Bioaccumulation, distribution and elimination of chlordecone in the giant freshwater prawn Macrobrachium rosenbergii: Field and laboratory studies

Highlights

• Chlordecone was accumulated in M. rosenbergii from the first hours of exposure.

• Chlordecone was mainly accumulated in hepatopancreas.

• Chlordecone was also found in cuticle tissue (up to levels of 40%).

• Depuration process of chlordecone was slow (∼94 days to reach the MRL).

Abstract

Chlordecone is a persistent organochlorine pesticide that has been widely used in Guadeloupe (French West Indies) to control the banana weevil Cosmopolites sordidus from 1972 to 1993. A few years after its introduction, widespread contamination of soils, rivers, wild animals and aquatic organisms was reported. Although high chlordecone concentrations have been reported in several crustacean species, its uptake, internal distribution, and elimination in aquatic species have never been described. This study aimed at investigating the accumulation and tissue distribution of chlordecone in the giant freshwater prawn Macrobrachium rosenbergii, using both laboratory (30 days exposure) and field (8 months exposure) approaches. In addition, depuration in chlordecone-free water was studied. Results showed that chlordecone bioconcentration in prawns was dose-dependent and time-dependent. Moreover, females appeared to be less contaminated than males after 5 and 7 months of exposure, probably due to successive spawning leading in the elimination of chlordecone through the eggs. Chlordecone distribution in tissues of exposed prawns showed that cephalothorax organs, mainly represented by the hepatopancreas, was the most contaminated. Results also showed that chlordecone was accumulated in cuticle, up to levels of 40% of the chlordecone body burden, which could be considered as a depuration mechanism since chlordecone is eliminated with the exuviae during successive moults. Finally, this study underlined the similarity of results obtained in laboratory and field approaches, which highlights their complementarities in the chlordecone behaviour understanding in M. rosenbergii.

Introduction

The tropical climate of the French West Indies (FWI) promotes the rapid development of pests which exert significant pressure on crops, leading to the use of considerable amounts of pesticides in these regions (Bocquené and Franco, 2005). The use of organochlorine pesticides first started in the 1950's and led to widespread contamination of the environment (Coat et al., 2006). The most worrying organochlorine pesticide residue for surface water in Guadeloupe (FWI) is chlordecone (C₁₀Cl₁₀O; CAS number 143-50-0) (Coat et al., 2011).

Chlordecone (CLD) is an insecticide whose production started in 1966 under the trade name Kepone^® (Allied Chemical Corporation, Hopewell, VA, USA) mainly for the export to tropical countries, where it was used against a wide range of pests (Dolfing et al., 2012, Sterrett and Boss, 1977). In 1975, the Hopewell accident caused acute toxicity in plant workers (i.e toxicity symptoms in the nervous system, liver and testes - Cannon et al., 1978), as well as extensive contamination of surface water, sediment and aquatic organisms (Huggett and Bender, 1980), leading to its prohibition in 1976 in the US (US ATSDR, 1995). In Guadeloupe, CLD has been commonly employed to control the banana weevil Cosmopolites sordidus from 1972 to 1978 (Kepone^®) and from 1982 to 1993 (Curlone^®) (Cabidoche et al., 2009, Cabidoche et al., 2006). Due to widespread pollution of soils, rivers, wild animals and aquatic organisms (Snegaroff, 1977), CLD was finally prohibited in 1993 (Cabidoche et al., 2009). In 2009, CLD has been included in the Stockholm Convention annexe's, and its production and use were banned worldwide (UNEP, 2009).

Nowadays, CLD is still present in soils, especially in andosols which are rich in organic matter, in the densely cultivated areas of the south of the Basse-Terre Island (Guadeloupe). It was estimated that CLD could persist for several centuries because of its resistance to degradation in the environment (Cabidoche et al., 2009). Although Fernández-Bayo et al. (2013) showed the existence of CLD-degrading microorganisms in andosols under aerobic conditions, CLD undergoes no significant or fast biotic or abiotic degradation (Dolfing et al., 2012, Levillain et al., 2012). In nitisols and ferralsols, CLD is more easily released, and progressively transferred to aquatic ecosystems by the water cycle (Coat et al., 2011). Because of its high Soil Organic Carbon Water Partitioning Coefficient (K_oc = 15849 L kg⁻¹), Octanol-Water Partition Coefficient (log K_ow = 4.5–6.0), and its affinity for lipids, CLD is persistent in the environment and accumulates in the food web (Cabidoche and Lesueur-Jannoyer, 2012, Clostre et al., 2013, Sterrett and Boss, 1977, UNEP, 2005). According to the Direction de l'Environnement, de l'Aménagement et du Logement (DEAL) of Guadeloupe, Guadeloupian rivers are contaminated by CLD at concentrations that ranged from 0.2 to 4 μg L⁻¹ with a maximum of 8.6 μg L⁻¹ measured in the River Grande Anse in 2003 (GREPP, 2004, InVS-Inserm, 2009).

Freshwater and coastal fishes, molluscs and crustaceans are the most contaminated organisms (Bertrand et al., 2010, Cabidoche et al., 2006, Coat et al., 2011, Dromard et al., 2016). Nevertheless, CLD has been detected in blood samples of about 70% of the Guadeloupe population (Guldner et al., 2010, Multigner et al., 2007, Multigner et al., 2006), mainly as a result of consumption of contaminated food, seafood and root vegetables (Dubuisson et al., 2007, Guldner et al., 2010). In such a context, a French legal Maximal Residue Limit (MRL) of 20 μg of CLD per kg wet weight for food of plant and animal origin has been adopted in 2008 (DGS, 2008), causing harsh restriction in fishing and consumption of fish. Furthermore, CLD contamination was detected in farms of the tropical giant freshwater prawn Macrobrachium rosenbergii, an important economic resource in Guadeloupe. This had led to the closure of many aquaculture units in 2008. In addition to be accumulate in organisms, CLD can exert toxic effects as most pesticides, and could disturb critical physiological processes including those controlled by the hormonal system (Giusti et al., 2013, Guzelian, 1982, Lafontaine et al., 2016a, Lafontaine et al., 2016b, Lafontaine et al., 2017). Several studies have demonstrated that CLD could impact the crustacean development, growth and reproduction through disturbance of hormonal processes (Bookhout et al., 1980, Lafontaine et al., 2016a, Lafontaine et al., 2016b, Nimmo et al., 1977, Oberdörster and Cheek, 2001, Sanders et al., 1981, Schimmel et al., 1979, Zha et al., 2007). However, although studies showed toxic effects of pesticides and biocides in M. rosenbergii (Revathi and Munuswamy, 2010, Satapornvanit et al., 2009), very few investigations have been carried out on CLD, especially its uptake and depuration kinetics, as well as its distribution within prawn tissues.

Therefore, the present study aimed at investigating the bioaccumulation and tissue distribution of CLD in the giant freshwater prawn M. rosenbergii, (i) in laboratory conditions (short-term exposure) and (ii) in the field (in situ) conditions (long-term exposure). This work allowed to understand the CLD behaviour in a crustacean decapod considered as a good model for the wild Macrobrachium spp. living in freshwater ecosystems of these regions. In addition, remaining prawns from the long-term exposure were used to investigate CLD depuration. As it is well known that gender can interfere with chemical uptake, distribution and elimination, CLD concentrations were measured separately in males and females when sexual differentiation was possible. Besides filling a knowledge gap on the fate of CLD in tropical prawns, which may help to understand its toxic effects in these organisms, results of this study may have practical implications, for example in the biomonitoring of river contamination, or regulatory control of the safety of marketed food products.