The suspension feeding mechanism of the larval lamprey Petromyzon marinus

Abstract

Larval lampreys (ammocoetes) feed by trapping small, water‐borne particles in mucus within the pharynx. Details of the feeding mechanism were studied; specifically, the morphology of feeding structures, the flow pattern of food‐containing water through the pharynx, and the food entrapment process per se.Pharyngeal morphology was studied in ammocoetes of several genera through both gross dissection and histochemistry (Alcian blue and PAS). In all genera, dense accumulations of goblet cells were found to occupy the most lateral parts of the pharynx. These cells are of two types, secreting an acidic and neutral (at pH 2.5) mucus, respectively.Similarities in pharyngeal pumping movements and in pharyngeal morphology indicate that ammocoetes ventilate like other fish, with a dual pharyngeal pump providing a basically unidirectional, lateral flow of water across the gills. Ammocoete ventilation is unusual, however, in that a small amount of water is sucked back into the pharynx through the gill pores during the inspiratory phase of each ventilatory cycle.The entrapment process was investigated in Petromyzon marinus by dissecting the pharynges of feeding animals killed by electric shock. The pharynges contained a series of mucous tributaries, one occupying each gill pouch. An experiment in which the lateral parts of the tributaries were labelled indicate the tributaries move continually inward to a central, longitudinal mucous cord. The latter in turn moves postcriorly to the oesophagus. The mucus is constantly produced by the goblet cells at the lateral sites of origin of the flowing complex. Suspended food particles are trapped all along this mass, although larger particles preferentially are trapped medially. The complex seems to be propelled by ciliary action, for intrapharyngeal ciliary tracts are associated with moving portions of the complex. Ventilatory water currents also may help move the mucous complex. Particles are aggregated, and mucus is condensed, in the lateral parts of the complex. The subpharyngeal gland (endostyle) secretes digestive enzymes into the condensed central portion. Because the endostyle is situated medially and the feeding mucus complex originates laterally, the former does not seem to be the source of the latter. This is contrary to common view.Consistent with this concept of the feeding mechanism is the fact that all structures implicated in larval feeding are absent from the adult pharynx, which is not involved in suspension feeding. Paradoxically, pharyngeal goblet cells are retained until the final stages of metamorphosis, well beyond the stage at which suspension feeding ceases.Morphological similarity suggests that ammoetes of all three lamprey families feed similarly.Whether suspension feeding was the ancestral vertebrate feeding mode is assessed through comparing the feeding mechanisms of ammocoetes and protochordates (Branchiostoma). Although differences exist, similarities in the locations of (a) branchial mucous cells and, (b) ciliary tracts involved in feeding, favour the claim for common ancestry.