The anus as a second mouth: anal suspension feeding by an oral deposit-feeding sea cucumber

Respiratory trees of holothurians are blind-ended evaginations of the posterior digestive system that are rhythmically inflated with seawater via the anus, and are considered to have respiratory and excretory functions. We tested the assimilatory capability of the respiratory tree epithelium by exposing adults of the oral deposit-feeding aspidochirotid sea cucumber Parastichopus californicus to (1) 14C-labeled unicellular algae and (2) iron-containing macromolecules, and then following the distribution of the labels in various body regions. The abundance of the 14C (nmol 14C g wet weight1) varied among body regions. The majority of the label was associated with the respiratory trees. The next greatest concentration was in the rete mirabile of the hemal system. The amount of 14C within samples of the anterior digestive system, posterior digestive system, and body wall muscle at each sampling time was lower than that of the respiratory trees. The presence and abundance of the 14C label in samples of the hemal system and the physical association between the respiratory tree and the rete mirabile suggest initial uptake by the respiratory tree and subsequent transfer to the hemal system. The iron label from the protein ferritin and the polysaccharide iron dextran entered cells of the respiratory tree luminal epithelium. The presence of the iron label in mesenchyme cells within the connective tissue compartment of the respiratory trees exposed to ferritin further suggests directional transfer of materials. Holothurians with respiratory trees are nutritionally bipolar; the anus serves as a second mouth.