Hemichordates - Acorn worms
A computer model of an acorn worm (enteropneust) with realistic colouration. Acorn worms belong to the
hemichordates, along with the bizarre
Cephalodiscus. These invertebrates have some of the features of
chordates (a group of animals including vertebrates like human beings) in particular pharyngeal gill slits -
slits or pores in the body wall and pharynx that connect the outside to the lumen of the pharynx (foregut).
The body consists of 3 main regions: the anterior proboscis, the collar and the trunk. The trunk has a
ventral groove formed by wing-like extensions of the body wall (the genital wings) which arch over but do
not meet, leaving a groove. There is a dorsal ridge along the back and a ventral ridge inside the ventral
groove. In the front branchial region of the trunk gill slits/pores can be seen either side of the ventral
ridge. Further back are the hepatic sacculations (green in this case).
Hemichordata: Enteropneusta (Acorn Worms)

External Features

The acorn worms are solitary cylindroid worms with numerous gill slits, but no tentaculated arms. Length
varies from several cm to over 2 m, for example,
Saccoglossus pygmaeus is 2-3 cm, while Balanoglossus
gigas
is 1.8 – 2.5 m. Enteropneusts are soft and covered with slime. They have no external appendages
and no exoskeleton. The body is divided into three regions: an anterior proboscis (
protosome), a middle
collar (
mesosome) and a trunk (metasome).

The
proboscis is short, rounded or conical, or elongated in Saccoglossus, and is circular in cross-
section. The proboscis may have a deep middorsal groove and may possess a midventral depression in
its base. The proboscis stalk is more or less concealed by the collar, and is continuous with the inner
dorsal surface of the collar.

The
collar is a short cylinder, usually shorter than the proboscis. The funnellike anterior part forms a
collarette that embraces the proboscis stalk (and sometimes the posterior proboscis). A circular
indentation marks the collar off from the trunk. The mouth is ventral and situated inside the collarette.

The
trunk has a middorsal and a midventral ridge. These accommodate median longitudinal nerves and
blood vessels. The trunk musculature consists of a longitudinal layer beneath the epidermis, which is
usually thicker ventrally and diminishes posteriorly. This muscle layer is very thin or absent on the
hepatic sacculations. Saccoglossus has two thick ventral longitudinal muscle bands, which cause a
spiral twisting of the trunk. There is also a circular muscle layer inside or outside of the longitudinal
muscle layer.

The posterior trunk may possess visible sacculations where the hepatic part of the intestine shows
externally, as in
Balanoglossus and Ptychodera. The anus is terminal. Visible trunk annulations are
formed by annular grooves with low poorly glandular epidermis and high glandular epidermis between the
grooves.

Enteropneusts are usually drab buff coloured, but the proboscis, collar and/or body may be orange or
reddish. The hepatic region is brown. The colours of the ripe gonads may show through the body wall.
Body wall

The external surface consists of a tall, slender, glandular epidermis. The gland cells are classifiable into
mulberry cells containing coarse granules, reticulated cells and goblet cells (secrete mucus). The bases
of each epidermal cell gives rise to a fine fibril that crosses the epidermal nervous layer situated at the
base of the epidermis. These epidermal fibres are continuations of a strong elastic fibre traversing the
cell. The epidermis and the epidermal nervous layer rest upon a basement membrane, comprised of two
lamellae (sheets) pressed together. An additional reticulated membrane may be present between the
main epidermal layer and the basal nervous layer.

The basement membrane is thickened to form the proboscis skeleton in the proboscis stalk. This
consists of a median plate with 2 posterior horns and sometimes a midventral keel. This skeletal plate is
a combination of epidermal and coelomic tissue secretion.

A definite peritoneum (epidermal lining of the coelom, usually ciliated) is only present in
Protoglossus.
Instead the coelomic cavities are mostly filled with connective tissue and muscle fibres.

Nervous System

An intraepidermal nervous layer ('intraepidermal' = 'within the epidermis') occurs in the base of the
epidermis (cf.
Asteroid nerve cords). This nervous layer is thickened to form cords in the middorsal and
midventral grooves of the proboscis. There is an
anterior nerve ring at the proboscis base.

The trunk contains
middorsal and midventral cords, which terminate at the anterior of the trunk. A
circumenteric (prebranchial) nerve ring ('circumenteric' = 'encircling the gut') connects the dorsal
and ventral cords. The dorsal cord extends to the collar, where it leaves the epidermis and runs through
the coelom above the buccal tube as the
collar cord (‘neurocord’). This collar cord is the nervous
centre and develops from an epidermal invagination. The collar cord may have a continuous open
lumen, or else contains numerous small cavities. The collar cord is connected to the exterior at both
ends via anterior and posterior
neuropores, in epidermal depressions. The collar cord is a conduction
path only, contains no cell body concentrations and gives off no nerves and is covered externally by a
basement membrane derived from the epidermis. Ciliated epidermis lines the internal cavities of the
cord. The collar cord contains 10-160 giant cells (large, especially fast-conducting nerve cells).

There is an additional nervous layer in the base of the digestive tract epithelium, with midventral and
middorsal thickenings connected by a ring-like thickening at the entrance to the buccal tube. Nerve
fibres from ventral mesentery plexi supply the blood vessels and muscles.
Sense Organs

Epidermal neurosensory cells are distributed over the epidermis. These are more numerous on the
proboscis, especially at its base. There may be a middorsal organ –presumably sensory - connected via
a strong nervous strand to the middorsal cord of the proboscis.

A
preoral ciliary organ ('preoral' = 'in front of the mouth') is present in some species on the ventral
side of the proboscis at the junction with the stalk, or on the stalk itself. This is a U-shaped epidermal
depression bounded by an epidermal ridge. This is also presumably sensory (check for updates).

Photoreceptors are present as modified neurosensory cells and all parts of the surface are
photosensitive, especially the proboscis and collar. The proboscis is essential for response to light and
an isolated proboscis will exhibit negative phototaxis (movement away from light).

If agitated, acorn worms retreat by reversed postero-anterior peristalsis. If the proboscis is prodded
there is a shortening reflex, accompanied by coiling of the trunk. It has been hypothesised that giant
cells mediate this retreat reflex.

Coelom

The coelomic wall gives rise to muscular and connective tissue (an ontogenetic peculiarity of the group).
The adult coelom is reduced and lacks a definite peritoneal lining. The proboscis coelom is an unpaired
cavity partially divided into 2 ventrolateral chambers and 2 dorsolateral chambers. The left dorsolateral
chamber is generally larger than the right. The right is usually blind and the left opens to the dorsal
surface via a proboscis canal and proboscis pore in an epidermal invagination. This pore may be
medial. In other species the right chamber opens in a pore whilst the left is blind, or both may open via
two pores. There is a sphincter muscle at the junction of the proboscis canal and coelomic sac.

In
Protoglossus there is a pair of collar coelomic sacs, but in other genera these are reduced or absent.
These continue anteriorly into the proboscis stalk. The proboscis stalk and the ventrolateral proboscis
coelomic chambers secrete
chondroid tissue around the proboscis skeleton. The collar coeloms may
open via a pair of collar canals and collar pores. A transverse collar-trunk septum separates the collar
and trunk coeloms.

The trunk coelom is paired, giving rise to dorsal and ventral
mesenteries above and below the
digestive tract. The dorsal mesentery is usually perforated, allowing the two trunk coeloms to
communicate directly. The trunk coeloms do not open via external pores, but are closed. In the trunk,
coelomic fluid derived from the peritoneum contains amoeboid
coelomocytes.

Musculature

The muscles are of coelomic origin and course through the coelomic spaces and the inner surface of
the epidermis. The fibres are of the smooth muscle type. Circular fibres occur beneath the epidermal
membrane in the proboscis. Longitudinal fibres almost fill the proboscis interior (coelom), but connective
tissue fills the proboscis centre. Dorsoventral fibres (extending from the back to the front body walls)
attach to the median sagittal skeletal plate in the posterior proboscis. The other proboscis fibres attach
to the epidermal basement membrane. The collar musculature is highly variable and the subepidermal
musculature is generally poorly developed here.

Nutrition

The digestive tract consists of a straight epithelial tube with little or no intrinsic musculature. There are
no longitudinal muscle fibres in the gut wall. Circular muscle fibres may be present around the branchial
and oesophageal regions. Radial fibres cross the trunk coelom between the digestive tube and the
trunk wall.

The large
mouth is situated in the ventral collar, between the collarette and the proboscis stalk. This
opens into the
buccal tube (pharynx) occupying the centre of the collar interior. This has a glandular,
ciliated luminal epithelium, with a basal nervous layer. The buccal tube leads into the
oesophagus,
which leads into the
anterior intestine in the hepatic region. The intestine luminal surface is ciliated.
Oesophageal canals may be present, opening to the exterior by pores. These are dorsal paired
structures. The canal may be supported by skeletal elements. One to 15 pairs of canals and pores are
present. There may also be as many as 60 unpaired or paired irregular pores (aborted gill slits?). The
anterior intestine leads into the
hind intestine, which may form a distinct rectum. The rectum or hind
intestine opens via the terminal
anus, which may be equipped with a sphincter muscle.

The entire luminal epithelium of the digestive tract is ciliated. These cilia move the food cord (food mixed
with mucus) backwards. Burrowers may eat sand or diatoms and protozoans. Some are mucous-ciliary
feeders. Particles touch the proboscis and become entangled in mucus and the mucous strands are
passed back along the proboscis to the collarette where they are rejected if the animal is not feeding or
else are directed to the mouth by ciliary currents. The
preoral ciliary organ directs some particles into
its grooves and then conveys them to the mouth. These grooves are possibly chemoreceptive. The gill
apparatus maintains a ciliary current entering the mouth and exiting via the gill pores.
Branchial Apparatus

The dorsal pharynx is equipped with gill slits, while the ventral pharynx is digestive (and reduced to a
hypobranchial ridge, a midventral strip, in
Schizocardium). A diverticulum sprouts from the roof of the
buccal cavity, into which it opens, and runs forward to the posterior proboscis. This has been
considered to be a notochord by some zoologists, though this argument seems unconvincing. This
diverticulum bears pairs of ventrolateral pockets or sacculations and may continue forward into the
proboscis as an anterior appendix.

There are two longitudinal dorsal rows of gill slits either side of the middorsal strip / epibranchial ridge.
The gill slits open into
branchial sacs, which in turn open to the outside via gill pores. Each branchial
sac is partially divided by a
U-shaped tongue bar, which contains a hollow coelomic cavity. The bars of
the U point towards the middorsal line. The gill or branchial region is behind the collar and there is a
longitudinal row of gill pores, either side of the middorsal ridge, which may be mounted in depressions,
or borne on ridges.

In some species the first 2-4 sacs open via a common pore. All the gill pouches on each side of
Stereobalanus canadensis are fused and open by a single longitudinal slit. The gill pores may be
equipped with sphincter muscles. The pore rows may be sunken into branchiogenital grooves (which
also receive the gonopores). There are no gills (i.e. no thin-walled projections from the gill septa)
associated with these ‘gill’ slits and pores. There may be from a few pairs of gill pores to hundreds of
pairs. The number of gill pores may increase with age as new ones are added posteriorly.

Branchial support. Septa form solid partitions between successive gill slits. The tongue bars never reach
the ventral end of a gill slit.
Skeletal rods (pharyngeal epithelium basement membrane thickenings)
support the tongue bars and the septa. The rods supporting the tongue bars are trifid (3-pronged), with
the median prong in the septum and the 2 lateral prongs in the adjacent tongue bars. The tongue bars
hang freely in the gill slit or are joined to the septa by immovable cross-connections (synapticules).

Haemal System

The blood system is located between the two lamellae of the basement membrane of the body
epithelium or between the two leaves of the mesenteries. There are two main blood vessels, the
dorsal
and ventral longitudinal vessels
. The dorsal vessel is located in the dorsal mesentery below the
dorsal nerve and runs from the anus to the collar where it passes into the
venous sinus that passes
into the
central sinus. The heart vesicle contains no blood, but is muscular and its contractions move
blood in the central sinus into the
glomerulus. The dorsal and ventral longitudinal vessels are lined by
endothelium encircled by a layer of muscle and are contractile.

The central sinus is non-contractile and its endothelial lining is often incomplete. All other parts of the
haemal system are
lacunae or spaces rather than capillaries. The blood is colourless and contains a
few cells, which may be detached endothelial cells. It is thought that the branchial apparatus may aerate
the blood.

The proboscis complex consists of the buccal diverticulum, heart vesicle, central sinus and the
glomerulus, and projects into the coelom of the proboscis base and is coated with peritoneum. The
glomerulus comprises fingerlike out-pushings clothed with peritoneum (see excretion below).

Excretion

It is thought that the glomerulus may function as an excretory organ (check for updates in literature). It
consists of a mass of peritoneal evaginations (simple or branched) with blood-filled interior cavities. The
blood they contain is continuous with that in the central sinus.

Metamerism?

Enteropneusts are not metameric since there is no repetition of the body parts in the three regions.
However, the branchial apparatus and the gonads may show metameric tendencies.
Locomotion

Coordinated beating of the strong trunk cilia, borne on the trunk ridges between the annulations (ring
depressions in the cuticle), and peristaltic movements propel the animal in a crawling/creeping
movement. Mucus coats the burrow and hardens to a smooth surface. Mucus is also used in feeding, to
cover the animal with sand and may have a pungent iodoform odour. The animal is constantly covered
by mucous, which is moved towards the posterior by ciliary action.

Burrowing is achieved by proboscis action. The proboscis extends and contracts in cycles of about 12
per minute. Cilia assist in removing particles from the path. When it gains headway, a peristaltic bulge
anchors the proboscis while the body passively follows. Sometimes enteropneusts take to the surface
and swim in swarms. The proboscis is the most active part of the animal; the rest of the body is sluggish.

The proboscis may effect crawling on the surface, with the aid of cilia and anteroposterior peristalsis of
the body. Movement in the burrow is possibly by cilia action alone. The proboscis exhibits constant
exploratory movements.

Luminescence

Some species of the family Ptychoderidae luminesce. For example, the whole body of Ptychodera flava,
except the branchial region, luminesces bright green. The luminescence of this species is inhibited by
light. It is thought that the luminescence may be due to luminescent slime.

Reproduction

The gonads occupy the lateral regions of the anterior trunk, and may give rise to visible lateral trunk
swellings, or genital ridges, or to genital wings, which are flattened extensions. These wings may be
curved dorsally giving the false impression that the animal has been split dorsally as in
Balanoglossus
and
Ptychodera. There may be 1 to several longitudinal rows to the sides of the digestive tube in the
anterior trunk. These gonads occupy the trunk coelom and are enclosed in a membrane continuous
with the epidermal basement membrane. Each gonad opens via a canal and external pore in the
branchiogenital grooves.

Stereobalanus has four short fluffy genital regions – 2 ventral and 2 dorsal. The gill openings are
concealed in a groove on each side between the dorsal and ventral genital swellings. Thus, thus region
of the body becomes the branchiogenital region. In many species the gonads do not show externally, in
which case the worm trunk is divisible into branchial and postbranchial regions. In those genera with
hepatic sacculations, the body may be divisible into branchiogenital, hepatic and posthepatic/caudal
regions. The caudal region may taper to the anus. The gonopores are small and invisible.

Acorn worms are dioecious (separate sexes) and the sexes are indistinguishable, except for the colour
of the ripe gonads showing through the body wall. An exception to this is
Ptychodera flava, in which the
male has brown flecks on its genital wings. In this species a sex ratio of 1 male to 65 females has been
measured.

In species with direct development the eggs are large (up to 1 mm) and yolky (F. Harrimaniidae). In
those with a tornaria larva stage, the eggs are small and poorly provisioned with yolk. The sperm are
flagellated. In
Saccoglossus horsti a mucous cord with 2000-3000 embedded eggs issues from the
burrow as a coiled mass. About 20 minutes later the males release sperm from their burrows.

Asexual reproduction is known in
Balanoglossus capensis. The juvenile phase (which lacks hepatic
sacculations) cuts off small pieces from its tail end in the summer. These pieces regenerate into sexual
adults, which are found in winter.

Development

Development is either indirect, with a tornaria larva stage or direct. Cleavage is holoblastic (the cells
separate completely during
cytokinesis), approximately equal and mostly radial. After 6-15 h a
coeloblastula results, which forms a blastula after 12-24 h.

Indirect development. Depending upon the species, this blastula gives rise either to a benthonic larva
(after 7 days) or to an embryo that elongates, becomes ciliated, and escapes (after 24-36 h) to a
planktonic life lasting days or weeks. This larva is ciliated, and when ciliated bands differentiate it
becomes a tornaria larva (less than 1 mm to 9 mm long) with an equatorial constriction. Eventually the
ciliated bands disappear and the larva becomes wormlike and benthonic. It may have a prehensile tail
(later resorbed) for anchorage in its burrow. Such a larva may move in its burrow by ciliary gliding or
leechlike crawling, attaching its proboscis, releasing the tail, drawing the body forward, reattaching its
tail and then extending its body forward.

Direct development. This gives rise to a wormlike benthonic larva, usually via a ciliated larval stage that
lasts for about one day.

Regeneration

Acorn worms are fragile and break into pieces when handled. Trunk pieces regenerate. The proboscis
(with or without the collar) can not regenerate, but lives and moves about for some time. Coelomocytes
remove old muscle and connective tissue and new tissue is derived from the coelom.

Ecology

Some acorn worms live in burrows, e.g. Balanoglossus, Saccoglossus, while others live under stones or
in plant tangles, etc. Most are upper littoral or intertidal, but some occur down to 180 m, while Gland.
Abyssicola occurs at 450 m. Burrows are U-shaped, with an anterior funnel and posterior casts on the
surface.

Numerous types of protozoan have been found as parasites in enteropneusts, as have trematodes (in
the coeloms of the proboscis and collar), nematodes (in the proboscis muscles) and copepods. These
copepods are much reduced and wormlike (males are also smaller than the females) and form galls or
tumours on the genital wings. Polychaetes have also been found in the dorsal trough between genital
wings and crabs and amphipods in enteropneust burrows. Some enteropneusts only live in the burrows
of other larger enteropneuists.
Acorn worm
Cross-section of proboscis
cross-section of collar
BT: Buccal tube; LM: Longitudinal muscle; PhS: Perihaemal spaces;
AC: anterior extensions of collar coeloms containing longitudinal muscles; ANR: anterior nerve ring;
BD: buccal diverticulum; CT: chondroid tissue (cartilage-like); DLV: dorsal longitudinal vessel; EGV:
efferent glomerular blood vessels; K: keel of proboscis skeleton; PS: proboscis skeleton, main plate.

Ptych: Ptychodera.

DBV: dorsal blood vessel; DNC: dorsal nerve cord; E: epidermis; G: gonads; GP: gonopore; GW:
genital wings; I: intestine; LS: lateral septum; LML: longitudinal muscle layer; VBV: ventral blood
vessel; VNC: ventral nerve cord.
Pterobranchs like Cephalodiscus are also hemichordates.
The glomerulus consists of blood-filled finger-like evaginations of epithelium that project into the
proboscis coelom.