Challenging the paradigms of gut architecture and feeding biomechanics in shallow water polychaetes

Abstract

For well over a century a great deal of effort has been expended into investigation of how polychaetes capture their food but there has been a relative lack of attention paid to the processing of ingested material in the various forms and functioning of the anterior gut in errant polychaetes. The principal focus of this study was the examination of the functional anatomy of the anterior digestive tracts from three families of polychaetes; the Arenicolidae; sedentary detritivores, the Nereidae; errant omnivores and the Nephtyidae; errant carnivores. Comparisons were made with the already well-studied gut anatomy and particularly the pharyngeal anatomy of Arenicola marina, so as to establish a baseline for the other families of polychaetes.

Particular attention was focused on the method of pharyngeal stabilisation in relation to food capture and processing.

It is universally accepted that ‘coelomic pressure’ has been the primary factor in the eversion of the pharynx and proboscis in polychaete worms. This study challenges this hypothesis. This was done with the use of micro-dissection in anaesthetised polychaetes, electro-stimulation, modern light microscopy methods and novel application of micro-computed x-ray tomography. Investigations using scanning
electron microscopy with freeze dried and freeze fractured specimens have revealed a very unusual interlacing muscle fibre pattern, in the Nephtys pharynx. This suggests that specialised pharyngeal muscles, and particularly a newly named muscle, the ventral coelomic muscle (VCM), in Nephtys, may be a primary mover of proboscis eversion rather than as a consequence of an increase in coelomic
pressure. To date, only one other study has recognised this muscle, describing it as a ‘ventral retensor’ that possibly aided in the retraction of the extruded pharynx. The VCM has its origin in the ventral pharynx; it is connected to the anterior intestine, and inserted into the ventral body wall from segment 40-45. This, at least, suggests a stabilising muscle for the pharynx and proximal intestine. The present study’s observations suggest that this muscle is in fact a major player in a primarily muscular driving force for proboscis extrusion. These findings strongly suggest that coelomic pressure increases, associated with proboscis extrusion, are secondary factors in proboscis extrusion in the Nephtyidae. In the Nereidae, it would appear, that the combined action of the powerful longitudinal and circular muscles, together with the firm integrity of the outer body wall, are important players in the muscular extrusion of the pharynx and jaws. Associated increases in coelomic pressure are possibly a secondary effect and linked more with burrowing and body movement
and hydrostatic support.

In errant polychaetes with relatively short straight guts the anterior sections of the gut should be expected to play an important role in food processing, especially as examination of the intestines of many species, especially Nephtyidae, have revealed many of them to be empty.

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