Metal bioaccumulation and detoxification processes in cephalopods: A review

Abstract

In recent decades, cephalopods have been shown to have very high capacities to accumulate most trace elements, regardless of whether they are essential (e.g., Cu and Zn) or non-essential (e.g., Ag and Cd). Among the different pathways of exposure to trace elements, the trophic pathway appears to be the major route of assimilation for numerous metals, including Cd, Co, Hg and Zn. Once assimilated, trace elements are distributed in the organism, accumulating in storage organs. The digestive gland is the main organ in which many trace elements accumulate, whichever of the exposure pathway. For example, this organ can present Cd concentrations reaching hundreds to thousands of ppm for some species, even though the digestive gland represents only a small proportion of the total mass of the animal. Such a specific organotropism towards the digestive gland of both essential and non-essential elements, regardless of the exposure pathway, poses the question of the detoxification processes evolved by cephalopods in order to sustain these high concentrations. This paper reviews the current knowledge on the bioaccumulation of trace elements in cephalopods, the differences in pharmaco-dynamics between organs and tissues, and the detoxification processes they use to counteract trace element toxicity. A peculiar focus has been done on the bioaccumulation within the digestive gland by investigating the subcellular locations of trace elements and their protein ligands.

The Role of the Cephalopod Digestive Gland in the Storage and Detoxification of Marine Pollutants

“…The vast majority of literature focusing on toxicants in cephalopods relates to metals, as cephalopods are known to bioaccumulate impressive amounts of hazardous elements, like Cd, albeit others, such as Hg, appearing to be less significant, which indicates metal- and organ-specific pathways (Penicaud et al, 2017). It has been shown that the digestive gland holds the highest concentrations of essential (like Cu and Zn) and non-essential (such as Ag, Cd and Pb) metals in several cephalopods, with emphasis on Sepia and Octopus , comparatively to other organs, mantle and arms included, the latter of which raise particular concerns regarding human consumption (e.g., Raimundo et al, 2004, 2005; Seixas et al, 2005; Bustamante et al, 2006; Pereira et al, 2009).…”

“…However, in cephalopods, MT induction in the digestive gland may not be entirely consistent with exposure to metals, even in the case of exposure to strong inducers such as Cd (Bustamante et al, 2002a; Raimundo et al, 2010b; Rodrigo et al, 2013). It is possible that elements such as Cd, are not involved in detoxification via spherulae (thus remaining in the cytoplasmic fraction), which in its turn, relies on MT and, potentially, unknown high molecular weight proteins (see Penicaud et al, 2017, for a summary). This interesting perspective, indicates that there can be novel mechanisms of toxicity and detoxification of non-essential metals like Cd in cephalopods that need to be unraveled.…”

“…However, the physiological and molecular mechanisms underlying toxicopathological effects and detoxification processes in cephalopods are not well understood, albeit the importance of other molluscs, especially bivalves, in biomonitoring and substance testing. Overall, most studies concerning exposure of cephalopods to marine contaminants relate to the accumulation of trace elements, in most cases being limited to commercial species (see Penicaud et al, 2017). …”

“…It is suggested that storing metals in various tissues can be an important strategy to cope with metal toxicity (see Miramand and Bentley, 1992; Bustamante et al, 2000; Raimundo et al, 2005 plus the recent review by Penicaud et al, 2017). This efficient strategy, which likely minimizes energetic costs, is seemingly common among Nautiloid and Coleoid cephalopods (Bustamante et al, 2000).…”

The potential role of spherocrystals in the detoxification of essential trace metals following exposure to Cu and Zn in the fighting conch Strombus (Lobatus) pugilis

“…The digestive gland of mollusks is a key organ involved in the digestion but also in lipid storage, mineral osmoregulation, and metal detoxification (Owen 1966;Voltzow 1994;Porcel et al 1996;Penicaud et al 2017). Most ecotoxicological studies have investigated the impact of metal exposure on i) the organ metal burden and ii) the subcellular partitioning of metals obtained by differential centrifugation.…”