Can Cephalopods Vomit? Hypothesis Based on a Review of Circumstantial Evidence and Preliminary Experimental Observations.

António V Sykes,Gavan M Cooke,Eduardo Almansa,Paul L R Andrews,Giovanna Ponte

doi:10.3389/fphys.2020.00765

Abstract

In representative species of all vertebrate classes, the oral ejection of upper digestive tract contents by vomiting or regurgitation is used to void food contaminated with toxins or containing indigestible material not voidable in the feces. Vomiting or regurgitation has been reported in a number of invertebrate marine species (Exaiptasia diaphana, Cancer productus, and Pleurobranchaea californica), prompting consideration of whether cephalopods have this capability. This “hypothesis and theory” paper reviews four lines of supporting evidence: (1) the mollusk P. californica sharing some digestive tract morphological and innervation similarities with Octopus vulgaris is able to vomit or regurgitate with the mechanisms well characterized, providing an example of motor program switching; (2) a rationale for vomiting or regurgitation in cephalopods based upon the potential requirement to void indigestible material, which may cause damage and ejection of toxin contaminated food; (3) anecdotal reports (including from the literature) of vomiting- or regurgitation-like behavior in several species of cephalopod (Sepia officinalis, Sepioteuthis sepioidea, O. vulgaris, and Enteroctopus dofleini); and (4) anatomical and physiological studies indicating that ejection of gastric/crop contents via the buccal cavity is a theoretical possibility by retroperistalsis in the upper digestive tract (esophagus, crop, and stomach). We have not identified any publications refuting our hypothesis, so a balanced review is not possible. Overall, the evidence presented is circumstantial, so experiments adapting current methodology (e.g., research community survey, in vitro studies of motility, and analysis of indigestible gut contents and feces) are described to obtain additional evidence to either support or refute our hypothesis. We recognize the possibility that further research may not support the hypothesis; therefore, we consider how cephalopods may protect themselves against ingestion of toxic food by external chemodetection prior to ingestion and digestive gland detoxification post-ingestion. Reviewing the evidence for the hypothesis has identified a number of gaps in knowledge of the anatomy (e.g., the presence of sphincters) and physiology (e.g., the fate of indigestible food residues, pH of digestive secretions, sensory innervation, and digestive gland detoxification mechanisms) of the digestive tract as well as a paucity of recent studies on the role of epithelial chemoreceptors in prey identification and food intake.

Highlights

In the obligative act of eating, animals expose themselves to the ingestion of food potentially contaminated with toxins, which may not have been detected by vision, olfaction, or gustation prior to swallowing (Davis et al, 1986; Glendinning, 2007); these systems are considered the first line of defense
Other strategies in vertebrates include, for example, vision, taste, smell, learned aversions, ingestion of clay to adsorb toxins, and hepatic detoxification (Davis et al, 1986; Glendinning, 2007; Stern et al, 2011). This hypothesis focuses on the possibility of vomiting or regurgitation in cephalopods, so a detailed discussion of all the potential toxin defensive mechanisms is outside the immediate scope of this paper, and functions of vomiting or regurgitation may extend beyond toxin defense
We describe examples of vomiting/regurgitation from three classes (Anthozoa, Malacostraca, and Gastropoda) of marine invertebrate solely to illustrate that this ability is not confined to marine vertebrates

Summary

INTRODUCTION

In the obligative act of eating, animals expose themselves to the ingestion of food potentially contaminated with toxins, which may not have been detected by vision, olfaction, or gustation prior to swallowing (Davis et al, 1986; Glendinning, 2007); these systems are considered the first line of defense. Assuming that cephalopods are able to vomit or regurgitate, the most likely functions are periodic ejection of indigestible material (e.g., crustacean exoskeleton pieces, fish bones and scales, and plastic fragments) and acute ejection of toxic food before the toxin can be absorbed in sufficient quantity to have systemic toxic effects These functions will depend on the diet of the species, so it is conceivable that not all species may have the capacity to either vomit or regurgitate, so formal investigation may require studies in representatives of at least each sub-class. Measurement of viscosity of crop/stomach contents at various stages of digestion would be useful for theoretical modeling of the forces required for vomiting/regurgitation in cephalopods Such modeling is likely to be challenging as full mathematical modeling of defecation in penguins (Pygoscelis antarcticus and Pygoscelis adeliae) was confounded by the inability to measure the viscosity of fecal samples due to the presence of crustacean cuticle, fish bones and scales, and other solid fragments (Meyer-Rochow and Gal, 2003)

DISCUSSION

A Conceptual Model of Vomiting or Regurgitation in Cephalopods

Findings

CONCLUSION

DATA AVAILABILITY STATEMENT