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

Abstract

The relevance of cephalopods for fisheries and even aquaculture, is raising concerns on the relationship between these molluscs and environmental stressors, from climate change to pollution. However, how these organisms cope with environmental toxicants is far less understood than for other molluscs, especially bivalves, which are frontline models in aquatic toxicology. Although, sharing the same basic body plan, cephalopods hold distinct adaptations, often unique, as they are active predators with high growth and metabolic rates. Most studies on the digestive gland, the analog to the vertebrate liver, focused on metal bioaccumulation and its relation to environmental concentrations, with indication for the involvement of special cellular structures (like spherulae) and proteins. Although the functioning of phase I and II enzymes of detoxification in molluscs is controversial, there is evidence for CYP-mediated bioactivation, albeit with lower activity than vertebrates, but this issue needs yet much research. Through novel molecular tools, toxicology-relevant genes and proteins are being unraveled, from metallothioneins to heat-shock proteins and phase II conjugation enzymes, which highlights the importance of increasing genomic annotation as paramount to understand toxicant-specific pathways. However, little is known on how organic toxicants are stored, metabolized and eliminated, albeit some evidence from biomarker approaches, particularly those related to oxidative stress, suggesting that these molluscs' digestive gland is indeed responsive to chemical aggression. Additionally, cause-effect relationships between pollutants and toxicopathic effects are little understood, thus compromising, if not the deployment of these organisms for biomonitoring, at least understanding how they are affected by anthropogenically-induced global change.

Keywords: Cephalopoda; aquatic toxicology; bioaccumulation; biomarkers; mollusca; toxicological pathways.

Figure 1

Comparative histology of the molluscan digestive gland (paraffin sections). bc, basal cells (also called replacement; crypt, basophilic or pyramid cells); dc, digestive cells; dv, digestive vacuoles; hm, haemocytes; it, intertubular tissue; tl, tubule lumen. (A) Digestive gland of the common octopus (Octopus vulgaris) evidencing large digestive tubules (diverticula) formed mostly by digestive cells. The distinctive digestive vacuoles of cephalopods are naturally pigmented and traditionally referred by the French term “boules.” Haematoxylin & Eosin. Scale bar: 25 μm. (B) Micrograph of the digestive gland of a cuttlefish (Sepia officinalis), showing a similar structure to that of Octopus. Brown bodies (bb) are distinctive of sepioids, being comprised of amorphous, undigested, materials. Tetrachrome stain. Scale bar: 25 μm. Inset: Basal cells were observed to hold calcic spherulae that include other metals as well, embedded in a proteinaceous matrix but the issue needs further research. The presence of calcium in spherulae in basal cells is here determined histochemically (stained black) through the von Kossa reaction, counterstained with Nuclear Fast Red (arrowhead). (C) Section through the digestive gland of the marine gastropod Onchidella celtica (Pulmonata), evidencing a similar structure and to that of cephalopods, albeit differences in the histochemical signal of digestive vacuoles, here predominantly blueish (from sugars), likely due to the herbivore feeding regime. The staining is similar to that of the preceding panel. The specimen was fixated in Zenker's solution, which contains (potassium) bichromate that reacts with metallic compounds originating yellow-orange deposits (arrowheads), once again visible in basal cells. Scale bar: 25 μm. (D) Section across the digestive gland of a bivalve (Ruditapes decussata), stained with Haematoxylin and Eosin. The tubules are smaller than previous examples and digestive cells less intricate with respective to variety, quantity and natural coloration of digestive vacuoles, regardless of digestive phase (which is similar among all panels). Basal cells are again evident and bear vesicular-like structures, potentially spherulae or similar. Note the wider and sparser intertubular tissue within which haemocytes can be found, as bivalves have an open circulatory system. Scale bar: 12 μm.