Hemichordata: Pterobranchs (C: Pterobranchia)

Classification

Pterobranchs (lit. 'feather-arms') are small hemichordates. They may possess gill slits and have 2 or more
tentaculated arms borne by the mesosome. The digestive tract is recurved. They live in
colonies housed in an
externally secreted encasement. There are three genera:
Cephalodiscus, Rhabdopleura and Atubaria and
about 15 species.

Cephalodiscus

Coenecium

Unconnected individuals arise by budding from a single progenitor in a secreted encasement or coenecium,
which also incorporates adherent foreign objects like spicules, bits of shells and tubes, etc.

The
orthoecus type of coenecium, found for example in Cephalodiscus densus, consists of upright tubes,
each of which is occupied by an individual zooid. The coenecium is permanently fixed to the substrate and the
tubes are more or less adherent to each other, especially basally.

The
Idiothecia type of coenecium, as found for example in Coenecium nigrescens, is branching or
arborescent. Small projections open at the tips to single tubular cavities housing the individuals.

The third type of coenecium is the
Demiothecia type. This may be adorned by filamentous projections that
give it a seaweed appearance. Spines (spicules) may support the projections.

Coenecia are often a drab yellowish-brown colour, but some are orange, red or brown.

External Features

The zooids consist of a body, usually < 5 mm long, but up to 14 mm in length and a stalk up to 4 cm long. The
body is plump and bears feathery arms on the dorsal side of the neck. The long attachment stalk gives off buds
near its distal end.

The
protosome forms the buccal shield or cephalic shield. The cephalic shield is flat and discoid or disciform
and tilted towards the ventral side concealing the mouth. The shield is equipped with lateral indentations
(notches) connected by a curved red pigment band. The shield continues dorsally with the collar or mesosome
(no stalk connects the two). The collar is longer dorsally than ventrally and so is curved.

The dorsal
collar (mesosome) bears the arms. The collar has bilateral rows of 5-9 arms each. The arms within
each row are fused basally. The arms consist of a stem bearing a ventral groove and a fringe of 25-50 tentacles
on each side. Each tentacle may terminate in a glandular knob. The number of tentacles is variable and may
increase with age. The oral lamella is a fold of the body wall that partly encircles the collar and extends from the
base of the most posterior arms around to the ventral side below the mouth. This lamella directs the food caught
by the arms to the mouth.

The trunk or
metasome consists of an anterior sacciform, plump region that contains the recurved digestive
tract and the gonads and a posterior
stalk. The trunk bears the anus and 2 dorsal gonopores near to the
collar. There is a single pair of
gill slits situated laterally on the trunk behind the posterior border of the collar.
The stalk is hollow and muscular and extends from the rear end.
Body Wall

The epidermis is ciliated, especially on the ventral surface, on the grooved surface of the arms and tentacles,
on the oral lamella and on the dorsal trunk sac near the anus. The epidermis is also glandular, especially on
the central part of the ventral cephalic shield, which is possibly responsible for secreting the coenecium. The
dorsal arm and tentacle surfaces and the trunk sac epidermis are also glandular. The terminal knobs, found on
the ends of the arms of some species, are involved in prey capture and possibly produce a sticky secretion for
this purpose. Attachment of the zooid to the coenecium is possibly by glandular secretion or a vacuum cup.

There is an
intraepidermal nerve plexus, as in enteropneusts. Beneath the epidermis is a strong supporting
basement membrane. Beneath this there are
subepidermal longitudinal muscle fibres. The peritoneum is
partially transformed into muscle and connective tissue, but remains intact in places.

Nervous System

There is an intraepidermal nerve plexus in pterobranchs. There is also an intraepidermal collar ganglion
in the dorsal wall of the collar between the bases of the arm rows. This ganglion is a plexus thickening. It gives
out nerves that are really plexus thickenings. It gives out an
arm nerve to each arm, which course along the
dorsal side of each arm, and median dorsal and paired
laterodorsal nerves in the cephalic shield and a short
middorsal nerve to the anus region.

The ganglion also gives out a pair of circumenteric connectives that course ventrally approximately along the
collar-trunk boundary behind the gill pores to the ventral side of the trunk sac where they form a midventral
trunk nerve. This midventral nerve gives out one or two pairs of lateral trunk nerves. The midventral and lateral
trunk nerves continue into the ventral side of the stalk. The midventral nerve of the stalk may turn around at the
end of the stalk and continue to run forward dorsally.

Coelom

There is an unpaired protocoel in the shield that opens to the outside via one pair of ciliated canals and
pores. The
mesocoel (collar coelom) and the metacoel (trunk coelom) are each subdivided by a median
dorsoventral mesentery and so both are paired. A septum separates the protocoel from the mesocoel.

The dorsal mesentery is a site for muscle attachment. The arms and tentacles are hollow and contain
extensions of the collar coelom or mesocoel. There is a ciliated collar canal and pore for each mesocoel half
just in front of the gill pores on the neck. A septum separates the mesocoel from the metacoel. Such septa give
each compartment of the fluid-filled coelom some functional individuality when functioning as a hydrostatic
skeleton.

The metacoel or trunk coelom is almost filled by the digestive tract and gonads. It extends into the stalk (where
there is no mesentery) where its lumen is almost filled by muscles and connective tissue.

Musculature

There is a subepidermal thin longitudinal muscle layer, which is possibly of peritoneal origin. This layer is
lacking in the muscular ventral part of the shield. Fibres radiate through the protocoel from the shield-collar
septum to the ventral wall of the shield (and some also extending to the dorsal wall).

The oral musculature in the collar can narrow the mouth and buccal tube, but the mouth is closed by bringing
the cephalic shield against it. Strong longitudinal fibres can contract the trunk and stalk. These extend into the
trunk sac as one pair of ventral bundles that extend to the gill region. Strong muscle bundles extend from the
collar canal to the adjacent body wall. All or most of the muscle is smooth muscle. The muscles attach to the
septa, basement membrane and the mesenteries which provide skeletal support.
Digestive System

The mouth is transversely elongated and more or less concealed by the cephalic shield. The upper and lower
lips are formed of thickened epidermis.

The
buccal tube contains mucous gland cells and a buccal diverticulum hangs from the buccal roof forming a
tubular evagination that extends forward along the shield-collar septum. The dorsal collar mesentery attaches
the diverticulum to the dorsal epidermis.

The buccal tube continues as the
pharynx. The pharynx passes through the collar-trunk septum. The pharynx
contains gill passages in its dorsolateral walls. There are no tongue bars and no branchial skeletal supports for
the gills.

The pharynx continues into the
oesophagous that connects to the stomach. The stomach is sac-like and fills
the greater part of the trunk sac. The stomach connects to the tubular intestine that curves dorsally forward to
the anus, with its ventral wall in contact with the stomach. The intestine leads into a
rectum expansion that
opens via the
anus. The anus is transversely elongated (i.e. elongated from side-to-side) and situated on the
dorsal surface of the anterior trunk sac.

Circulatory System

The structure of the circulatory system is not well known. It is wholly lacunar (made up of blood spaces rather
than vessels). A
dorsal sinus (a sinus is a blood-filled cavity) originates from lacunae in the stomach wall and
runs forward above the oesophagous and pharynx and connects to sinuses around each gonad, then
continues beneath the collar ganglion and terminates in the
central sinus. The central sinus is associated with
a
contractile heart vesicle.

The central sinus gives out the
ventral shield sinus that runs back beneath the buccal tube and buccal
diverticulum as a pair of
peribuccal channels or a lacunae system. From these peribuccal channels or
lacunae originate the main
ventral sinus. This sinus extends posteriorly from the collar-trunk septum along the
ventral side of the stalk and then turns dorsally at the end of the stalk and continues forward along the dorsal
side of the stalk and along the dorsal side of the intestine where it disappears. In
enteropneusts the heart
vesicle and central sinus are positioned above the buccal diverticulum, whilst in
Cephalodiscus they are
positioned in front of the buccal diverticulum.

Glomerulus

The glomerulus is the much-folded wall of the ventral shield sinus where it passes beneath the buccal
diverticulum. These folds are surrounded by altered peritoneal cells that are possibly excretory. It is thought
that these cells may detach and be emitted through the canals and pores of the cephalic shield and collar.
Reproduction

Cephalodiscus are dioecious (the sexes are separate) and the sexes are not distinguishable externally, except
in
Cephalodiscus hodgsoni in which the female is red and has 12 arms while the male is brown and has 10-11
arms. The coenecium may be of one sex or a mixture of both sexes. Hermaphrodite individuals often occur with
one male and one female gonad.

In
Cephalodiscus sibogae one coenecium was found with neuter and male zooids and no females. The neuters
had 4 pairs of tentaculate arms and lacked gonads. The males had 2 arms and no tentacles and a vestigial
digestive tract, with the space filled by the testes instead.

There is one pair of gonads in the anterodorsal trunk in front of the stomach. These gonads are oval or
sacciform and each opens to the outside by a short gonoduct with the gonopore on the anterodorsal surface
just behind the collar-trunk boundary. The two gonads are separated by the median dorsal trunk mesentery.
Breeding is probably seasonal. In
Cephalodiscus gilchristi the eggs are shed into the coenecium cavities where
they develop.

Development

The eggs are quite large and yolky. Cleavage is holoblastic (the cells completely separate during cytokinesis)
and more or less equal. A
blastula results (hollow or solid?) and subsequent endoderm formation results in an
embryo that is completely ciliated and escapes from the egg. This undergoes a brief swimming period and
possesses an apical sense organ and may have an apical tuft of long cilia.

The larva elongates and resembles a young
enteropneust. The intestine is initially straight but later bends
dorsally (as the dorsal surface shortens) to acquire the adult U-shape. The heart vesicle is possibly of coelomic
origin.

Asexual Reproduction

Buds form from a zone near the distal end of the stalk. There are usually 1-14 buds per zooid at any instant.
These offspring remain in the parent colony. The coenecium is asexually produced from a sexually produced
progenitor. Each bud contains an extension of the stalk coelom. Soon the bud develops a stalk, cephalic shield
with pigment stripe, and then the trunk sac develops proximal to the shield as an enlargement. The arms
appear as buds (hollow extensions of the collar) and the collar becomes delineated from the trunk sac. The
heart vesicle develops from part of the protocoel and gills, buccal diverticulum, and coelomic canals and pores
form.
Ecology and Behaviour

The stalk stretches and the zooids reach out of the coenecium openings and wind about the coenecial
projections, using their adhesive cephalic shield as a holdfast. Alternatively the zooids emerge totally and hold
on by the shields of their buds.

The arms are adhesive and presumably capture minute organisms and particles. These particles are conveyed
along the arm grooves, by ciliary action, to the oral lamella and then to the mouth. This is a form of
filter-feeding.

Coenecia grow on muddy, sandy, gravelly or rocky bottoms and sometimes on other sessile animals. Hydroids
and bryozoans may grow on the coenecia. Sporozoan parasites have been found in the intraepidermal nervous
layer and copepod parasites have been found in the stomach.
Cephalodiscus occurs from 50 m to 650 m in
depth. Most species are Subantarctic and Antarctic.
Atubaria

Atubaria is found at 200-300 m and lacks a coenecium. The stalk twines about larger hydroids. The anatomy is
very similar to
Cephalodiscus. There are 8 tentaculated arms borne on the collar. There is a cephalic shield
with a red pigment stripe. The trunk sac is plump and the stalk is long, flexible and muscular. The 2nd pair of
arms have long and rodlike distal parts devoid of tentacles and of a glandular nature. The stalk has no
adhesive tip. There is one pair of gill slits and the anus is more posterior than in
Cephalodiscus. Other internal
structures are the same as in
Cephalodiscus. Juveniles bear only two arms and have no tentacles. There is
some evidence of budding.
Rhabdopleura

Coenecium

The rhabdopleuran coenecium is a pale brown prostrate branching tube partitioned into chambers and
cemented to the substratum. It gives off short erect tubes at frequent intervals, each of which houses a zooid.
The coenecium usually grows on hard surfaces, such as rocks, shells, bryozoans, and tunicates, etc, but can
grow on sandy bottoms. The maximum colony diameter is 10 cm. The coenecium is formed by budding from a
single progenitor and the branch ends continue new growth.

The prostrate tube is flattened on the side in contact with the substrate. They may incorporate foreign
particles. The erect tubes are cylindroid, clean, translucent and 6-7 mm tall. The coenecium walls are secreted
by the glandular centre of the cephalic shield and is of an unknown non-chitinous chemical nature.

The black stolon is a black cord embedded in the attached wall of the creeping tube. It gives off a branch to the
base of each zooid at each transverse partition. It consists of a hard black hull enclosing living vacuolated
tissue with a central denser syncytial core that connects the zooids and terminates as a knob in the zooid stalk
coelom. The periphery of the living stolon is separated from the zooid by up to 10 partitions in each side
branch.

The progenitor secretes a hemisphere encircled by a ring tube enclosing the ring-shaped black stolon. A
creeping prostrate tube grows from this hemisphere. The stolon gives off buds into each transversely
partitioned chamber.
External Features of Zooids

The zooids resemble Cephalodiscus and are small, being less than about 1 mm long excluding the stalk. They
are dark brown in colour. They have a cephalic shield, a collar bearing one pair of tentaculated arms or
plumes. The cephalic shield has a pigment stripe but no lateral notches.

When the zooid is extended the arms are held curved backwards, but when in its tube the arms are held
straight forward.

There is a marked asymmetry in favour of the right side. The right fold of the oral lamella is larger than the left.
The anus is dorsal and just behind the arm bases on the right side. There is a single gonopore on the right
dorsal surface just in front of the anus. The stalk attaches to a branch of the black stolon.

Internal Structure

The internal structure of Rhabdopleura is similar to that of Cephalodiscus. The epidermis is ciliated, especially
on the tentacles, ventral sides of the arms and the groove of the oral lamella. The cephalic shield is similar to
that of
Cephalodiscus. The protocoel has one pair of canals with external pores just anterior to the arm bases.
The collar has a pair of coelomic cavities continuous with the arm coeloms and oral lamella. There are the
usual collar canals and pores, though the pores are very minute.

The circulatory, nervous and digestive systems are very similar to those of
Cephalodiscus. There is one pair
of gill pouches or dorsolateral pharyngeal grooves with no external pores. There is a subepidermal
longitudinal muscle layer, but this is very weakly developed. The stalk is well muscled and possesses two
ventral longitudinal muscle bands that connect to the dorsal arm musculature and the mouth and buccal
musculature. There is glomerular tissue around the central sinus and the ventral shield sinus.

Reproduction

Most of the Rhabdopleura colonies found have been sterile. Some, however, have been found with male or
female zooids. In those with male zooids, about ⅓ of the zooids are male, the rest neuter. Females are very
scarce.

A single gonad in the right metacoel opens via a short duct and gonopore to the right of and behind the anus.
The testis is elongated with the proximal portion producing sperm and the distal portion forming a seminal
vesicle for storage of ripe sperm. The ovary is rounded and contains only one very large yolky egg at any one
time.

The eggs are discharged to the exterior and have been found adhered to the arms. Embryonic development is
not known (check this for updates). Only the actively growing stolon ends bud. These young stolons consist of
epidermis enclosing a pair of coelomic cavities lined by peritoneum and separated by a median mesentery.
Older stolons secrete a wall around themselves, which turns black and the coelomic cavities are lost.

Black stolons can not bud but are possibly able to regenerate. Some buds are sterile and do not develop, but
remain encapsulated in the hull. These are possibly dormant buds, since they are common in autumn and may
represent an overwintering stage. Zooids may degenerate from the arms basally and regenerate again from
the stalk, from a new regeneration bud.

Ecology and Behaviour

Stalk contraction withdraws the zooid into its tube, as a protective response. Extension from the tube is very
slow and achieved by application of the cephalic shield to the tube wall.

At least some rhabdopleurans prefer temperatures in the range of 5-10 oC and survival at 12 oC is reduced to
days. There is no apparent response to light. Diatoms, radiolarians and crustacean larvae have been found in
the stomach.
Rhabdopleura is found from 2 to 550 m depth.
Hemichordates - Pterobranchs
A computer model of a Cephalodiscus (lit. 'disc-head') zooid (size in life about 5 mm + stalk). The back
of the neck or collar bears a crown of tentacled arms and the 'head' is the disc-shaped (as seen from
beneath) cephalic shield which conceals the ventral mouth and gives the animal its name. Asexual
buds branch from the stalk. Notice the red pigment stripe on the underside of the cephalic shield. The
back of the cephalic shield is continuous with the trunk (there is no stalk connecting the two). The gut,
coloured orange-brown includes the sac-like stomach and the intestine which arches above the
stomach and opens in the anus just behind the cephalic shield on the back. there is one pair of
gonads (shown in yellow) one either side of the gut in front of the stomach.
Enteropneusts - the acorn worms are also hemichordates.