In this article we will discuss about Balanoglossus:- 1. Derivation of Balanoglossus 2. Geographical Distribution of Balanoglossus 3. Habit and Habitat 4. External Structures 5. Body Wall 6. Supporting Structures 7. Locomotion 8. Coelom 9. Digestive and Respiratory Systems 10. Circulatory System 11. Excretory System 12. Nervous System 13. Reproductive System 14. Development 15. Affinities and Systematic Position.
Contents:
- Derivation of Balanoglossus
- Geographical Distribution of Balanoglossus
- Habit and Habitat of Balanoglossus
- External Structures of Balanoglossus
- Body Wall of Balanoglossus
- Supporting Structures of Balanoglossus
- Locomotion in Balanoglossus
- Coelom in Balanoglossus
- Digestive and Respiratory Systems of Balanoglossus
- Circulatory System of Balanoglossus
- Excretory System of Balanoglossus
- Nervous System of Balanoglossus
- Reproductive System of Balanoglossus
- Development of Balanoglossus
- Affinities and Systematic Position of Balanoglossus
1. Derivation of Balanoglossus:
Balanoglossus is developed from two Greek words, balanos meaning an acorn (fruit of oak) and glossa meaning tongue. Delle Chiaje first recorded the animal from the Naples region in 1829 and gave the name Balanoglossus clavigerus.
Hyman (1959) stated that the balano part does not derive from the Greek balanos, meaning an acorn, in reference to the shape of the proboscis, but from the barnacle genus Balanus, to which Delle Chiaje found some resemblance in his specimens. Delle Chiaje also reported that the animal was called ox- tongue by the local fishermen.
2. Geographical Distribution of Balanoglossus:
Balanoglossus is a marine animal and inhabits all the seas of the world. About 20 species of Balanoglossus have been recorded in the tropical and sub-tropical seas.
Some species are B. carnosus (Indo-Pacific region); B: capensis and B. natalensis (South Africa); B. aurantiacus (Carolina coast, U.S.A.); B. biminiensis, B. jamaicensis (W. Indies); B. apertus, B. gigas (Brazil); B. clavigerus (Italian coasts, British Isles); B. misakiensis; B. borealis(Japan) and B. australiensis (Australia).
3. Habit and Habitat of Balanoglossus:
Balanoglossus is a burrowing animal. It may remain concealed under stones or aquatic weeds. It is mostly an inhabitant of intertidal zone, although a few descend to about 100 m of the sea. Balanoglossus excavates its own burrow in sand or sandy mud. The burrow of Balanoglossus clavigerus is U-shaped with two openings 10 to 20 cm apart (Fig. 2.2).
The anterior end of the burrow is funnel-like and the posterior end is round. The anterior vertical part of the burrow may be branched. The animal moves inside the burrow. When the tide starts ebbing, the proboscis protrudes out of the burrow to explore the surface. The posterior end also projects out to expel the faecal matters.
A constant secretion of mucus over the body causes adhering of sand-grains over the body in the form of a cast. Balanoglossus emits a peculiar odour resembling that of iodoform. This is regarded as a protective device. Balanoglossus is a sluggish animal and the proboscis is the most active part of the body.
Burrowing is exclusively done by the proboscis. The proboscis becomes elongated by the contraction of circular muscles and the shortening of the proboscis is caused by the contraction of its longitudinal muscles. The two sets of antagonistic muscles are so co-ordinated that when one set contracts the other set relaxes, and vice versa.
Balanoglossus is less sensitive in response to external stimuli. It takes sand-containing diatoms, protozoans and many other micro-organisms. The larval form (Tornaria larva) of Balanoglossus is a free- swimming planktonic form which exploits the natural resources of the sea.
4. External Structures of Balanoglossus:
Balanoglossus is an elongated and wormlike animal. The length of the body usually ranges from 10-15 cm. But Balanoglossus aurantiacus of the south eastern coast of the United States attains about 1 meter in length. The largest acorn worm Balanoglossus gigas reaches is more than 2.5 metre in length and ranges from North Carolina, Brazil to Cape Hatteras. It can construct a burrow up to a depth of 75 cm or more.
The body is divisible into three major parts—the proboscis or protosome, collar or mesosome and trunk or metasome (Fig. 2.3A). The trunk is further subdivided into an anterior branchiogenital region, a median hepatic and a posterior caudal or post-hepatic region.
Proboscis:
The proboscis is a short club-shaped structure forming the anterior most division of the body. The proboscis narrows posteriorly to a proboscis stalk. It is hollow and communicates with the exterior by a single proboscis pore situated on the left side of the proboscis.
Collar:
The median part of the body consists of a flap of muscular tissue forming the collar. The proboscis is anterior to the collar. The proboscis stalk and a portion of the posterior part of the proboscis are concealed by the collar. The collar cavity is paired and opens to the exterior by two apertures. The collar houses the mouth on the ventral side (Fig. 2.3B).
Trunk:
The trunk is rather long. The branchiogenital region is marked by a pair of thin flap-like longitudinal genital ridges which contain the gonads (Fig. 2.3C). Double rows of gill-slits or pharyngeal slits are present on the dorsal surface of this region. The gill-slits increase in number as the animal grows older. The gill-slits are placed on a prominent elongated ridge.
Hepatic region:
The hepatic region is externally marked by the sacculations of the intestine. The caudal region is more or less uniform in diameter and is marked externally by annulations. The trunk bears a mid-ventral and a mid-dorsal ridge which contain the longitudinal blood vessels and the longitudinal nerves. The hepatic region tapers posteriorly and terminates into the anus.
5. Body Wall of Balanoglossus:
The body wall is composed of a ciliated epidermis. The ciliated cells are mostly tall and slender. Gland cells are also present in the epidermis.
There are three types of gland cells:
(a) Reticulate gland cells, where the cytoplasm contains mesh-like reticulum;
(b) Mulberry gland cells, having coarse granules and
(c) Coblet cells, which are filled up with fine granules.
The cytoplasm is homogeneous (Fig. 2.4A). The cell body is divided into two parts— a distal flask-shaped expanded portion and a proximal slender stalk. The stalk extends up to the base of the epidermis. The base of the epidermis is occupied by a thick nervous layer.
A very thin connective tissue layer is present between the nervous layer and the epidermis. The nervous layer is separated internally by a well-developed basement membrane. The basement membrane is made up of two lamellae closely applied with one another.
Beneath the basement membrane lies the muscular sheath. The circular muscle fibres are present in the proboscis and in the funnel like anterior end of the collar (collarette). In the trunk region only longitudinal muscle fibres are recognised. The muscle fibres are of smooth variety. The inner side of the body wall is lined with parietal coelomic epithelium.
6. Supporting Structures of Balanoglossus:
Notochord or Buccal Diverticulum or Stomochord:
The so-called ‘notochord’ in Balanoglossus is a questionable structure. The thick- walled anterodorsal hollow prolongation of the buccal cavity (buccal diverticulum) (see Fig. 2.3B) is considered by many workers, specially by Bateson (1885), as the notochord.
It has been named Stomochord by Willey (1899) and later was adopted by Dawydoff (1948), and the recent zoologists like Jollie (1962), Ruppert and Barnes (1994), Kent and Millar (1997) and Kardong (2002) are also in favour to use the term ‘stomochord’ rather than notochord.
The stomochord is an endodermal derivative and is not a supportive structure. It contains a cavity which opens into the pharynx. So it is called stomochord instead of notochord. It extends into the proboscis cavity and is covered over by a sheath of basement membrane.
It is composed of tall vacuolated endodermal cells. But topographically as well as developmentally this structure is quite unlike the true notochord of other chordates. The buccal diverticulum, according to most of the modern workers, is a preoral extension of the buccal cavity.
The structures of stomochord and notochord are not homologous and are presumed to have evolved independently. Current studies using gene expression similarly fail to find homology between stomochord and notochord.
Proboscis Skeleton:
The basal part of the proboscis stalk and the roof of the buccal cavity are supported by a skeletal structure, called proboscis or nuchal skeleton. It is a Y-shaped body and is composed of cartilaginous tissue. It has a median plate with two limbs (horns) diverging backwards (Fig. 2.4B). The proboscis skeleton has a lamellate body and is formed by the thickening of the basement membrane.
The median plate is situated on the proboscis stalk and it occupies a median position between the buccal diverticulum and the buccal epithelium. The median plate bears a mid-ventral keel. The horns diverge posteriorly to support the roof of the buccal cavity.
Branchial Skeletal Rods:
The tongue bars and their septa are supported by skeletal rods. These skeletal rods, like those of proboscis skeleton, are formed by the thickening of the basement membrane. Each skeletal piece has got the appearance of a hairpin.
One prong of the skeleton is present in the septum and the other lies in the tongue (Fig. 2.4C), i.e. each tongue bar and septum get two prongs from two skeletal pieces. The skeletal pieces of the adjacent septa are connected by transverse rods, called synapticulae.
Pygochord:
In the posterior part of the intestine of some Ptychoderidae (e.g., Balanoglossus, Ptychodera), a longitudinal mid-ventral band of cells extends from the intestinal wall to the body wall, called pygochord. It may be solid or hollow, and may contain isolated cavities. The function of this structure is still unknown.
7. Locomotion in Balanoglossus:
Balanoglossus is a sluggish animal and spends most of its time in burrows. The cilia present on the epidermal cells of the body help in locomotion. The animal moves by alternate lengthening and shortening of the body produced by the action of muscle fibres. It moves first by the vigorous forward protrusion of the proboscis and collar and then draws the rest of the body towards the direction of movement by dragging.
The relative position of the buccal diverticulum and the proboscis skeleton make the proboscis and collar stiff. The stiffness of the proboscis and collar helps in burrowing through the sand. Balanoglossus utilizes the cilia for normal movement and the muscles are employed only during emergency escape.
8. Coelom in Balanoglossus:
Balanoglossus possesses a spacious coelom. The coelom is enterocoelous in origin and is lined by coelomic peritoneum. The original cavity of the coelom is greatly reduced by the presence of fibrous network and muscle fibres. In some regions the coelomic epithelium is found to be lacking due to its transformation into other tissues.
Coelomic sacs are present in the body of Balanoglossus. The proboscis coelom (protocoel) is an unpaired cavity. This cavity is greatly reduced by the connective and muscular tissues except at a central space which accommodates the proboscis complex. The buccal diverticulum, central sinus, heart vesicle and glomerulus constitute the proboscis complex.
The proboscis coelom opens to the exterior through a proboscis pore by way of tubular proboscis canal. All species under this genus have one proboscis pore and canal, but Balanoglossus australiensis has two such canals and pores. Such occurrence is to be treated as an individual variation.
The collar coelom (Mesocoel) is shifted as a pair of sacs between the buccal tube and the collar wall. The collar coelom and the proboscis coelom are not communicated with one another. Absence of septum between the proboscis and collar is an important feature in the anatomy of Balanoglossus.
The dorsal and ventral mesenteries separating the collar coeloms are mostly incomplete. In the proboscis stalk, the posterior end of the proboscis coelom and the anterior end of the collar coelom secrete a stiff chondroid tissue. It resembles the vertebrate cartilage and surrounds the main plate of the proboscis skeleton as a network.
The collar coeloms communicate to the exterior by the collar tubes and collar pores. Like that of collar coeloms, the trunk coelom (Metacoel) is divided into two lateral halves by the presence of dorsal and ventral mesenteries.
The former one is incomplete at many places which permit mixing of coelomic fluid in the two trunk coeloms. The central mesentery is complete. The collar coelom and the trunk coelom are separated by collar- trunk septum.
Each trunk coelom projects into the collar in the form of two evaginations, one is digit form and called perihaemal space and the other is peribuccal space. The peribuccal space is less developed in this genus. The evaginations push the collar-trunk septum into the collar and thus make the collar coelom complicated.
The coelomic fluid contained in the different coelomic cavities is different in composition. As the proboscis coelom and the trunk coelom have external communications, the coelomic fluid contains largely sea water. But the coelomic fluid present in the trunk coelom has amoeboid coelomocytes and the fluid coagulates in histological fixatives.
9. Digestive and Respiratory Systems of Balanoglossus:
The alimentary canal is a straight tube running between the mouth and anus. It is peculiar because musculature is absent. The mouth is a large opening situated on the ventral side of the collar.
Formerly, the mouth was believed to remain permanently open. But Knight-Jones (1953) has shown that the mouth is capable of being closed or opened. There are two sets of muscle fibres— the radial fibres which open the mouth and the sphincter muscles which close it.
The mouth leads into a short buccal tube housed in the collar. From the roof of the buccal tube, a buccal diverticulum is protruded into the proboscis coelom. The details of the buccal diverticulum have already been discussed under the heading—Supporting Structures. The buccal tube opens into the pharynx.
The pharynx is an elongated structure and plays the double role of food concentration and respiration. The physiological differences are marked by the morphological divisions of the pharynx.
A Para pharyngeal ridge on each side divides the cavity of the pharynx into two incomplete halves—a dorsal respiratory half pierced by gill-slits and a ventral half that helps in food concentration (see Fig. 2.3C). The pharynx leads into a short oesophagus which is followed posteriorly by the intestine.
The intestine is a straight tube and is distinguishable into an anterior hepatic region, marked by the sacculations on the dorsal wall of the intestine and a narrow post-hepatic region that opens to the exterior through the anus.
The branchial region is perforated by a longitudinal series of pharyngeal slits or gill-slits (Fig. 2.3B and 2.5A). The numbers of pharyngeal slits or gill-slits vary from 40 to 100 pairs in most cases but in Balanoglossus auranticus, the numbers of pharyngeal slits are 700 pairs and normally the number increases as the animal grows older.
Each pharyngeal slit is a U-shaped aperture (Fig. 2.5A). In Balanoglossus, the pharyngeal slit starts development as an oval slit (Fig. 2.6A). Subsequently, the dorsal end of the aperture projects downwards as the tongue-bar (Fig. 2.5A).
The tongue bars are immovable and remain fixed. The tongue bar does not touch the ventral side of the pharyngeal slit — as a result each pharyngeal slit assumes a U-shaped appearance.
The portions of the pharyngeal wall separating the successive pharyngeal slits are called primary pharyngeal bars or septa (Fig. 2.5B) and the tongue dorsal nerve dorsal blood pharyngeal bar cord vessel pore coelomic cavity bar (tongue bar) tongue bars that come to divide the primary pharyngeal slits are called secondary pharyngeal bars (Fig. 2.5B).
The secondary pharyngeal bars have a coelomic canal derived from the trunk coelom. The lateral sides of the primary and secondary pharyngeal bars are beset with lateral cilia, and help to move water currents through the pharynx.
The frontal cilia occur within the lining of the pharynx (Fig. 2.5B), also occur in the mucus-secreting epithelium along the medial edges of tongue bars and help in the movement of mucus. The primary pharyngeal bars and the tongue bars are supported by skeletal rods.
The gill-slits have no direct openings to the exterior. Each gill-slit leads into a pouch like cavity, called branchial sac which, in turn, opens to the exterior by the gill-pore.
All the species under the genus Balanoglossus have separate gill-pore for each branchial sac, but, in Balanoglossus misakiensis, the first four branchial sacs fuse with each other and open to the exterior through a common pharyngeal or gill-pore (see Fig. 2.10A). The gill-pores are situated along a longitudinal groove, called branchiogenital groove which also contains the gonopores.
Feeding and Digestion:
Balanoglossus takes sand as it burrows through the sand. The mucus, secreted by the proboscis, entangles the sand or other food particles from the surrounding region and the mucus coated particles are pushed directly into the mouth by the action of cilia (Fig. 2.7).
Balanoglossus is a ciliary feeder. It collects food particles outside the digestive tract. This process is done through the action of cilia of the body surface and the mucus secreted by the mucous glands. The gill-slits have little to do in trapping of the food particles. But the gill-slits in other protochordates—viz., the urochordates and cephalochordates—play a significant role in food collection.
The epidermal secretion in Balanoglossus, in addition to its normal participation in locomotion and burrowing, plays an essential role in feeding process. During feeding, the proboscis is protruded from the mouth of burrow. In this condition, the particles adhere to the mucus secreted by the epidermal glands and are carried towards the mouth.
The lateroventral beating of dorsal cilia at the base of the proboscis is significant in this ciliary feeding mechanism. The mucus threads are thus directed towards the ventrally located mouth.
Balanoglossus is able to stop continuous taking in of food particles and thus is able to reject unsuitable particles. The muscular lip of the collar plays the significant role in this process. It becomes folded over the mouth to close it. Closing occurs when a large particle is approaching and thus transported posteriorly over the collar.
A U-shaped epidermal groove bordered with strong cilia (preoral ciliary organ) situated at the base of proboscis plays significant role in the process. The preoral ciliary organ (Fig. 2.8) has receptor functions and provides a means for testing water and its contents approaching the mouth.
The alimentary canal of Balanoglossus is a straight tube extending from mouth to anus. It is lined by ciliated epithelium which has secretory and absorptive functions. The ciliated epithelium plays a major role in moving the gut contents as the gut musculature is weakly developed.
The food particles and mucus are drawn in through the mouth into the buccal cavity by the action of cilia, aided by the respiratory water current. The respiratory water current enters the mouth and leaves through the gill-slits. This current is primarily caused by the beating of the strong lateral cilia of the gill-bars.
The cilia beat in metachronal fashion to create waves passing around each gill-slit in an anti-clockwise direction. The pharynx in Balanoglossus plays a minor role in the collection of food particles. Burdon- Jones (1962) has shown the mechanism of food collection in Balanoglossus gigas (Fig. 2.9). The food particles are transferred to the ventral, i.e., non-respiratory division of the pharynx.
The finest particles which pass into the dorsal, i.e., respiratory-region are eventually collected by the synapticulae and are then transferred to the ventral division by ciliary action. The food materials pass on from the pharynx into the oesophagus by local contraction of gut musculature.
The process of digestion is not known in Balanoglossus. But in a related genus, Saccoglossus, the process of digestion has been recorded. As described earlier, the entire alimentary canal is ciliated and the backward beating causes the movement of the food posteriorly. Peristalsis is observed in the first sector of the alimentary canal.
The oesophagus is the most glandular part of the alimentary canal and is regarded to be the site of secretion of enzymes. The proboscis slime contains amylase. So the food is subjected to the action of enzyme before it gets entry into the intestine. The hepatic region of intestine produces traces of protease, maltase and lipase. These enzymes help in digestion.
Respiratory Mechanism:
In enteropneusts the pharynx is perforated by a series of gill pores that sum primarily to be respiratory in function. In Balanoglossus, the cilia present in the gill apparatus (Fig. 2.5B) and in the pharyngeal cavity help to maintain a powerful current of water.
The water current enters into the mouth and goes out through the gill-pores. The incoming water current brings food as well as fresh oxygen dissolved in water. During the expulsion of the water through the gill-pores, the carbon dioxide goes out along with the exhalant water current.
10. Circulatory System of Balanoglossus:
The circulatory system is well-developed is Balanoglossus (Fig. 2.10C). It comprises of blood, propulsatory heart vesicle, definite blood vessels and lacunar spaces.
The blood is colourless and contains a few detached endothelial cells. There are two main longitudinal blood vessels running along the length of the body. The dorsal vessel is situated just below the dorsal nerve cord and is contained in the dorsal mesentery.
The blood flows anteriorly through the dorsal vessel. The ventral vessel is located in the ventral mesentery and in it the blood flows posteriorly. These two blood vessels are composed of an inner endothelium surrounded by muscle layer.
The dorsal vessel extends from the anus to the collar where it takes a median position between two perihaemal cavities. The dorsal vessel at this region expands to form venosus sinus which passes anteriorly into a central sinus or heart. The central sinus is situated above the buccal diverticulum.
Immediately on the dorsal side of the central sinus there is a triangular sac called heart vesicle. The blood passes directly into the glomerular cavities from the central sinus. From the glomerulus, the blood is collected by four vessels. These vessels are regarded as the arteries because the blood leaving the glomerulus is regarded to be purified.
The arteries are:
(a) A mid-dorsal proboscis artery,
(b) A mid-ventral proboscis artery and
(c) Two efferent glomerular arteries.
The mid-dorsal and mid-ventral proboscis arteries supply blood to the proboscis wall. The efferent glomerular arteries run backward on the two sides of the buccal diverticulum. These vessels then run ventrally to encircle the buccal tube as the peribuccal arteries. The peribuccal arteries unite together ventrally to form the ventral longitudinal vessel.
The ventral longitudinal vessel gives origin to a ventral collar vessel to supply the collar. The collar tissue contains two distinct lacunar networks which communicate posteriorly with a ring vessel. The ring vessel is located in the collar-trunk septum. It arises from the ventral longitudinal vessel and is connected with the dorsal longitudinal vessel.
The ventral longitudinal vessel continues up to the anus and gives off lacunar networks all along the alimentary canal. The ventral longitudinal vessels give out a vessel in each gill septum which bifurcates to supply the two adjacent tongue-bars. Thus, each tongue-bar receives two afferent branchial arteries which break up into a plexus.
From this plexus an efferent branchial vein is formed. It runs dorsally up to the middle of the tongue-bar and joins with the efferent branchial vein of the adjacent tongue-bar. The common branchial vein opens into the dorsal longitudinal vessel (Fig. 2.10B). The blood from the intestinal plexus in the trunk region is collected mostly by the dorsal longitudinal vessel.
11. Excretory System of Balanoglossus:
A mass of coelomic evaginations in the proboscis complex is regarded as the excretory organ. Because of its similarities with the glomeruli of vertebrate kidney, the organ is regarded as the glomerulus. The glomerulus is situated on either side of the heart vesicle and assumes the shape of the heart vesicle and the central sinus (see Fig. 2.10C).
The cavities of the glomerulus are filled with blood which is confluent with the blood of the central sinus. The covering of the glomeruli is composed of excretory cells, called nephrocytes. Besides the glomerulus, some cells in the proboscis peritoneum, connective and chon- droid tissues of the collar and proboscis are regarded to be excretory in function. These excretory cells are named as paranephrocytes or arthrocytes.
12. Nervous System of Balanoglossus:
The nervous system of enteropneusts shows some resemblance to the ectoneural system of echinoderms. The nervous system of Balanoglossus represents a very primitive condition (Fig. 2.11). It consists of an intra-epidermal nervous layer at the base of the epidermis.
The nervous layer is composed of longitudinal nerve fibres with bipolar and multipolar nerve cells at the margin. The nervous layer becomes thickened to form two nerve cords, one is situated in the mid-dorsal and the other in the mid-ventral lines of the trunk.
The ventral and the dorsal trunk cords are connected by a circumenteric or peribranchial nerve ring along the collar- trunk septum. The dorsal trunk cord in the collar leaves the epidermis and projects into the collar coelom as the collar cord or neurocord.
The collar cord is situated above the buccal tube and contains a continuous lumen in other hemichordates. But such a lumen is not seen in Balanoglossus. The cellular nerve cord contains many giant nerve cells with axons projecting anteriorly and posteriorly. These are believed to control the contraction of the body. In the base of the proboscis, the nervous layer becomes thickened to form a circular anterior nerve ring.
From the anterior nerve ring longitudinal nerve fibres are given out. There is no central nervous system in Balanoglossus. Isolates, from any part of the body, exhibit local reflex responses to touch or light stimulus for a considerable period.
The organization of nervous system of enteropneusts reflects a more primitive condition than the echinoderms because it has not any clearly defined motor system that may resemble the hypo-neural system of the starfish. There is no special organ of sense. Extending all over the body, there are receptor cells which respond to tactile stimulation.
13. Reproductive System of Balanoglossus:
Balanoglossus reproduces normally by sexual process. Asexual reproduction occurs very rarely.
Asexual Reproduction:
Asexual reproduction is an unusual phenomenon and occurs in Balanoglossus capensis. It reproduces by separating off a small fraction of the body from the posterior end in summer. This fragment regenerates into sexual adult.
Sexual Reproduction:
The sexes are separate (gonochoristic), but the males and females cannot be distinguished externally. The gonads are sacculated bodies arranged in longitudinal rows outside the coelom of the branchiogenital region of the trunk (see Fig. 2.3C). Many secondary gonads are produced from the primary gonads. Each gonad proliferates and bulges into the coelomic cavity.
Each gonad is covered by somatopleure and forms a slender tubular neck which opens externally by a gonopore. The gonopores are situated in the branchiogenital groove. The gametes are discharged to the exterior and fertilization is external.
The eggs are small.
The yolk content is very poor.
Regeneration:
Balanoglossus exhibits great regenerative potency. Isolated pieces from the trunk have the inherent property to regenerate the lost parts.
14. Development of Balanoglossus:
The development is indirect, i.e., the development is followed by the metamorphosis of a well-developed larval form.
Pre-larval Development:
The pre-larval developmental stages resemble closely that of Branchiostoma. The cleavage is holoblastic and occurs along radial planes. The resultant blastomeres are approximately equal. A coeloblastula is produced which is transformed into a gastrula by invagination within 24 hours.
The developing embryo elongates along the anteroposterior axis and develops cilia. The mouth and the anus are formed anew. The coelom develops by enterocoelic method. After about 24 to 36 hours, the embryo escapes as a larva. This larva was first observed by Johannes Muller (1850) who gave the name Tornaria because of its habit of rotating in circles.
Larval Development—Tornaria Larva:
The tornaria larva has an oval and bilaterally symmetrical body (Fig. 2.12A). The size of the tornaria larva varies from 1-3 mm, The mouth is present on the ventral side near the equatorial plane of the body. The portion of the body anterior to the mouth is prolonged into a preoral lobe.
Anterior end of the pre-oral lobe bears a distinct apical plate bearing nerve fibres, ganglionic nerve cells, a tuft of immobile cilia and a pair of pigmented eye-spots. There are three distinct ciliated bands on the body. The name of the bands has been given according to their position. The preoral and postoral ciliated bands unite for a short distance at the apical plate.
The other ciliated ring is present around the anus. This band is called the circumanal ciliated band or telotroch. The cilia in this band are long, powerful and act as the chief locomotors organ of tornaria. The anus is located medially on the posterior end of the body. The digestive tract is distinguishable into oesophagus, stomach and intestine.
The tornaria larva possesses only one pair of gill-slits. Five coelomic cavities are present which exhibit the trisegmental condition of the body. Finally, the tornaria larva sinks to the bottom and metamorphoses into an adult (Fig. 2.12B-C). The body becomes divided into three parts by two constrictions. It then undergoes morphological changes to become an adult.
15. Affinities and Systematic Position of Balanoglossus:
Balanoglossus has a peculiar anatomical organisation. Its systematic position in the animal kingdom is still uncertain. Almost all the non-chordate phyla have been suggested to be nearest to the Hemichordata. Many authors have claimed Hemichordata as a separate phylum under the non-chordates.
Some of the views existing on this particular aspect of Balanoglossus are described below:
Non-chordate Affinities:
Balanoglossus shows many structural similarities with non-chordates.
Relationship with Annelida:
Many authors like Dohrn (1875), Semper (1876) and Minot (1897) have attempted to bring Balanoglossus and Annelids on the level of a distinct phylogenetic relationship.
The relationship was based on the following points of similarities:
(a) Both of them have a vermiform and coelomate body.
(b) The arrangement of the blood vessels is similar.
(c) The collar of Balanoglossus is comparable to the clitellum of oligochaetes.
(d) The Trochophore larva of annelids bears close structural resemblances with the Tornaria larva, specially in the apical sense organ and the ciliated rings.
Remarks:
Despite such resemblances, these two groups are fundamentally different:
(i) The Trochophore larva bears a pair of nephridia which are absent in Tornaria larva,
(ii) Biochemistry is dissimilar,
(iii) Notochord is absent in Annelida.
Relationship with Phoronida:
Masterman advocated the relationship of Balanoglossus with Phoronida.
The Actinotrocha larva of Phoronis and the Tornaria larva show the following similarities:
(a) Both have similar disposition of the coelom.
(b) The anus is surrounded by a ring of cilia,
(c) The proboscis pore is comparable to the water pore of the Actinotrocha.
Remarks:
Many authors have placed the phoronids under a separate order of the Hemichordata. Masterman gave the strongest support to this idea.
Relationship with Pogonophora:
Marcus (1958) showed the following similarities between Hemichordata and Pogonophora:
(a) Enterocoelous coelom with similar divisions,
(b) Intra-epidermal nervous system,
(c) Gonads placed at trunk region,
(d) Some pogonophores have pericardial sacs,
(e) Septum between mesosome and metasome.
But the main nervous system in pogonophores is concentrated at protosome but it is concentrated at mesosome in Balanoglossus. Pogonophore does not have any alimentary canal. Balanoglossus has no metacoelic coelomoducts while pogonophores have mesocoelic coelomoducts.
Remarks:
The proposed affinities are superficial and the similarities are due to common phylogenetic connection.
Relationship with Echinodermata:
Adult hemichordates and echionoderms are quite different in their organization and it is difficult to draw their phylogenetic relationship between themselves.
Some resemblances are as follows:
A. Anatomical similarity:
a. Nervous system is intra-epidermal in both groups and constructed on the nerve net principle.
b. Glomerulus of enteropneusts may be homologous to the axial glands of echinoderms.
B. Palaeontological Similarity:
The most primitive known echinoderms— the Cambrian and Ordovician carpoid might be conceived as Tornaria-like forms, which had begun to settle down to a sedentary life, acquiring an exoskeleton of many plates, together with a water pore system developed out of ciliated grooves.
Gislen (1930) said — “There must be a similarity between carpoid echinoderms with Hemichordata”. This view has been challenged by Prof. MacGregor.
Jefferies (1968, ’81) tries to create links between the two groups – the early echinoderms, called carpoid echinoderms and hemichordates. The similarities drawn between Cephalodiscus and the early cornuate Ceratocystis (Calcichordate) are the gill- slits and other essential characteristics of the true chordata.
This view has been criticised by Ubaghs (1979, ’99) and Jollie (1982). But Willmer (1990) states that echinoderms, hemichordates and chordates are closely allied groups.
C. Biochemical Similarity:
The phylogenetic similarity can be drawn between the hemichordates and echinoderms by biochemical studies. In some echinoderms (echinoids), there are creatine phosphate which are also found in hemichordates. Needham (1932) has shown the presence of phosphogen as the Phosphorus-carrier in the echinoderms and chordates.
D. Embryological Similarity:
Willey, Metschnikoff and others tried to draw the relationship in between tornaria larva of enteropneusts and auricularia larva of Echinoderms. Hemichordates, like both echinoderms and chordates are deuterostomes.
Similarities:
a. Both have similar twisted ciliated bands.
b. Enterocoelomic method of coelom formation.
c. Pattern of embryonic cleavage (radial) is same in both groups.
d. The position of mouth and anus is similar.
e. Simple digestive system in both.
f. Mode of development is similar.
g. The larvae are free-swimming.
A possible homologies between echinoderms and hemichordates are given in Table 11.
Remarks:
H. B. Fell (1948):
After having a detailed discussion he concludes that the resemblance is due to parallel or convergent evolution and so there cannot be true affinity between the two groups.
Hyman (1959):
It is not reasonable to suppose that many resemblances in the embryonic events between hemichordates and echinoderms can be accidental or the result of convergence. There appears no escape from the conclusion that hemichordates and echinoderms stem from a common ancestor.
Molecular Analysis:
Molecular analysis offers a great source of data for the comparison of gene sequences of any gene between two dissimilar animals or groups to draw a” phylogenetic relationship. Recent DNA analysis, such as 18rDNA sequence analyses, of enteropneusts suggests that enteropneusts are more closer to the echinoderms than between hemichordates and chordates.
Chordate Affinities:
Inclusion of Balanoglossus under the Phylum Chordata is not universally accepted. Because of the three fundamental characteristics of the chordate organisation, the nature of notochord is really questionable. Recent workers do not accept the notochordal nature of the buccal diverticulum.
The nervous system, in general, is typically of non-chordate type excepting the presence of lumen in collar nerve cord. The only important chordate feature is the gill-slits.
Because of the reasons, some authors include the hemichordates under the non-chordates and others place them under an appendix to the Phylum Chordata. In the present discussion, the Hemichordata has been given the status of a phylum. This will help to avoid controversies to a large extent.
Relationship with Urochordata:
The nearest to the existing forms of the hemichordates are the urochordates, because they exhibit many close similarities with the hemichordates. The similarities in the pharynx and in the branchial apparatus are most convincing. The development of the central part of the nervous system is quite similar in both.
Remarks:
The above relationship becomes difficult to establish because the chordate nature of the hemichordate itself is questionable. The resemblances are due to the fact that the hemichordates are very remotely connected with the central stock from which the urochordates have descended.
Relationship with Cephalochordata:
Similarities in the structure and function of the branchial apparatus, in the arrangement of coelomic sacs and in development establish close relationship of the hemichordates with the cephalochordates.
Presence of un-segmented muscle fibres in hemichordates and dissimilarities in the developmental history stand as barriers to establish any close relationship. Hemichordata must be regarded as lower in rank than Cephalochordata, because most of the characters in Hemichordata are primitive and rudimentary in nature.
Systematic Position and Phylogeny:
Discussing the structural organisation it is still controversial and problematical for the systematic position of Balanoglossus or hemichordates. First Bateson (1885) placed Balanoglossus under the phylum chordate as a sub-phylum Hemichordata, for its notochord structure. Later authors like Young (1962, ’81), Marshall and Williams (1964), also followed this scheme.
According to Marshall and Williams (1964) — the gill-slits with their tongue-bars and the dorsal tubular neurocord are the important features for the inclusion under the Phylum Chordata. Again according to Young (1981) — the hollow dorsal nerve cord, the tongue-barred gill-slits and notochord are sufficient to show affinity with the chordates.
But starting from Van der Horst (1939) and later authors like Hyman (1959), Jollie (1962), Barrington (1979), Barnes (1987), Ruppert and Barnes (1994), Anderson (1998), Pechenik (2000) and Kardong (1998, 2002) — they have all chosen to remove the Hemichordata from the Phylum Chordata and treat the group as a separate invertebrate Phylum-Hemichordata.
Among three main features for the Phylum-Chordata, the pharyngotremy remains as the chief link between hemichordates and chordates. Other two features-like nervous system (partly) and notochord, do not strongly support in favour of chordates.
Again analysing the molecular structure (gene expression) of enteropneusts, Hemichordata may be considered as a separate invertebrate phylum status because Hemichordata is more closely related to echinoderms rather than chordates, ignoring the doubtful homologies of some structures with the chordates.
Regarding phylogeny, the structural similarities with the different groups demand a link between chordates in one hand, and echinoderms and groups of other invertebrates in other hand. The hemichordates, mainly the enteropneusts, provide a link between the true chordates and echinoderms.
In the later part of 19th century and first part of 20th century the buccal diverticulum of Balanoglossus was considered as a notochord and established a main link with the chordates.
But the structural analysis of notochord (= stomochord) in enteropneusts reveals that stomochord is a hollow structure, develops anterior to the pharynx from the endoderm and lacks a fibrous sheath around it, fails to give the rigidity of the stomochord. So to include in the chordates, the concept becomes failure.
Again molecular analysis fails to find a homology between the stomochord of hemichordates and notochord of other chordates. Though most authors admit that there are more resemblances to chordates, but larval similarities (auricularia larva of echinoderms and tornaria larva of enteropneusts) and molecular analysis draw a closer link between echinoderms and hemichordates rather than hemichordates and other chordates.
The chordates, hemichordates (mainly acorn worms) and echinoderms (such as starfish) comprise the group deuterostomia and are well-established as monophyletic.
Different schemes have been proposed regarding the phylogenetic relationships of the deuterostomes. Most earlier and traditional view is that the deuterostomes have arisen from a common central stock, probably the dipleurula larva.
In this scheme (Fig. 2.13) echinoderms were departed near the base of the deuterostome tree and hemichordates were close to the branch but could not qualify a fully chordate.
Many authors like Berrill (1955), Carter (1957), Marcus (1958), Hyman (1959), Bone (1979, ’81) and Jefferies (1986) do not support the view. There is other view which is now used widely.
In this view all deuterostomes arise from a hemichordate-like animal, and hemichordates or tunicates give rise to higher chordates (cephalochordates and vertebrates) by a process of neoteny (Fig. 2.14). The neoteny is seen in larvacean tunicates and in some cephalochordate larvae. So this concept may be acceptable as the origin of hemichordates.
Again Barrington (1965) has summarised the interpretations of Berrill (1955), Bone (1960), Carter (1957), Marcus (1958) and Whitear (1957) and has given a scheme to point out the relationship of hemichordates with other chordates (Fig. 2.18).