Spoon, a worm

There now follows an extract from the Encyclopaedia Britannica, 1964 edition, volume 7, starting from page 898 and continuing until page 901. The information printed here is the complete text reference given from the book. Copyright under International Copyright Union.

This work was written by Grace Evelyn Pickford, Research Associate, Bingham Oceanographic Laboratory; Associate Professor, Department of Zoology, Yale University.

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  ECHIURIDA (ECHIUROIDEA), a phylum of generally sausage-shaped marine worms that, in spite of an apparent lack of segmentation, must be considered nearly related to the Annelida (q.v.).  Although formerly considered a class and placed in the obsolete phylum Gephyrea, together with Sipunculida (q.v.) and Priapulida (q.v.), echiuroids have little in common with the former, and it is probable that supposed relationships with the latter can be altogether discounted.


  Typical representatives of the Echiurida are several species that, because of the extended scooplike proboscis (prostomium) overhanging the mouth, are called spoon-worms.  Spoon-worms are moderately large, sac-shaped creatures that inhabit U-shaped tubes on sandy mud bottoms.  The northern cold water species, Echiurus echiurus, is described below as an example.
  External Features.—The body consists of a cylindrical trunk which reaches a length of 12 cm. or more, and a preoral lobe or prostomium, shaped like a hemispherical fan when fully extended, which is about half as long as the trunk.  The prostomium is ciliated on its ventral surface and its margins are fused at the base, forming a funnel around the mouth.  During feeding the prostomium is extended over the surface of the surrounding mud, and particles of detritus are swept along ciliary tracks toward the mouth.
  The trunk is encircled by rings of mucous-secreting papillae, the slime being used to line the walls of the burrow.  The anus is terminal.
  Autonomy (Self-Amputation).—The prostomium is readily detatched from the trunk, less so in the Alaskan than in the European subspecies.  The body wall in the area of detachment is thinned forming a special autotomization ring behind the mouth, and in front of this ring is a powerful sphincter muscle, which upon sudden contraction discards the anterior end.  The trunk regenerates the missing parts within a few weeks and feeding is then resumed.
  Setae.—At the anterior end, behind the mouth, is a pair of powerful ventral bristles (setae) that are used in burrowing.  At the posterior end are two incomplete rings of smaller setae, interrupted ventrally, that are used in cleansing the burrow.  The setae resemble those of annelids: each seta is formed by the secretion of a single basal cell; and when an old worm seta is discarded, its place is taken by a new one derived from a reserve follicle.  Muscles corresponding to the protractors of an oligochaete annelid move the seta forward, backward and sideways; other muscles, including an interbasal one, move the two ventral setae apart.
  Body Wall.—The skin consists of a simple columnar epithelium that, except on the ciliated regions of the prostomium, secretes a thin cuticle.  The subepidermal connective tissue layer contains yellow and red pigment cells.  The muscular coat consists of three layers: the strongly developed longitudinal layer lies between outer circular and inner oblique layers.  A thin membrane, the peritoneum, separates the body wall from the spacious coelom or true body cavity (see below).
  Internal Features.Body Cavities.—The cavity of the prostomium is a system of canals and lacunae that are separated from the coelom by an incomplete partition, the diaphragm.  These cavities are provided with an endothelial lining, and coelomic fluid moves freely between the two compartments.  It has been shown that the prostomial cavity is derived from the embryonic blastocoele that develops a secondary connection with the coelom.  Because of this unusual embryonic development F. Baltzer has likened the body of an echiurid to a chimera in which the anterior part is larval and the posterior part adult.
  Coelomic Fluid.—The coelomic fluid contains two types of cells, spherical erythrocytes, which in the Californian species Urechis caupo contain a respiratory pigment similar to hemoglobin; and amoeboid leucocytes, often laden with red-brown pigment granules.  In all but the youngest individuals, maturing sex cells are also found in coelomic fluid.  The coelomic fluid performs respiratory as well as nutritive and excretory functions.  Respiratory exchanges take place in part through the skin, since the worm keeps up a constant flow of water through the burrow by peristaltic contractions of the body.  Water is also taken into the anal vesicles and expelled periodically.  According to A. C. Redfield and M. Florkin (1931), the properties of Urechis hemoglobin are such that it gives up oxygen at low tensions when the worm is confined to its burrow at low tide.  This "oxygen resevoir function" is criticized by E. Eliassen (1954), who favours the "low tension transport" function (see also ANNELIDA: Introduction).
  The coelomic fluid of Echiurus is isotonic with the sea water in which it lives and contains no plasma proteins in solution.
  Digestive System.—The mouth communicates with the pharynx, which makes a double loop in the region of the diaphragm; a thick-walled esophagus is dilated posteriorly to form a crop in which the food bolus is molded.  These parts, constituting the fore-gut, are of ectodermal origin.  The endodermal mid-gut, separated from the fore-gut by a sphincter, is divided into three regions, the pre-, mid- and postintestine.  The midintestine is accompanied by a narrower accessory tube, which is continuous before and behind with an open ciliated groove.  This accessory tube or siphon is of unkown function and, although similar structures occur in unrelated groups, as for example among polychaetes (Capitellidae) and in sea urchins, its presence is considered to be one of the more distinctive features of the Echiurida.  The postintestine opens into a short anal tube, also of endodermal origin.  Both mid- and postintestine are strongly coiled and convoluted.  The intestinal juice is alkaline and contains a powerful protein-digesting enzyme.  A fat-splitting enzyme is also present, but evidence for a starch-digesting one is inconclusive.
  Excretory Organs.—The anal tube recieves a pair of endodermal sacs; in the newly meteamorphosed larva these sacs communicate with the coelom, each by a single funnel, the nephrostome; in the adult the number of nephrostomes is greatly increased.  The anal vesicles are highly characteristic of the phylum.  They subserve both excretory and respiratory functions and, since they are provided with typical nephrostomes, they probably represent a posterior pair of metanephridia.
  Vascular System.—The vascular system is closed; a ventral vessel runs the whole length of the trunk above the nerve cord and forks anteriorly to form a ring around the margin of the prostomium.  A short dorsal vessel, confined to the anterior part of the body, receives blood from the ventral vessel by way of a sinus surrounding the mid-gut.  It pumps the blood forward into a median prostomial vessel that communicates anteriorly via the marginal loop with the ventra vessel.  The blood is colourless and contains only phagocytic amoebocytes.
  Nervous System.—There is a ventral nerve cord in which, in the adult, no separate ganglia can be recognized.  It divides anteriorly, and the circumpharyngeal connectives form a long drawn-out loop that follows the margin of the prostomium.  There are no special enlargements or cerebral ganglia.  The ventral nerve cord arises embryonically by the union of two ectodermal thickenings and, in Echiurus, exhibits 16 transitory ganglionic masses.  In Urechis the number of these supposedly primary trunk ganglia is only 12.
  Sense Organs.—Groups of sensory cells, which may be either tactile organs or chemoreceptors, underlie the epidermis and are especially abundant along the margins of the prostomium.  Special sense organs are lacking in the adult, but eyespots are present in the larva.


  Reproduction.—In Echiurus the sexes are separate but superficially alike.  The gonad is suspended from the ventral vessel, and the maturing sex products are shed into the coelom.  The naked eggs grow from 0.01 to 0.2 mm. in diameter, nourished by the coelomic fluid, and are then taken up by the ciliated funnels of the storage organs.  In some genera, like Bonellia, the developing ovum is enclosed in a follicle and nutrition is mediated by a special cap of nurse cells.  In males the sperm clusters also develop in the body cavity and the liberated spermatozoa are collected as they become mature and free-swimming.
  There are two pairs of gonoducts that act as storage organs.  They are regarded as modified metanephridia and although they perform no excretory function, are confusingly termed "nephridia" by some authors.  Each of these ducts is provided with a bilobed ciliated funnel that gathers up the mature sex cells, and a large thin-walled sac that serves as a storage chamber.  In Echiurus the funnel opens into the gonoduct close to its external end, but the presumably more primitive condition in which the funnel is at the internal end of the sac occurs in some other genera (see below).
  Development.—The most complete study of echiurid development is that of W. W. Newby on Urechis.  Fertilization is external and the early stages show a spiral cleavage similar to the of Platyhelminthes, Mollusca and Annelida.  A typical "annelidan cross" is formed from the first four cells, the first quartet, but the later stages show a predominance of supposedly molluscan features.  Thus the blastopore, pushed forward ventrally by the expansion of the somatic plate, forms only the mouth.  In typical annelids the somatic plate, as it grows downward on each side, unites ventrally to divide the blastosphere into a mouth-forming and an anus-forming region.  Mesoblastic teloblasts are absent in the better known European and North American species. Growth in length is achieved by expansion of the trunk region and not by the teloblastic addition of segments at the posterior end, as in the Annelida.  However, C. N. Dawydoff described the appearance of two teloblasts and a transient metamerism in the giant larva of an unidentified echiurid from Annam.  The body cavity is a schizocoele, that is, formed by splitting of the mesoblast into layers.
  The embryo develops into a free-swimming trochopore of the annelidan type, provided with a pair of larval protnephridia.
  Sex Determination in Bonellia.—Zoologists have long been interested in this problem and many outstanding contributions have been made, especially by Baltzer and C. Herbst.  The trochophore becomes transformed into an indifferent larva.  If it finds the prostomium of a female it becomes attached and remains for several days (B. viridis) during which period a gradual metamorphosis toward the male condition takes place.  It then migrates to the fore-gut and thence to the antechamber of the female storage organ, where it remains for at least one breeding season.  On the other hand, larvae that develop in sea water usually become females.  However, the presence of female extracts, from the fore-gut or prostomium, will stimulate male transformation.  The active principle, which resists boiling and is probably not a protein, has not been identified.  Moreover, a diversity of foreign agents such as acids, potassium ions, heavy metals, glycerine and even shaking or transference from Mediterranean to North sea water, have been shown to induce masculinity.
  The simple facts, outlined above, appear to justify the view that all larvae are potentially bisexual and that the male response is elicited by a variety of different stimuli and is therefore, fundamentally, a response to an irritant.  The investigations of Baltzer have shown that when larvae are removed prematurely from the female prostomium they exhibit various stages of male transformation.  The degree of intersexuality is approximately correlated with the duration of the attachment period, but, since extracts also elicit a graded series of transitional types, it appears probable that organs in the mouth region have a lower threshold toward the male-inducing substance than have those situated more posteriorly.  Baltzer advanced the view that male transformation is essentially an inhibition.  The stimulating action of potassium ions led Herbst to suggest, in view of the known effect of the ions in increasing cellular permeability, that an increased water uptake might be a masculinizing agent, and this hypothesis received support from the experimentally proved antagonistic action of calcium ions.  Later Herbst suggested that glycerine derived from the metabolism of fat in the larval gut must play some role.  R. Goldschmidt attempted to bring the facts in line with his famous theory of sex determination, and M. Hartmann pointed out similarites with the phenomenon of sex reversal in the polychaete Ophrytrocha.  The theory that all eggs are potentially bisexual has been challenged by J. Z. Wilczynski (1960).


  The Echiurida is a small phylum, with over 30 genera and about 80 species.  Several systems of classification have been proposed; that adopted below is essentially identical with that of Dawydoff (1959):

  Echiuridae.—As now restricted, this family comprises the single genus Echiurus, described above.
  Urechidae.—W. K. Fisher placed the genus Urechis in a separate order, Xenopneusta, on account of the absence of a vascular system.  There is only one ring of anal setae.  The small prostomium is not used as a feeding organ; food is captured by means of a finely netted slime tube, secreted periodically by a glandular girdle, that filters the water as it is swept through the burrow by peristaltic contractions of the body.  The slime tube, together with its catch, is then eaten.  It has been estimated that the net must have a mesh with pores of 36 to 40 Ångstrom (Å) units (Å = 1/10,000,000 mm.), since molecules of ovalbumin can pass through, whereas those of serum globulin are partly retained and those of hemocynin completely retained.  Another peculiar feature of Urechidae is the absence of a definitive gonad; the sex cells are found free in the coelomic fluid from their earliest identifiable stage.  There are two or three pairs of gonoducts with external funnels in which the lips are drawn out into spirally twisted, whiplike processes.
  Thalassematidae.—Members of this predominantly tropical and subtropical family were separated from the Echiuridae by S. Bock on account of the absence of anal setae.  There are seven genera, comprising some 50 species.  Some thalassematids inhabit shells of sea urchins or sand dollars.  Thalassema dendrorhynchus, from Chilka lake, a brackish bay on the northeastern coast of India, is tolerant of low salinities; both this species and a related one have gill-like processes on the margins of the prostomium.  Anelassorhynchus abyssalis has been taken at a depth of 1,083 fathoms off the coast of California.  A presumably primitive metameric arrangement of the gonoducts is found in some species of Ochetostoma, with three to five pairs in sequence.  More usually the number is restricted to one or two pairs.  On the other hand Ikedosoma has 6 to 14 pairs, some of which are represented by groups of organs, reflecting a local, nonmetameric multiplication of the embryonic rudiment.
  Ikedidae.—Fisher placed the remarkable Japanese species Ikeda taenioides, which attains a length of over one metre, in a separate order Heteromyota because, unlike the arrangement in other echiurids, the longitudinal muscle layer is external to the circular layer.  The excessively long prostomium is readily discarded, and this part was formerly mistaken for a nemertean worm.  The trend to multiplication of the gonoducts, noted above in the thalassematid Ikedosoma, has advanced so far in Ikeda, with 200 to 400 organs, that all traces of metameric paring are obliterated.  The funnels are situated at the internal end—a primitive feature.
  Bonellidae.—This interesting family, with over 20 genera, is characterized by a pronounced sexual dimorphism.  Females are typical echiurids, distinguished primarily by the structure of the excretory organs: the nephrostomes are not sessile, but communicate with the anal vesicles, or rarely communicate directly with the cloaca by slender tubules.  The prostomium is usually long and ribbonlike, but in Nellobia it is short and truncated; frequently it is deeply cleft or forked, as in Bonellia.  In Prometor the margins of the prostomium unite to form a cuplike funnel at the base.  There are usually two ventral setae, but they are lacking in some genera; anal seta are absent.  Acanthobonellia has two clusters of small ventral setae on muscular pads.  In Acanthohamingia minute ventral spinelets, without musculature, are situated in the genital groove (see below).  There may be a single gonoduct, as in Bonellia, but more frequently the primitive paired condition prevails.  The funnel may be apical or basal.  Archibonellia retains a pair of supposedly larval metanephridia, and Australobonellia has a single such organ between the gonoducts.  The siphon, rudimentary in Achaetobonellia, is said to be absent in Sluiterina.  The majority of species are of an intense green colour; the pigment, known as bonelline, is a mesopyrrhochlorine, chemically a degradation product of chlorophyll.  It is highly toxic to other organisms and may therefore have a protective function; the green tissues are usually rejected by predators.  The lytic properties of bonelline solutions toward echinoderm larvae are enhanced by simultaneous exposure to light; it may be, for this reason, that Bonellia, which avoids light and is nocturnal, cannot tolerate appreciable illumination.
  In the late 1950s specimens of four hitherto undescribed genera were recovered from Pacific deeps by a Soviet expedition; among these are Votjazema, taken at 5,500-9,950 metres.
  The males are usually minute, 1-3 mm. in length, and live as parasites upon or within the body of the female.  Immature stages may be found developing in the fore-gut, on the prostomium or attached to the skin.  Mature males of Bonellia migrate into the muscular antechamber of the gonoduct; in Achaetobonellia this region forms a thick-walled bulbous expansion.  The androecium, or male tube, of Pseudobonellia is situated between the genital pores.  Males of Amalosoma are found in an androecial groove in front of the genital openings; in Acanthohamingia this groove is set with setae.  A relatively large male of Acanthobonellia miyajimai, 28.5 mm. in length, was found by I. Ikeda (1907) in the body cavity of the female.  Except in the possession of functional reproductive organs, the dwarf males present a combination of degenerate and persistent larval characteristics.  Setae may be present or absent.  There is no prostomium and the mid-gut is closed at both ends (Bonellia) or degenerate (Acanthobonellia).  The single collecting funnel of Bonellia opens into the blind fore-gut that functions as a sperm resevoir and spermatozoa are discharged through the mouth.  The vas deferens of Acanthobonellia has four funnels.  The excretory organs are a pair of larval metanephridia.
  Doubtful Genera.—Two genera formerly placed among the Echiurida are now definitely excluded.  Sternaspis is a polychaete, and "Epithetosoma" a nemertean of the genus Micrura.  Poeobius meseres regarded by its discoverer, H. Heath, as a connecting link between Echiurida and Annelida, is clearly an aberrant polychaete.  Sactosoma (=Saccosoma), placed by Fisher in the echiurid class Sactosomida, has not been seen since its original discovery and is of uncertain status.  It is said to possess one pair of gonoducts but to lack prostomium, setae, anal vesicles and blood vessels.
  Relationships.—The Echiurida have many features in common with the Annelida.  Distinctive features of the group are the apparent lack of segmentation and the persistent "larval" anterior end that forms the proboscislike prostomium.  It is by no means certain that the lack of segmentation is primary, although W. W. Newby favoured this view.  Evidence of supressed segmentation may be derived from the appearance of transitory ganglia in the ventral nerve cord, from the varying number of setal groups and from a metameric interpretation of the gonoducts and excretory organs.  Molluscan features are evident in early development and for this reason it is difficult to regard the Echiurida as a degenerate class of the Annelida.
  Molluscan affinities have also been suggested for the Sipunculida, another unsegmented phylum remotely related to the Annelida but widely different from the Echiurida.  Echiurids are clearly more primitive, as shown by the half-larval character of their body, and more annelidian than the sipunculids, as shown by the possession of setae and by the terminal position of the anus.
  Relationships with the Priapulida are extremely doubtful since the body cavity of the latter is probably a pseudocoele.
BIBLIOGRAPHY.—F. Baltzer in Kukenthal and Krumbach's Handbuch der Zoologie, Bd. 2, Heft 2 (1931) ;  C. N. Dawydoff, "Classe des Echiuriens," in P. P. Grassé's Traité de Zoologie, tome 5, fasc. 1 (1959) ;  J. Z. Wilczynski, "On Egg Dimorphism and Sex Determination in Bonellia viridis R., J. Exp. Zool., 143 (1), pp. 61-75 (1960).

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