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. 2020 Jul 23:11:765.
doi: 10.3389/fphys.2020.00765. eCollection 2020.

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

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

António V Sykes et al. Front Physiol. .

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.

Keywords: Octopus vulgaris; Sepia officinalis; digestive tract; motility; nutrition; regurgitation; vomiting; welfare.

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Figures

Figure 1
Figure 1
The brain of Octopus vulgaris as it appears using sonographic scanning (for additional details see Grimaldi et al., 2007) and histological sections after Nissl staining (in black and white). (A) Ultrasound examination (left) of the entire cerebral mass in the coronal plane, and the corresponding histological section (right). The optic lobes are visible bilaterally and appear connected through the optic tracts to the central brain (supraesophageal mass, SEM). The subesophageal mass (SUB) lies ventrolateral to the esophagus (Es). (B) Ultrasound examination of the central brain in the sagittal plane (left), and the equivalent histological section (right). The two masses (SEM and SUB: dorsally and ventrally, respectively) are clearly visible with the esophagus in the middle. OL, optic lobe; Es, esophagus; SEM, supraesophageal mass; SUB, subesophageal mass. Scale bars: 5 mm.
Figure 2
Figure 2
Pictures taken each second (1–18 s) from a video recording of the digestive tract of O. vulgaris, in vitro (in sea water gassed with air). The animal had been fed a crab 1 h before killing (see Fiorito et al., 2015). The sequence shows the progression of a peristaltic wave (indicated by a white dot) from close to its origin and progressing aborally to the crop/stomach junction. The pressure created by the contraction moves material (yellow arrow) from the crop to the stomach and it is no longer visible after Frame 10. In Frame 16, the crop contraction reaches the stomach and in frames 17 and 18, the contraction subsides allowing material (yellow arrow) to reflux from the stomach toward the crop. The vertical axis of the frames is ~8 cm. B, beak; Es, esophagus; Cr, crop; and St, stomach.
Figure 3
Figure 3
(A) Video frame showing the beak, esophagus, crop, and stomach in vitro (see above text for details) from an O. vulgaris fed a crab 1 h before killing. The vertical axis of the frame is ~8 cm. Arrows indicate the measurements made of the apparent diameter of the lower crop (blue), distal crop (red) at the crop-stomach junction and the length of the crop (green). B, beak; Es, esophagus; Cr, crop; St, stomach. (B) Measurements of the changes in the dimensions of the crop made in vitro from an animal fed a crab 1 h before killing. The measurements defined above are made each second from 100 s of video recording (see Figure 2) and show two cycles of contraction. All measurements are expressed as a percentage change relative to those taken at t = 1 s. The two contractile cycles closely duplicate each other ~1 min apart. The graph shows the wave of contraction of the lower-crop (1) passes to the distal crop (2). The contraction of the distal crop is accompanied by longitudinal shortening of the crop (3). Note that both the lower and distal crop change apparent diameter by ~50% during the passage of the peristaltic contraction.

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