Elsevier

Marine Pollution Bulletin

Volume 91, Issue 1, 15 February 2015, Pages 191-199
Marine Pollution Bulletin

Are red mullet efficient as bio-indicators of mercury contamination? A case study from the French Mediterranean

https://doi.org/10.1016/j.marpolbul.2014.12.005Get rights and content

Highlights

  • Hg was monitored in Mullus spp. from 5 French Mediterranean zones during 18 months.

  • All concentrations were below recommended European health safety levels.

  • Hg trends were consistent with environmental contamination except in Corsica.

  • Oligotrophy could explain the high and unexpected values in Corsica.

  • Biotic and abiotic parameters must been considered when using bioindicators.

Abstract

Mercury (Hg) is one of the main chemicals currently altering Mediterranean ecosystems. Red mullet (Mullus barbatus and M. surmuletus) have been widely used as quantitative bio-indicators of chemical contamination. In this study, we reassess the ability of these species to be used as efficient bio-indicators of Hg contamination by monitoring during 18 months Hg concentrations in muscle tissue of mullet sampled from 5 French Mediterranean coastal areas. Mean concentrations ranged between 0.23 and 0.78 μg g−1 dry mass for both species. Values were consistent with expected contamination patterns of all sites except Corsica. Results confirmed that red mullets are efficient bio-indicators of Hg contamination. Nevertheless, the observed variability in Hg concentrations calls for caution regarding the period and the sample size. Attention should be paid to environmental and biologic specificities of each studied site, as they can alter the bioaccumulation of Hg, and lead to inferences about environmental Hg concentrations.

Introduction

Chemical contamination is one of the main threats currently causing alteration to marine ecosystems (Halpern et al., 2008), with observed impact on individuals, populations, species and ecosystems (Fleeger et al., 2003). Chemical pressure is high in the Mediterranean Sea, a semi-enclosed sea surrounded by highly industrialized and densely populated countries (Durrieu de Madron et al., 2011). Among all chemicals, mercury (Hg) is of great concern, as it has neurotoxic, immunotoxic and teratogenic effects on vertebrates (Scheuhammer et al., 2007, Tartu et al., 2013). Metallic mercury (Hg0) is emitted in the environment from natural (mainly volcanic emissions) and anthropogenic sources, with an increase in the anthropogenic sources since the end of the 18th century (Streets et al., 2011). Hg0 is highly volatile and can be transported during long periods of time and over long distances. After deposition as HgII, Hg is methylated by heterophic bacteria as methylmercury (MeHg). In marine environments, this process occurs in low oxygen zones in the water column, and at the water/sediment interface (Blum et al., 2013, Cossa et al., 2009, Heimbürger et al., 2010). MeHg is the chemical form of Hg of greatest concern, as it can enter the trophic networks after being uptaken by the phytoplankton. High MeHg concentrations are observed in high trophic level species, due to the high level of biomagnification of MeHg throughout the trophic networks. To cope with such high Hg concentrations, physiological mechanisms were developed against the adverse effect of metallic contaminants. The synthesis of metallothionein is commonly proposed as an important detoxifying mechanism in fishes. Metallothionein is a class of low molecular-weight proteins able to bind to metals and to play a role in the detoxifying process as high metallothionein concentration are measured in fish sampled in contaminated zones (Filipović and Raspor, 2003, Zorita et al., 2008). Others detoxifying mechanisms can involve antioxidant synthesis or metabolisation of contaminants in the liver (Company et al., 2010).

Monitoring Hg contamination can by performed by assessing environmental concentrations in water or sediment. This approach produces an immediate measure of contamination in a specific place but is complex to use, mainly due to low concentrations and the high temporal and spatial variability observed. In addition, high contaminant concentrations in the environment do not always lead to high values and adverse effects on organisms and vice-versa (Beyer et al., 1996, Martínez-Gómez et al., 2012). Consequently, in most cases, contamination has been assessed by bio-monitoring, i.e. inferring the contamination in the environment from values measured in organisms. This approach can provide time and space integrated information about the actual Hg contamination, and also about the bio-available fraction of the contaminant, which actually enters the trophic networks. Determining Hg concentrations in marine organisms is also required for sanitary purpose, as consumption of contaminated products is the main pathway leading to human intoxication (Endo et al., 2013, Martí-Cid et al., 2007). Nevertheless, this approach is rendered complex because of the influence of various biotic and abiotic factors on the bioaccumulation (Phillips and Rainbow, 1998).

Red mullet (Mullus spp.) exhibit several features allowing them to be considered as appropriate bio-indicators of mercury contamination. These species are observed off all Mediterranean shores, providing a basis for wide-ranging geographical comparison of the results (Kucuksezgin et al., 2001, Labropoulou et al., 1997, Lombarte et al., 2000, Morat et al., 2012, Reñones et al., 1995, Tserpes et al., 2002). The biological and ecological features of this species, such as diet, growth, spatial patterns and reproduction have been extensively studied and may provide a basis for explaining the contamination patterns observed (Bautista-Vega et al., 2008, Cresson et al., 2014a, Cresson et al., 2014b, Labropoulou et al., 1997, Lombarte et al., 2000, Machias et al., 1998, Machias and Labropoulou, 2002, Morat et al., 2012, Reñones et al., 1995). Since food is considered to be the main source of Hg contamination in fish (Hall et al., 1997), a good knowledge of dietary habits is crucial to the understanding of contamination patterns. Both M. barbatus and M. surmuletus have similar mesocarnivorous diets based on benthic invertebrates, such as crustaceans and annelids (Bautista-Vega et al., 2008, Cresson et al., 2014b, Labropoulou et al., 1997, Machias and Labropoulou, 2002). With increasing size, M. barbatus changes its diet, consuming larger shrimps and annelids and avoiding small crustaceans. In contrast, M. surmuletus has the same diet whatever the size (Bautista-Vega et al., 2008, Labropoulou et al., 1997). Mullus species are considered to be rather territorial (Morat et al., 2012), even if spatial and depth segregation between large and small individuals has been reported (Lombarte et al., 2000). Due to their strong benthic affinity, their burrowing activity and the low range of movement of these species, the level of contamination in Mullus spp. can be considered representative of the local contamination level in the environment. These species are also expected to accumulate pollutants at a higher rate than other fish species (Zorita et al., 2008) and were recommended as suitable species for the monitoring of environmental contamination (UNEP/RAMOGE, 1999). Finally, these species have a commercial value and have been fished mainly by small-scale coastal fisheries since Roman and Greek antiquity (FAO, 2012, Leleu et al., 2014, Tipton, 2008, Tserpes et al., 2002). For the French Mediterranean, red mullet annual catches ranged between 280 and 500 metric tons before 1990 and decreased to nearly 200 t in recent years (FishStatJ, FAO). A high Hg concentrations in muscle tissue of fish could thus represent a concern for human health. As a consequence, Hg concentrations have been extensively surveyed in Mullus surmuletus and M. barbatus throughout the Mediterranean Sea (Capelli et al., 2004, Conti et al., 2012, Copat et al., 2012, Corsi et al., 2002, Falcó et al., 2006, Harmelin-Vivien et al., 2009, Kucuksezgin et al., 2001, Martínez-Gómez et al., 2012). But as previously observed by Dierking et al. (2009), most of the studies on contamination in fish were carried out over a single area, where contamination was expected to be high. Similarly, papers comparing Hg concentration in M. barbatus and M. surmuletus are scarce (e.g., Harmelin-Vivien et al., 2009) and no data are available regarding temporal variations of Hg content of the fish tissue. Finally, no study has investigated Hg concentration in fishes from Corsica. Consequently, on the basis of sampling of M. barbatus and M. surmuletus from five French Mediterranean coastal zones during 18 months, we assessed temporal and spatial patterns of Hg concentrations in Mediterranean red mullet muscle, and determined to what extent these species can be considered as good quantitative bio-indicators of Hg contamination of their surrounding environment.

Section snippets

Sample collection and preparation

Individuals of the two main Mediterranean mullid species (Mullus barbatus barbatus Linnaeus, 1758, hereafter M. barbatus and Mullus surmuletus Linnaeus, 1758) were collected every two months from June 2012 to December 2013 by fishermen operating trammel nets in shallow (∼20–50 m depth) coastal waters of the French Mediterranean (Fig. 1), at two sites in the Gulf of Lions (Banyuls-sur-Mer, hereafter Banyuls, and Sète), two in the Provence area (La Seyne-sur-Mer, hereafter La Seyne, and Nice) and

Sample size, biometry and age

A total of 1042 fishes were captured, including 556 Mullus surmuletus and 486 M. barbatus. M. surmuletus was the predominant species at all sites except at Nice (Table 1). The actual number of fishes by species, site and date is detailed in Table S2. Individuals aged 1 and 2 years represent 90% of the sampling (496 and 328 respectively), followed by individuals aged 3 (69). Individuals aged 0 and 4 years were under-represented (22 and 2 respectively). Significant differences of fish length between

Discussion

Albeit Hg content has been largely investigated in Mediterranean red mullet (M. barbatus and M. surmuletus), few studies have compared results obtained from different areas. Similarly, seasonal variations of Hg concentration have rarely been investigated in marine teleosts whereas seasonal cycles can potentially affect Hg concentrations. This study has made good this lack, and identified certain features that may be the cause of the patterns observed.

Conclusions

The results obtained here confirmed that Mullus spp. caught along the French Mediterranean coast are efficient bio-indicators of mercury contamination. This is not surprising as those species have been identified as such and already used in several studies. The geographical trend observed is consistent with knowledge regarding different levels of chemical contamination, mainly at La Seyne on the one hand and at Sète and Banyuls on the other hand. In addition, as M. barbatus and M. surmuletus are

Acknowledgements

Thanks are due to the fishermen (Frederic Le Guen, Philippe Mazel and Julien Grodeau) and to our colleagues (Yves Dimeglio, IRSN La Seyne sur Mer, Yoan Baldi, Ifremer, LER/PAC, Bastia and Jean Michel Cottalorda, ECOMERS, Nice University) who caught and processed the fishes. Special thanks to F. Le Guen who kindly provided information on his fishing practices and observations about red mullet. We would also like to thank Jean-François Chiffoleau (Ifremer, LBCM Nantes) for data on Hg

References (69)

  • B.K. Greenfield et al.

    Seasonal and annual trends in forage fish mercury concentrations, San Francisco Bay

    Sci. Total Environ.

    (2013)
  • M. Harmelin-Vivien et al.

    Difference of mercury bioaccumulation in red mullets from the north-western Mediterranean and Black seas

    Mar. Pollut. Bull.

    (2009)
  • L.E. Heimbürger et al.

    Methyl mercury distribution in relation to the presence of nano- and picophytoplankton in an oceanic water column (Ligurian Sea, North-western Mediterranean)

    Geochem. Cosmochim. Acta

    (2010)
  • F. Kucuksezgin et al.

    Trace metal and organochlorine residue levels in red mullet (Mullus barbatus) from the Eastern Aegean, Turkey

    Water Res.

    (2001)
  • F. Kucuksezgin et al.

    Evaluations of heavy metal pollution in sediment and Mullus barbatus from the Izmir Bay (Eastern Aegean) during 1997–2009

    Mar. Pollut. Bull.

    (2011)
  • M. Labropoulou et al.

    Feeding habits and ontogenetic diet shift of the striped red mullet, Mullus surmuletus Linnaeus, 1758

    Fish. Res.

    (1997)
  • C. Lafabrie et al.

    Trace metals assessment in water, sediment, mussel and seagrass species–validation of the use of Posidonia oceanica as a metal biomonitor

    Chemosphere

    (2007)
  • K. Leleu et al.

    Métiers, effort and catches of a Mediterranean small-scale coastal fishery: the case of the Côte Bleue Marine Park

    Fish. Res.

    (2014)
  • A. Machias et al.

    Intra-specific variation in resource use by red mullet, Mullus barbatus

    Estuar. Coast. Shelf Sci.

    (2002)
  • M.C. Magalhães et al.

    Intra- and inter-specific variability in total and methylmercury bioaccumulation by eight marine fish species from the Azores

    Mar. Pollut. Bull.

    (2007)
  • R. Martí-Cid et al.

    Intake of chemical contaminants through fish and seafood consumption by children of Catalonia, Spain: health risks

    Food Chem. Toxicol.

    (2007)
  • C. Martínez-Gómez et al.

    Health status of red mullets from polluted areas of the Spanish Mediterranean coast, with special reference to Portmán (SE Spain)

    Mar. Environ. Res.

    (2012)
  • C. Pergent-Martini

    Posidonia oceanica: a biological indicator of past and present mercury contamination in the Mediterranean sea

    Mar. Environ. Res.

    (1998)
  • G. Pergent et al.

    Organic and inorganic human-induced contamination of Posidonia oceanica meadows

    Ecol. Eng.

    (2011)
  • M.M. Storelli et al.

    Mercury speciation in the muscle of two commercially important fish, hake (Merluccius merluccius) and striped mullet (Mullus barbatus) from the Mediterranean sea: estimated weekly intake

    Food Chem.

    (2005)
  • E. Tessier et al.

    Study of the spatial and historical distribution of sediment inorganic contamination in the Toulon bay (France)

    Mar. Pollut. Bull.

    (2011)
  • L. Tolga Gonul et al.

    Mercury accumulation and speciation in the muscle of red mullet (Mullus barbatus) and annular sea bream (Diplodus annularis) from Izmir Bay (Eastern Aegean)

    Mar. Pollut. Bull.

    (2007)
  • V. Vassilopoulou et al.

    Factors influencing the uptake of PCBs and DDTs in red mullet (Mullus barbatus) from Pagassitikos Gulf, central Greece

    Mar. Pollut. Bull.

    (1993)
  • I. Zorita et al.

    Assessment of biological effects of environmental pollution along the NW Mediterranean Sea using red mullets as sentinel organisms

    Environ. Pollut.

    (2008)
  • A.A. Bautista-Vega et al.

    Difference in diet and size-related trophic level in two sympatric fish species, the red mullets Mullus barbatus and Mullus surmuletus, in the Gulf of Lions (north-west Mediterranean Sea)

    J. Fish Biol.

    (2008)
  • J.D. Blum et al.

    Methylmercury production below the mixed layer in the North Pacific Ocean

    Nat. Geosci.

    (2013)
  • Bosc, E., Bricaud, A., Antoine, D., 2004. Seasonal and interannual variability in algal biomass and primary production...
  • R. Capelli et al.

    Study of the distribution of trace elements in marine organisms of the Ligurian Sea (North-Western Mediterranean) – comparison with previous findings

    Anal. Chim.

    (2004)
  • G.O. Conti et al.

    Evaluation of heavy metals and polycyclic aromatic hydrocarbons (PAHs) in Mullus barbatus from Sicily Channel and risk-based consumption limits

    Bull. Environ. Contam. Toxicol.

    (2012)
  • Cited by (0)

    View full text