were not significantly different (Aston and Fowler, 1985; Cossa and Coquery, 2005).
  • Due to its low density of population and absence of large factories, Corsica is commonly considered as a semi-pristine area with low Hg or PCB concentrations (Porte et al., 2002; Galgani et al., 2006; Pergent et al., 2011; Serrano et al., 2013).
  • But, similarly to the trend observed at a larger spatial scale throughout the Mediterranean (Aston and Fowler, 1985; Cossa and Coquery, 2005), oligotrophy may be the cause of the discrepancies observed for Corsican hake as it drives the biogeochemical cycle of Hg and the life history parameters of individuals.
  • Similarly, the predominance of small phytoplanktonic cells would explain the low isotopic ratios, as a significant correlation is observed between phytoplankton size and isotopic ratios.
  • From a biological point of view, lower production leads to lower growth rate of organisms, thus lower bio-dilution of Hg contamination in newly synthesized tissues.

4.3. Combining multiple biomarkers to interpret contamination patterns and separate local populations

  • In the recent years, contaminant analyses switched from a public health focused approach (i.e. assessing the risk of human contamination while consuming marine products) to an ecological approach (i.e. using contaminants as proxies of ecological processes).
  • These studies also confirmed that a combined approach is needed, and that isotopic or contaminant biomarkers alone are not sufficient.
  • With regard to Corsica, shape was not a major discriminating factor between adults and juveniles, even if conclusions might be limited by the low number of otolith shape analyses performed on juveniles.
  • Combining contaminant, stable isotope and otolith shape analyses provided a basis for the refining of previous knowledge regarding hake contamination in the French Mediterranean, by adding a spatial and temporal component to earlier studies.
  • Consistently with previous results, oligotrophy was the main driver of the “Corsican Hg anomaly”.

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  • ...P-values were calculated by 9999 random permutations of residuals under a reduced model and Type III sum of square (Anderson, 2001)....

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  • ...The most striking feature observed for Hg was the wide spatial difference (PERMANOVA F = 319.40, p 0.0001), driven mostly by the high concentrations measured in Corsica....

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  • ...Average total length was close to 270 mm (Table 1) and not significantly different between sites (PERMANOVA F = 2.16, p= 0.12; Table S2)....

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Frequently Asked Questions (1)
Q1. What are the contributions mentioned in the paper "A multitracer approach to assess the spatial contamination pattern of hake (merluccius merlussius) in the french mediterranean" ?

By combining these approaches with otolith shape analyses, the aim of the present study was to document the spatial variability of Hg and PCB contamination of the European hake ( Merluccius merluccius ) in the French Mediterranean, hypothesizing that local contaminant sources, environmental conditions and biological specificities lead to site-specific contamination patterns.