Aspects of the biology of the echiuran worm Bonellia viridis

Abstract

The morphology and histology of the adult female and male of Bonellia viridis is described. Two types of cilia appear to be present on the proboscis surface, normal filamentous cilia, and others with an expanded tip. There are no discrete ciliary tracts, however, there is great variation in density of ciliation in the various regions of the proboscis. The cilia are densest in the fringe region (1000-2000/1000um2) and in the terminal lobe gutters and the lateral margins of the proboscis (1000/1000um2). The dorsal surface of the proboscis is extremely sparsely ciliated except for a short distance form the leading edge which has a dense covering of locomotory cilia. Four different types of burrows have been found in rocks containing Bonellia, of which the largest (UBA burrows), contain three main species: Upogabia daltaura, B. viridis and Alphaus dentipes. Evidence is provided that Upogabia is responsible for the burrows, though Bonellia may secondarily modify them. Bonellia is negatively phototactic, and sensitive to mechanical stimulation. There is a definite Upogebia-Bonellia-Alpheus community. A food web is suggested. an account is given of the various movements of the trunk and proboscis of B. viridis. Trunk irrigatory and locomotory movements consist of peristaltic waves of constriction. Irrigation is by means of antero-posterior waves. Locomotion in the burrow may be produced in three different ways (i) by antikinetic, (ii) by synkinetic and (iii) by antikinetic and synkinetic waves in strict alternation. Bonellia can turn in the burrows and pass out of narrow holes. The animal can move by peristalsis also outside the burrow. When at rest the proboscis is coiled in front of the trunk. the proboscis lobes progress away from the trunk by means of the powerful cilia situated on the ventral surface of the leading edge. The lobes passively drag and uncoil the proboscis stem which is further uncoiled by muscular contraction taking place along the uncoiled part of the stem. Proboscis contraction is strictly muscular. The terminal lobe can attach to the substrate of the proboscis stem. The proboscis often ties itself into a knot which it can untie. The versatility of locomotory modes is related to the fact that Boneilia inhabits ready-made burrows. The feeding behaviour of Bonellia is described. Small individual particles (=<94pm) are taken up by the proboscis by means of cilia, those of intermediate size (~150um) by a combination of ciliary and muscular activity, while larger particles (230-290um) are picked up by muscular notion. Large accumulations of particles are shovelled onto the ventral surface of the terminal lobes by active muscular notion. The ciliary currents on the ventral surface of the proboscis are mapped. Transport along the proboscis may be ciliary for the smallest particles (=<290um); ciliary and muscular for the intermediate sizes (230-480um); or purely muscular for the largest particle (500um). Particles may be rejected at various levels along the proboscis, the site of rejection also being dependant on size. When presented with a monolayer of clean sand grains of different sizes, most animals only pick up particles of ~150um and less. When presented with a choice of clean sand grains or sand enriched with various plant and animal extracts, the terminal lobes actively pick up enriched particles but not, to any appreciable extent, the clean sand. The terminal lobes are not attracted to the enriched substrate from a distance, but, once on the enriched substrate they spend significantly more time on Isochrysis-enriched sand. With two other plant-enriched substrates (Phaedactylum, Ulva) they again spend more time on them than on clean sand, though the difference is not statistically significant. The terminal lobes do not feed exclusively on enriched substrates but graze over all the are available. The structure of the faecal pellets is described and a rough analysis of their content made. The alimentary canal of Bonellia contains an amylase, a lipase, a protease but no cellulase. The foregut has pH of 6.70, the midgut a pH of 7.26 and the hindgut a pH of 7.32. The variation of amylase, lipase and protease activity with temperature at constant pH is determined and the relative activity of the various enzymes in the different regions of the gut estimated. Digestion takes place mainly in the midgut, though both foregut and hindgut show some enzymic activity. The digestive enzymes of Bonellia are similar to those of other echiurans and detritus feeding polychaetes due to parallelism or convergence since they all exploit the same food source. The palatability of the proboscis and body-wall tissues of Bonellia were on the shrimp Palaemon elegans, two species of fish and on an anthozoan. P. elegans refused to feed on Bonellia tissues when offered a choice. When Bonellia tissue is mixed with mussel in varying proportions, starved P. elegans consume progressively less of the mixture as the proportion of Bonellia tissue to mussel meat increases. Bonellia/mussel tissue mixture containing high proportions of Bonellia were also found to be unpalatable to the other animals tested. The green integumentary pigment of B. viridis, bonellin, is a chlorin, and not derived from chlorophyll. Solutions of bonellin were shown to paralyze sperm of Arbacia, the activity of the solutions decreasing with decreasing concentration. The porphyrins, chlorophyll, haemin, and anhydrobonellin Me-ester are shown not to be active. Solutions of bonellin gave negative results when tested on frog sciaticgastrocnemius and frog hear preparations. It is postulated that Bonellin individuals secrete pigment when irritated and this acts as a chemical defense. Bonellin probably acts partly through photosensitization of tissues and partly through an intrinsic bioactivity. Fertilizations in Bonellia is internal. About a 1000 eggs are laid which hatch into free-swimming trochophore larvae in 48 hours at 20°C. After some 7-21 days the trochophores settle and metamorphose. In the conditions of culture employed in this study, 98% of the indifferent larvae settle on the proboscis of a female worm when it is available and become males while when cultured in isolation from the adult females, 85% of the indifferent larvae settle on the bottom and become females. It has been postulated by many authors that the female worm secretes an ectohormone which causes the indifferent larvae to become males. In the absence of this hormone, the larvae become females. When indifferent larvae were cultured in 1 ppm, 0.5 ppm, 0.2 ppm and 0.01 ppm bonellin seawater solutions, 31.3%, 36.5%, 14.4% and 44.5% became masculinized. Bonellin is postulated to act through a switch mechanism. Bonellin or a close derivative is probably the natural ectohormone of Bonellia. These findings are interpreted in the light of Baltzer's theory that sex determination in Bonellia is due to both genetic and environmental factors. A possible evolutionary history of sex-determination in bonellids from ancestors with external fertilization and an equal sex-ratio through various intermediate stages to the present condition of metagamic sex determination is given.