بریوزوآ-Bryozoa

Bryozoa

 

A phylum of sessile aquatic invertebrates (also called Polyzoa) which form colonies of zooids. Each zooid, in its basic form, has a lophophore of ciliated tentacles situated distally on an introvert, a looped gut with the mouth inside the lophophore and the anus outside, a coelomic body cavity, and (commonly) a protective exoskeleton (Fig. 1). The colonies are variable in size and habit (Figs. 2 and 3). Some are known as lace corals and others as sea mats, but the only general name is bryozoans (sea mosses).

 

Fig. 1  Morphological features of autozooids, in frontal view.

 

 

 

 

 

 

Fig. 2  Stenolaemate morphologic features, some of which are found only in living colonies and others only in fossil colonies. The enlarged oblique view is from the colony at the lower right.

 

 

 

 

 

 

Fig. 3  Morphological features of gymnolaemate colony, and enlarged oblique view of block from it.

 

 

 

 

 

 

General Characteristics

 

Byrozoans form colonies by asexual budding from a primary zooid, or ancestrula, formed by metamorphosis of a sexually produced larva or from some kind of resting bud. Structurally the zooids are metazoan, triploblastic, unsegmented, and bilaterally symmetrical, with a regionated fluid-filled body cavity that is considered to be a coelom. The body wall comprises epidermis underlain by a feebly developed peritoneum, between which muscle may be present. The epidermis secretes a chitinlike cuticle or gelatinous layer, and the cuticle may become calcified as a rigid exoskeleton.

Much of the zooid consists of the lophophore, alimentary canal, and associated musculature, together known as the polypide. The lophophore comprises a circle or crescent of slender, ciliated tentacles plus their supporting ridge. When spread for feeding, the tentacles form a funnel with the mouth at its vertex. During withdrawal the tentacles close, and are pulled downward from their base through the simultaneously in-rolling introvert. They then lie within the introvert, called the tentacle sheath. The open distal end of the in-rolled tentacle sheath is termed the orifice, and it may be closed simply by a sphincter muscle or by more elaborate structures.

The alimentary canal is deeply looped, and regionated into pharynx, stomach, and rectum. The limb descending from the mouth consists basically of the pharynx and stomach cardia; the central stomach and its dilatation, the cecum, form the base of the loop; and the stomach pylorus and the rectum constitute the ascending limb. The anus opens outside the lophophore. The nerve ganglion, center of a system that may be complex, lies between the mouth and the anus. There are no special excretory or respiratory organs, and no circulatory system. Colonies, but not all zooids, are hermaphroditic. Zooids are generally not more than 0.04 in. (1 mm) long.

The colony may be minute, of not more than a single feeding zooid and its immediate buds, or substantial, forming masses 3 ft (1 m) in circumference, festoons 1.5 ft (0.5 m) in length, or patches 0.67 ft2 (0.25 m2) in area. Commonly the colonies form incrustations not more than a few square centimeters in area, small twiggy bushes up to about 1.2 in. (3 cm) in height, or soft masses up to about 4 in. (10 cm) in the largest dimension. In many colonies much of the bulk consists of the zooid exoskeletons, termed zooecia, which may persist long after the death of the organism and account for the abundance of fossilized bryozoan remains.

Many bryozoans display polymorphism, having certain zooids adapted in particular ways to perform specialized functions, such as protection, cleaning the surface, anchoring the colony, or sheltering the embryo. The evolution of nonfeeding polymorphs is dependent upon some form of intercommunication between zooids.

All bryozoans are epibenthic, and are generally attached to firm substrata, less often anchored in or resting on sand. Most are marine, but one complete class (Phylactolaemata) is confined to fresh water. In the latter habitat, statoblasts and hibernacula, resting bodies resistant to cold and desiccation, are produced. Sexual reproduction leads either to a distinctive, planktotrophic larva, called the cyphonautes, or more usually to a subspherical, nonfeeding, short-lived type that has had no particular name until recently distinguished as “coronate,” because of its extensive ciliary corona.

 

Taxonomy and classification

 

Bryozoa is the name of a phylum for which Ectoprocta is generally regarded as a synonym, these names being used by zoologists according to personal preference. Entoprocta (synonym Calyssozoa) is likewise regarded as an independent phylum. A minority regard Ectoprocta and Entoprocta as subphyla within the Bryozoa, while others maintain Ectoprocta and Entoprocta as phyla but link them under Bryozoa as a name of convenience.  See also: Entoprocta

The phylum contains some 20,000 described species, one-fifth of them living. These are distributed among three classes and a somewhat variable number of orders.

Class Phylactolaemata

Order Plumatellida

Class Gymnolaemata

Order: Ctenostomata

Cheilostomata

Class Stenolaemata

Order: Cyclostomata

Cystoporata

Trepostomata

Cryptostomata

Hederellida

 

 See also: Gymnolaemata; Phylactolaemata; Stenolaemata

Until somewhat over 200 years ago bryozoans went unrecognized. When discovered they were thought, with coelenterates, to be plants—a confusion that led Linnaeus to invent the term zoophyte. In 1830 J. Vaughan Thompson characterized bryozoans, separating them from other zoophytes, but at the same time ambiguously introducing a class Polyzoa. G. C. Ehrenberg's name Bryozoa followed in 1831.  See also: Cryptostomata; Ctenostomata; Cyclostomata (Bryozoa); Cystoporata; Hederellida; Trepostomata

Comparative morphologists link the Bryozoa with the Phoronida and the Brachiopoda, characterized especially by possession of a lophophore, which L. H. Hyman defined as “a tentaculated extension of the mesosome that embraces the mouth but not the anus, and has a coelomic lumen.” The tentacle circlet of the Entoprocta is postanal and noncoelomic. The designation of the bryozoan lophophore as mesosomal, and its body cavity as mesocoelic, rests entirely on the interpretation of a supraoral flap of tissue, the epistome, present in phylactolaemates, as the protosome or first region of a tripartite body. In addition to the lophophore and presumed tripartite body, all three phyla have a U-shaped alimentary tract. The lophophore is crescentic in some members of all three groups. Even if the relationship is correct, however, it sheds little light on bryozoan origins. The soft-bodied Phylactolaemata have left no fossil record, but comparative anatomy suggests that they, the Stenolaemata, and the Gymnolaemata must already have been distinct by the Ordovician. The view that Bryozoa arose from entoprocts, perhaps by internal budding from the larva, seems tenuous, and implies at most no more than a similarity between larvae such as that which links Mollusca to Annelida. Certainly the immediate ancestor must have been vermiform and sedentary, for cylindrical zooids, terminal lophophores, and deeply recurved digestive tracts with the anus rather close to the mouth represent the primitive state in all classes.

 

Functional morphology of zooid

 

Zooids in all three bryozoan classes display the same ground plan: eversible lophophore, U-shaped gut, fluid-filled coelom, and deformable body wall. The lophophore is everted by increase in hydrostatic pressure caused by inflexion of the body wall; withdrawal is achieved by the direct pull of retractor muscles anchored to the wall. The flexible phylactolaemate wall incorporates circular and longitudinal muscle, and its contraction everts the lophophore. Recent work indicates that stenolaemates, as evidenced by the extant Cyclostomata, have a remarkably modified system. Throughout this class the zooid is cylindrical (often inaccurately described as tubular; only the exoskeleton is tubular). Except in the immediate vicinity of the orifice, the cuticle is calcified and totally rigid. The peritoneum, with a hypertrophied basal membrane and associated bands of circular muscle, has detached from the epidermis and lies freely as a bag, the membranous sac, anchored at some points to the body wall. The endosaccal cavity is coelomic, but the exosaccal cavity, external to the mesoderm, is not. The sac contracts to evert the lophophore; exosaccal fluid must be displaced proximally as the polypide is eased toward the orifice.

The simplest gymnolaemates (Ctenostomata) have cylindrical zooids and deformable walls, although the musculature is extrinsic. The circular (now renamed transverse parietal) muscles lie inside the peritoneum, and the longitudinal muscles are reduced and specialized. Mechanically the system works as in Phylactolaemata. An early trend of zooidal evolution in the Gymnolaemata was toward a flat, membranous, coffinlike shape, adherent to the substratum. It seems probable that the cheilostomes arose from ctenostomes like that by calcification of the lateral walls and the differentiation of a cuticular lid, the operculum, to close the orifice. Cheilostomes of this plan, classified as the suborder Anasca, preserve a wholly or partially flexible front wall. Transverse parietal muscles, relocated to span the coelom from the rigid lateral walls to the frontal membrane, bring about its inflexion.

Natural selection in cheilostomes has favored modifications which better protect the polypide while preserving the function of the frontal membrane. Thus the frontal membrane can be underlain by a shelf, at a distance sufficient to permit inflexion; or it can be overarched by flattened spines or by a meshwork of partially fused spines. In the subclass Ascophora the membrane may be overgrown or replaced by a calcified frontal wall, but the flexible membrane either remains or is replaced more deeply by a functional equivalent. A saclike cavity or ascus, opening just behind the orifice, is created either by overgrowth of the wall or by involution from the orifice underneath the wall. Transverse parietal muscles insert on the lower face of the ascus, which is pulled down to evert the lophophore, while water to compensate for the volume change enters the ascus through its opening.

 

Feeding

 

The expanded lophophore of marine bryozoans forms an almost radially symmetrical funnel of 8–30 tentacles, although fixed or transient bilateral symmetry may occur. In gymnolaemates the base of this funnel stands free above the surface of the zooid, but in stenolaemates it lies concealed within the orificial region of the exoskeleton. The top diameter is in the range of 0.01 to 0.05 in. (0.25 to 1.25 mm). In primitive phylactolaemates 20–30 tentacles form a funnel, but in most members of this class the large lophophore comprises 100 or more tentacles disposed in a horseshoe, the lobes of which project from the adanal side.

The base of the lophophore is the most complex part of the polypide. Essentially it is a hollow epidermal annulus, with thickened basement membrane. The lumen (mesocoel) opens into the main body cavity (metacoel) by an adanal pore. The cerebral ganglion partly occludes this pore, and a nerve tract parallels the mesocoel. Radial and circular muscles open and close the mouth. The tentacles rise from the annulus as slender hollow cylinders. Their central coelom is surrounded by a thick, flanged collagenous tube, the hypertrophied basement membrane of the epidermal cells. The lumen, which opens terminally through a minute pore, is lined by peritoneum and contains frontal (that is, facing into the funnel) and abfrontal longitudinal muscles. The lateral epidermal cells bear long cilia (about 25 micrometers) and the frontal cells shorter cilia (about 15 μm). Laterofrontally is a line of static sensory cilia. The tentacles contain motor and sensory nerves.

The lateral cilia generate a water current that enters the top of the funnel and flows downward and outward between the tentacles. Particles such as bacteria and phytoplankton are separated from the water and directed at the mouth by the frontal cilia without the use of mucus. The mechanism of separation is uncertain, but a likely explanation is that particles passing out between the tentacles, perhaps sensed by the rigid laterofrontal cilia, are flicked back into the funnel by localized reversal of ciliary beat. Small particles accumulate just above the mouth; heavier particles may be projected down the funnel and directly into the partly open mouth.

Unwanted particles are rejected by closing the mouth, flicking the tentacles, closure or concerted movements of the funnel, and ejection from the pharynx (see below). A few bryozoans with large lophophores have rejection tracts leading centrifugally between the ventromedial (abanal) tentacles. Bryozoans are vigorous feeders, and it has been calculated that the lophophore of even a small zooid filters about 0.3 ml/h (and a colony may contain thousands of zooids).

Bryozoan colonies may have exhalant chimneys or set points of water outflow. The reason is clear: if the colony is large, solid, flat, and uniformly covered by tentacular funnels pumping toward its surface, the filtered water requires a means to get away. Small colonies may have a single, central chimney; large colonies may have a mamillate surface, the summit of each mamilla marking a chimney; and wholly flat colonies produce chimneys by an apparently coordinated bending away of lophophores from predetermined points. Filtered water flows toward the chimneys, through which it is expelled. Lophophores surrounding a chimney display strong bilateral symmetry, with the bordering tentacles standing tall and upright instead of curving into the chimney. A consequence of the posture is that the beat of the current-generating lateral cilia becomes centripetal to the chimney rather than being unhelpfully directed toward its base.

The pharynx is a remarkable organ. It is short, thick-walled, and situated immediately below the mouth. Its exterior is circular in section, its interior deeply furrowed. The frontal ciliation from the lophophore continues through the mouth and may cover the distal part of the pharynx: the midventral groove is ciliated, even when the rest of the pharynx is not, and its cilia beat upward, whether there is a ventromedial rejection tract or not. Between the grooves, the inwardly bulging walls are made up of vacuolated cells which incorporate intracellular myofibrils. The simultaneous contraction of all the myofibrils, acting against the fluid-filled vacuole, causes a brief convulsive dilation of the pharynx, engulfing the particles accumulated outside the mouth.

A sphincter and valve separate the pharynx from the cardia (descending arm of the stomach). In some ctenostomes, and a few other bryozoans, part of the cardia is differentiated as a gizzard, armed internally with teeth or keratinized plates, presumably for crushing the frustules of diatoms. The unmodified wall of the cardia contains secretory cells. The floor of the central stomach is ciliated, evidently to carry particles into the cecum, which is the main locus of extra- and intracellular digestion and absorption. The epithelium of the pylorus is ciliated and serves to compact the undigested remains into a revolving cord. A sphincter separates the pylorus from the rectum, which has an absorptive function and modifies the cord of reject material into fecal pellets. The pellet is moved through and expelled from the rectum by peristalsis. At summer temperatures (72°F or 22°C) the gut transit time is less than 1 h but at 43°F (6°C) it is 2 h.

 

Metabolic integration and colony evolution

 

The simplest bryozoan colonies presumably consisted of loosely interconnected, monomorphic feeding zooids. In the most ancient fossil stenolaemates, confluence of coeloms had been achieved either by means of internal pores or by the so-called double wall, in which a superficial (or hypostegal) coelom unites the colony outside the calcification. The hypostegal coelom must have been reasonably effective as a means of distributing metabolites, since the colonies of trepostomes were large by bryozoan standards, and the fenestrates evolved colony forms of considerable complexity. However, rapid growth and the proliferation of nonfeeding zooid polymorphs requires a transport system more efficient than aqueous diffusion. The funiculus provides such a system.

In living single-walled stenolaemates (cyclostomes) zooids communicate via small, open interzooidal pores. The funiculus is a small muscular strand linking the proximal end of the cecum with the base of the membranous sac at its attachment to the zooid wall. The testis is positioned where the funiculus joins the cecum. The phylactolaemate funiculus similarly is muscular, supports the testis, and links the cecum to the proximal end of the ventral body wall. More importantly, it contains a core of blastogenic tissue from which the statoblasts arise. These are the future resting buds and become richly supplied with yolk. The obvious inference is that the products of digestion are transported, perhaps to the testis but certainly to the developing statoblasts, along the funiculus. Communication between zooids in phylactolaemates is by open pores; indeed in many of them the dividing walls have almost completely broken down, so that the polypides are suspended in a communal coelom.

The adaptive radiation of zooid form has been very slight in both Cyclostomata and Phylactolaemata. Cyclostome zooids have remained as slender cylinders, while the colonies have evolved mainly in terms of the way in which the zooids are disposed. Thus regular, alternating placement of zooid orifices is replaced by a pattern of separated short rows or fascicles, presumably to improve feeding efficiency; and erect or partially erect colonies have evolved from creeping ones. The reproductive zooids, at first clearly in series with the rest, become larger, more central, and often truly colonial by incorporating neighboring structures. Phylactolaemates have evolved larger, deeply crescentic lophophores, but the zooids have not diversified. Evolution of the colony has been toward unity by confluence of coeloms.

Primitive gymnolaemates have an organization very like that of the simpler phylactolaemates: elongate zooids connected by simple open pores, with the funiculus confined within each zooid. The radiation of stolonate ctenostomes has been facilitated by the development of a colonial, essentially nonmuscular funiculus which passes through the internal pores between zooids and along the stolons. A flux of lipid from feeding zooids into the stolonal funiculus occurs and spreads toward the growth and budding zones. The funiculus has become a colony-wide metabolic expressway.

When cheilostomes evolved from ctenostomes, they inherited the funicular system. They added mural calcification and developed complex communicating pores in the lateral walls, while retaining simple pores in the end walls. The main funicular trunks are longitudinal, passing from the proximal pores to the distal pores via the cecum, with branches to the lateral pores. The success of the Cheilostomata, in terms of species numbers, adaptive radiation, and polymorphism, is evidently the result of a high-potential module, plus the distributive efficiency of the funiculus in nourishing large numbers of specialized, nonfeeding zooids.

 

Nervous system

 

The cerebral ganglion is dorsally (adanally) situated in the lophophore base and has a diameter of 30–60 μm. It is extended circumorally as a ring or deep crescent. Apart from the fibrillar component, the anascan ganglion contains distal, central, and proximal groupings of cell bodies. The principal nerves are the following. (1) Sensory and motor lophophoral nerves. (2) Paired direct tentacle sheath nerves which unite with the first branch of the trifid nerve to form (3) the compound tentacle sheath nerves: these extend up the tentacle sheath to the superficial part of the zooid, including the sensitive region near the orifice. (4) The trifid motor nerve; of its three branches, the first, 4a, is visceral, meeting its opposite number at a small suprapharyngeal visceral ganglion; the second, 4b, innervates the paired retractor muscles of the polypide; and the third, 4c, joins the compound tentacle sheath nerve and innervates the tentacle sheath muscles, the orificial sphincter, occlusors of the operculum, and the transverse parietal muscles that deflect the frontal membrane. It will be noted that 4b and 4c innervate the antagonistic effectors in polypide withdrawal and eversion. (5) Paired parietal nerves parallel the direct tentacle sheath nerves, but pass deep to join a peripheral encircling ring which enters in turn each of the interzooidal pores. Here the parietal nerves of neighboring zooids make contact. (6) Paired visceral nerves originate in the suprapharyngeal ganglion.

Electrophysiological research has confirmed the existence of a functional colony-wide nervous system in anascans. Stimulation near the orifice results in the immediate withdrawal of all nearby expanded lophophores (while stimulation of a lophophore results only in its withdrawal).

 

Polymorphism

 

Phylactolaemates have achieved integration at the expense of zooid individuality, so that polymorphs have not evolved (unless the statoblasts are so regarded). Stenolaemates have metabolic integration dependent on diffusion gradients, and display weakly developed polymorphism. In living cyclostomes, four morphs are commonly encountered: (1) normal-feeding or autozooids; (2) empty or kenozooids of various kinds, which support colonies, make up attachment rhizoids and stolons, in-fill spaces, and project as spines; (3) female or gynozooids, also called brooding or gonozooids, that do not feed but produce ova and shelter the developing embryos; and (4) dwarf or nanozooids, containing a reduced unitentaculate polypide which sweeps and cleans the surface of the colony. All zooids which are not autozooids may be termed heterozooids.

Among gymnolaemates, which have metabolic integration via the funiculus, the ctenostomes have limited polymorphism. Apart from the autozooids, only kenozooids are commonly present, either as stolon segments or as spines attached to autozooids. The cylindrical type of zooid, whether calcified or cuticularized, has not provided the potential for extensive polymorphism. In cheilostomes, on the contrary, one sees a wide range of heterozooids, high numbers of heteromorphs per colony, and the grouping of polymorphs into functional units or cormidia (colonies within colonies). Of importance in contributing to such impressive adaptive radiation seem to be the funicular system, the retention of individualistic zooids, and the calcified, boxlike zooid with its partly membranous front and hinged, lidlike operculum closing the orifice.

Cheilostome zooid types merge with one another, but the following may usefully be recognized: (1) sterile or fertile autozooids, which may also brood embryos but do feed, at least for most of the time; (2) androzooids or nonfeeding males with reduced polypides; (3) gynozooids (gonozooids), nonfeeding females which produce ova and sometimes brood the embryo; (4) avicularia, in which the operculum is enlarged; (5) vibracula, in which the operculum is lengthened to whiplike proportions; (6) kenozooids for in-filling, or associated with attachment rootlets and stolons; (7) kenozooids in the form of spines; and (8) ooecia or brood chambers.

Avicularia appear to be zooids modified for grasping. They vary in form from something close to an autozooid, differing only in having an enlarged operculum, or mandible, to diminutive and highly modified structures. The large ones often obviously replace autozooids in the colony, and are termed vicarious; the smaller ones are attached to auto-zooids, and are termed adventitious. Often a zooid may bear several adventitious avicularia of different kinds and in a variety of positions. Abductor muscles open the mandible by pulling down the small frontal membrane just behind the hingeline, whereas larger adductors snap it shut. In its most evolved form, the bird's-head avicularium, the zooid is pedunculate and mobile. The avicularian polypide is much reduced, and is believed to fulfill a sensory role.

Some avicularia have a long slender mandible, and may be precursors of vibracula, in which the operculum has become a whiplike seta. The vibracular seta, however, is mounted on asymmetrical condyles and can be swiveled by gyrator muscles, as well as being moved through a regular arc. In some species the vibracula remove sediment from the colony surface, and in nonattached sand-living forms they also act as struts or legs.

Spines are small kenozooids of varied form. They are normally adventitious and presumably have a protective role. The arguments for regarding cheilostome spines as zooids are basically three: they are separated from their bearing autozooid by a communication pore of standard morphology; they terminate with a flat membrane, seen as homologous to a frontal membrane; and they may replace an undoubted polymorph, for example, an autozooid or avicularium. The fundamental arrangement of spines in anascans is as a marginal ring around the frontal membrane. One worker sees this as the vestige of an ancient type of budding, each spine representing what was once a free-rising series of zooids. Even when this annular pattern is modified, as in certain erect, branching anascans and in ascophorans, the basic arrangement frequently persists in the founding zooid or ancestrula. In later zooids the spines are confined to the immediate region of the orifice.

Marginal spines may be modified, as when one or a series overarches the frontal membrane. One major fossil group (with a few extant species) has a porous, protective frontal shield formed by the fusion of such spines.

Most cheilostomes brood their embryos in special external chambers of standard plan: a hoodlike upfolding from the distal/proximal boundary of two zooids, which may become partly or wholly immersed in or between these zooids. It is called an ooecium and is double-walled, with outer ectooecium and inner entooecium separated by a coelomic lumen. In some species at least, the lumen is confluent with the coelom of the bearing zooid, and the ooecium appears to be a spinous polymorph. However, its development is inconsistent, for example, commencing with paired outgrowths from the proximal zooid or with a single outgrowth from the distal zooid. It is easy to interpret the former as representing the distal pair of marginal spines, especially since these are usually otherwise lacking in ooeciferous zooids. Development from the distal zooid is more difficult to explain, although it should be noted that proximally situated spinelike zooids are not unknown in cheilostomes.

The bryozoan colony is made up from replicated zooids. The simpler polymorphs are vicarious and dispersed through the colony in an ordered or apparently random manner. With the development of adventitious polymorphs, however, a second-order unit, the cormidium, becomes recognizable. Cormidia are groupings of dissimilar polymorphs. Siphonophora (Cnidaria) provide the standard example of colonies with cormidia and it seems generally unappreciated that cheilostomes have cormidia that are at least as complex and probably better integrated. Thus an autozooid may bear spines, an ooecium, adventitious avicularia, and perhaps a vibraculum. Little is known about behavioral coordination in cormidia; much more is known about the metabolic relationships between a female zooid and its ooecium.

 

Reproduction and growth

 

Propagation by statoblasts is important in Phylactolaemata. They develop in large numbers on the funiculi, and are liberated when the colony breaks up. Statoblasts have a protective coat, often a float, and sometimes hooked spines. They are resistant to cold and desiccation and give rise to a new colony under favorable conditions. Nonphylactolaemates in fresh and brackish water may produce resting zooids or hibernacula, and many marine species overwinter as nutrient-filled stolons. Asexual reproduction by fragmentation occurs in a few marine bryozoans, and is said to be important to the free-living sand forms. Lobulation of colonies is characteristic of the more evolved phylactolaemates.

Gonads in bryozoans are associated with the peritoneum: testes on the funiculus, ovaries more often on the zooid wall. Cyclostome spermatozoa develop in tetrads, but in phylactolaemates and gymnolaemates large numbers develop around a common mass, the cytophore. In marine bryozoans (at least) they escape from the body via the mesocoel and the terminal pore in two (the dorsomedial pair) or all of the tentacles. Special male zooids with nonfeeding polypides may be localized in chimneys, thereby taking advantage of the exhalant current to disperse the spermatozoa.

The fertilized egg in phylactolaemates develops in an invagination of the body wall. When released, it is already essentially a motile zooid ready to settle and found a colony. The cyclostome gynozooid is inflated and may occupy much of the colony. Its embryo, having reached the blastula stage, lobulates a series of secondary blastulae, which may repeat the process, until the brood chamber contains 100 or more embryos. Each develops into a simple, ovoid, coronate larva which swims for a short time and then metamorphoses into a proancestrula or incomplete primary zooid. This lengthens and becomes functional.

Sexual reproduction in gymnolaemates follows one of three general patterns. (1) Small eggs are discharged into the sea via the intertentacular organ, an inflated tube situated between the dorsomedial tentacles. Fertilization takes place there. The zygote develops into a planktonic, feeding, triangular, flattened, bivalved larva or cyphonautes. This probably lives for several weeks before it settles. (2) A large, fully yolked egg is produced in the coelom, and extruded through the supraneural coelomopore (replacing the intertentacular organ) into an external brood chamber. If this is an ovicell, the embryo receives no nourishment, for its size is unchanged during development. A nonfeeding coronate larva is liberated. (3) Smallish yolky eggs are transferred to the lumen of an ovicell via the supraneural pore. The ovicell comprises the ooecium, previously described, and an internal membranous extension of the mother zooid, the inner vesicle. The fertilized egg lies between the ooecium and the inner vesicle. The vesicular epithelium, well supplied with funicular strands, hypertrophies where it is in contact with the embryo and becomes a pseudoplacenta. That food is supplied to the embryo is evidenced by its growth during development. A nonfeeding coronate larva is liberated.

The larva responds to light and other stimuli. It achieves limited dispersal and selects a settlement site. Prior to metamorphosis the larva explores a surface with special long cilia; at the moment of attachment a hollow organ, the adhesive sac, is everted, spreads as a disk, and flattens onto the surface. Metamorphosis is total and its details are complex, but the larval organization disappears and a reversed polarity emerges. (Phylactolaemate development does not include this reversal.) The ancestrular polypide differentiates from the upper wall, and colonial budding commences.

The method of budding differs between the three classes. In phylactolaemates new polypide rudiments appear, abanally to the parent, in an ordered manner which determines the branching pattern of the colony. Differentiation of cystids (the zooid walls), insofar as they are present, follows the polypides.

In stenolaemates polypide rudiments also appear first, but are adanal to the parent zooid. Since the cystids are essentially tubular, they grow around the polypide rudiments following division of the longitudinal walls. However, it is important whether these calcified walls meet or remain slightly distant from the terminal epithelium. In the latter case, coelomic confluence remains around their distal end (the double-walled structure), whereas in the former, cystids are separate once formed and communicate only through interzooidal pores.

Gymnolaemate budding is different again, and dependent from the outset on the connecting pores and funiculus. The cystid is produced first, adanally to the mother zooid, and the polypide develops within it.

The pattern of colony formation is termed astogeny. Early on, it is often characterized by sequential change in the size and morphology of the zooids; later astogeny is repetitive, with the production of virtually identical zooids, groupings of zooids, cormidia, or groups of cormidia. The continuous colony in cheilostomes arises from the apposition of repeatedly dividing lines of zooids. The walls between contiguous lines are therefore morphologically double, and the communication pores in them have differentiated from potential zooid buds, which is one reason why they are more complex than the pores in end walls. Frontal budding, of a layer of zooids above the existing layer or layers, may also occur.

Initial formation does not complete the zooid's development. Wall thickening may continue, phases of reproductive activity come and go, while a cycle of polypide aging and renewal continues until senescence. This cycle, in which the whole polypide regresses, and is histolyzed until only a compacted, fibrous “brown body” remains, is peculiar to bryozoans. Old zooids may consist only of an accumulation of brown bodies.

 

Ecology

 

Fresh-water bryozoans are present on submerged tree roots and aquatic plants in most lakes, ponds, and rivers, especially in clear water of alkaline pH. Their presence is best confirmed by dip-netting for statoblasts at the water's edge. Most other bryozoans are marine, although some gymnolaemates inhabit brackish water. They are common in the sea, ranging from the middle shore to a depth of over 26,000 ft (8000 m), and are maximally abundant in waters of the continental shelf. Most attach to firm substrata, so that their distribution is primarily determined by the availability of support. Mud is unfavorable and so is sand unless well provided with stone, dead shells, hydroids, or large foraminiferans, as in regions of strong current, where colony densities may reach 470/ft2 (5000/m2) of hard substrate.

Intertidal bryozoans shun the light, and are found under boulders, below overhangs, and on algae, particularly under conditions of high flow; they avoid turbid water and accumulating sediment. The seaweed dwellers are mainly fleshy ctenostomes and specially flexible cheilostomes, or are very small. Experiments with larvae have demonstrated high selectivity with regard to substrate, for example, algal species or shell surface. Settlement is influenced by texture and contour, with larvae often preferring concavities.

Colony form in bryozoans is to some extent related to habitat. Encrusting and bushy flexible species are adapted to wave exposure; brittle twiglike and foliaceous species are found deeper; some erect branching species tolerate sediment deposition. One group of tiny discoid species lives on sand in warm seas, and in one genus the colonies are so small that they live actually among the sand grains; a few species live anchored by long kenozooidal stems in mud. A number of stolonate ctenostomes bore into the substance of mollusk shells; other species are associated only with hermit crabs, and a few are commensal with shrimps or polychaete worms.

Primarily, however, bryozoans are inhabitants of shaded rock surfaces, where they compete with each other, sponges, and compound ascidians for space. They have no set size or shape, and reproductive capacity is simply a function of size. Some display adaptations, such as raised margins, long spines, or frontal budding, to resist being overgrown. When colonies meet, there is often a mutual cessation of growth, but with different species the one with larger zooids may overgrow its rival or impair its feeding efficiency. Closely related species sometimes display slightly different habitat preferences, thereby avoiding direct competition. Pendent and outgrowing colonies escape the surface competition and become better placed for feeding; they include elegant lace corals and robust fans rising 6–12 in. (15–30 cm) in height.

Bryozoans have few serious predators. Nudi-branch mollusks and pycnogonids (sea spiders) specialize in feeding on zooids but are rarely destructive of entire colonies. Loxosomatids (Entoprocta) and a hydroid (Zanclea) are common commensals.

Life spans vary. Small algal dwellers complete their life cycle in a few months. Many species survive a year but have two overlapping generations; others are perennial, with one known to survive for 12 years.

Bryozoans may be a nuisance in colonizing ship hulls and the insides of water pipes, and one species has caused severe dermatitis in fishers. Recently some delicate kinds have been used in costume jewelry, and green-dyed clumps of dried Bugula are often sold as “everlasting plants.”

John S. Ryland

 

 

Cystoporata

 

Within the Bryozoa is an extinct order, the Cystoporata, in the class Stenolaemata. Cystoporates had encrusting, mound-shaped, or basally attached, erect, calcified colonies made of sheets or branches composed of tubular feeding zooids and extrazooidal vesicular skeletal deposits.

Zooecia, the skeletal tubes delimiting the zooids, in many cystoporates are characterized by lunaria, which are thickened strips that extend up one side of each zooecium. Lunaria commonly have a different degree of transverse curvature than does the rest of the zooecium, and extend somewhat above the general surface of the colonies and arch slightly over the zooecial aperture. Polymorphic zooecia are uncommon and consist of small “space-filling” structures and, less commonly, enlarged, apparently female zooids.

Ceramoporine cystoporates are characterized by laminated wall structure, usually short zooecia, sparse diaphragms, and commonly by gaps of pores in the skeletal walls that may have served for nutrients to move between zooids. These organisms ranged from the Middle Ordovician to the Lower Devonian.

Fistuliporine cystoporates have laminated, granular, or granular-prismatic wall structure, short to long zooecia, and sparse to abundant diaphragms, and lack gaps or pores in the skeletal walls; and in many the extrazooidal vesicular skeletal deposits are replaced outwardly by continuous, dense skeletal material (stereom). Rodlike structures (acanthostyles) may occur in skeletal walls, oriented perpendicularly to the skeletal surface and projecting above the colony surface. These organisms ranged from the Lower Ordovician to the upper Permian.

Cystoporates were exclusively marine and lived in a wide variety of relatively low-energy environments on continental shelves and seas. Both subgroups had diverse growth habits, slightly greater in the fistuliporines. Erect colonies grew as two-layered sheets with zooids growing back to back (bifoliate), as narrow bifoliate branches that bifurcated to form bushes or that anastomosed to form perforated sheets, as radially symmetrical branches that could be several centimeters in diameter, and in other growth habits.

Most cystoporates, except those with narrow branches, have maculae—small, uniformly spaced areas composed of a group of zooecia or a similar-sized spot of extrazooidal skeleton. Maculae may be elevated, depressed, or surrounded by slightly enlarged zooecia that typically tilt away and have lunaria on the side closest to the maculae. Spacing, size, and disposition of zooecia around maculae suggest that they mark points where water, filtered by the surrounding zooids, flowed away from the colony surface in a focused, chimneylike flow, as seen in many living bryozoans with large surface areas.

 

Fossils

 

Fossil Bryozoa have a long geological history, from early in the Ordovician Period [500 million years ago (Ma)] to the Recent (Fig. 1). Individual fossils range in size from a few millimeters to several meters in maximum dimension. Various encrusting or erect growth forms are common, though some were free-living (Fig. 2). Representatives of the marine orders that secreted calcareous skeletons (Cryptostomata, Cyclostomata, Cystoporata, Trepostomata, and Cheilostomata) commonly are abundant in sedimentary rocks formed where benthic organisms flourished. Skeletons generally are calcite, though some are aragonite or mixed calcite and aragonite. Ctenostomata have nonmineralized skeletons, so they have been preserved only as excavations or borings in marine shells or on the undersides of other organisms that overgrew them (a preservation style termed bioimmuration). The fresh-water Phylactolaemata have gelatinous skeletons, but their tough statoblasts (dormant reproductive bodies) have been reported from sediments as old as the Jurassic (at least 150 Ma).

Fossil Bryozoa are most abundant in calcium carbonate–bearing rocks such as various limestones, calcareous shale, and calcareous siltstone, and they are especially common in some alternating thin-bedded limestones and shales. During the Ordovician, Carboniferous, and Permian periods, bryozoans were important parts of many fossil reefs, reef flanks, and other carbonate buildups in shallow (less than 100 m depth) tropical waters. Bryozoans commonly dominate and may reach very high diversities in post-Paleozoic cool-temperate carbonate deposits, indicating a shift in primary environment after the Paleozoic.

In the study of bryozoans, examination with a microscope is necessary. Although colonies of many species are large, the individual skeletons of each zooid (unit of the colony) range from less than 0.1 to about 1 mm in diameter. The smaller diameters are typical for cross sections of elongate tubes that characterize zooids in stenolaemate bryozoans, and the larger diameters are typical for the more equidimensional zooids of cheilostomes. Identification is based on numerous external and, for most stenolaemates, internal features that require study with a microscope. Adequate classification of most stenolaemate bryozoans generally requires variously oriented thin sections through the colony interior (Fig. 2x).

 

Classification

 

Features of the colonial skeletons (zoaria) as well as the morphology of the individual zooidal skeletons (zooecia) are used to classify bryozoans. Many fossil bryozoans had only one type of zooid (autozooids), which apparently could feed and carry out all other necessary biological functions of the colony. Others were polymorphic, with various types of specialized zooids supplementing the autozooids. Number, types, and morphology of polymorphs is important in classification. Other characters important in classification of fossil bryozoans are wall structure, reproductive chambers, general growth habit or specific shape of colonies, and for some, surface topography of the colony.

 

Geological history

 

The earliest bryozoans (representatives of the Cryptostomata, Trepostomata, Cyclostomata, and Cystoporata) are recorded from Lower Ordovician rocks (a few fossils from the Cambrian have been assigned erroneously to the Bryozoa). In Mid-Ordovician time, diverse groups of these various bryozoan orders, including the suborder Ptilodictyoidea of the order Cryptostomata, had a broad geographic distribution (Fig. 4). The phylum continued to evolve rapidly, and toward the end of the Ordovician Period the Trepostomata and the ptilodictyoid Cryptostomata were dominant. The Cystoporata, Cyclostomata, and Ctenostomata were less important faunal elements of the time period.

In the Silurian, the Trepostomata and Cryptostomata were still dominant. New groups diversified in other orders, including the Fenestellina (a suborder of Cryptostomata also referred to as fenestrates), which occurred sparsely in the Late Ordovician. The cystoporates also became a more distinctive part of the bryozoan faunas. Relatively little is known about the Silurian bryozoans of many regions because the principal sedimentary rocks are dolomites and evaporites and the bryozoans are either poorly preserved or they did not inhabit these environments.

Diversity of genera and species further increased in the Devonian Period. Fenestellinid and rhabdomesine cryptostomes were very abundant, and the number of fistuliporid cystoporates increased. The trepostomes continued to be well represented by new species and genera.

The Carboniferous and Permian bryozoans were dominated by various kinds of fenestellinids, rhabdomesines, and cystoporates. The trepostomes were less numerous, and cyclostomes remained uncommon. Toward the end of the Permian Period, almost all trepostomes, cryptostomes, and cystoporates became extinct. This drastic reduction in bryozoan groups extended throughout much of the late Permian and parallels similar patterns in other Paleozoic fossil groups.

Bryozoans are sparse in the Triassic Period. A few cystoporates, trepostomes, rhabdomesines, and cyclostomes occur in Triassic rocks. Representatives of the first three groups are Triassic “holdovers” from the Paleozoic fauna, and the oldest Mesozoic occurrence of cyclostomes is in Upper Triassic rocks.

The Jurassic Period witnessed a great expansion of the Cyclostomata. This order dominated bryozoan faunas until the Late Cretaceous. The Cheilostomata, initially represented by anascans, first appeared late in the Jurassic and rapidly became the dominant bryozoan group, undergoing explosive diversification during mid-Cretaceous. Many of the major cheilostome groups and major evolutionary innovations had developed before the end of the Late Cretaceous.

The cyclostomes continued to evolve a few new families during the Cenozoic Era, but their diversity was reduced by one-third at the end of the Cretaceous and the group has never rebounded. With the exception of the very beginning of the Cenozoic Era (the Danian Stage of the Paleocene Epoch), the Bryozoa of the Cenozoic Era, like the present-day fauna, were principally cheilostomes. Although cheilostome diversity was reduced by over one-fourth at the end of the Cretaceous, the group resumed rapid diversification by the Eocene Epoch (35-55 Ma). Some of the cheilostome groups, such as the cribrimorphs, which flourished in the Late Cretaceous, declined in numbers in the Cenozoic. The anascans, a dominant group in the Cretaceous, continued to maintain their importance in Cenozoic bryozoan faunas and to the present day. The ascophorans diversified especially rapidly during the Eocene, and they maintain high diversity to the present.

Bryozoans have experienced several vigorous radiations and two devastating extinction events. The first adaptive radiation occurred during the Ordovician and involved the Trepostomata and ptilodictyoid cryptostomes, and the second occurred during the Devonian and involved the fenestellinid cryptostomes, which were the dominant bryozoans during the late Paleozoic. All these stenolaemate groups, plus the rhabdomesines and cystoporates, were severely reduced by the end-Permian extinction and were completely extinct before the end of the Triassic Period. A third radiation, which involved only the cyclostome stenolaemates, occurred during the Jurassic, and the cheilostome gymnolaemates had the first of their two radiations during mid-Cretaceous. The end-Cretaceous extinction event strongly reduced the diversity of both cheilostomes and cyclostomes. The cyclostomes never recovered their Late Cretaceous diversity, but by the Eocene cheilostomes were experiencing a renewed interval of vigorous diversification and reached diversity levels higher than those of Late Cretaceous.

 

Evolutionary relationships

 

The fossil records of all orders of the class stenolaemate bryozoans (cyclostomes, cystoporates, trepostomes, and cryptostomes) begin in the Arenigian Stage (478–488 Ma) of the Lower Ordovician, and the soft-bodied gymnolaemate order Ctenostomata is represented back to the Late Ordovician Ashgillian Stage (438–448 Ma) by borings in shells. Thus, there are two problems with using the fossil record to interpret early evolutionary relationships among bryozoans. The first is that earliest representatives of the highly skeletonized stenolaemate orders appear fully differentiated and essentially simultaneously in the fossil record, so relationships among these highly mineralized groups cannot be inferred from the sequence of appearance. The other problem is that the soft-bodied ctenostomes must have had a substantially longer existence than indicated by the fossil record, because the oldest ctenostome fossils are specialized, apparently nonprimitive ctenostomes that left borings in shells. (Most ctenostomes live on surfaces of shells and other substrata and do not excavate chambers.)

Ctenostomes are widely considered to be a paraphyletic group (a group of taxa that contains the ancestar but not all of its descendants) that gave rise to the Stenolaemata during the early Paleozoic and to the cheilostome Gymnolaemata during the Jurassic. One hypothesis about the origin of the Stenolaemata concerns the method of protrusion of the tentacles of zooids to the feeding position. Ctenostomes have a completely flexible body wall. Their only defense against predators is either to remain small and cryptic or to bear allelochemicals, yet their completely flexible body wall can be easily contracted to translate fluid that pushes out the feeding apparatus (analogous with squeezing a toothpaste tube to extrude the toothpaste). Stenolaemates have rigidly calcified lateral body walls, and within the calcified tubular zooids there is a separate, mesodermal “membranous sac” that can be squeezed by transverse parietal muscles to protrude the feeding apparatus. It has been hypothesized that the stenolaemates originated when the ectodermal epithelium of a ctenostome-like ancestor secreted calcite as well as an outer organic membrane, along with separation of the muscle-bearing mesoderm from the ectoderm to form the membranous sac of the proto-stenolaemate. This condition would allow predator-resisting calcification to develop and still permit protrusion and retraction of the feeding apparatus. This evolutionary innovation apparently occurred early in the Ordovician Period, and stenolaemates rapidly diversified into several distinct types that are recognized as orders. Detailed phylogenetic analysis indicates that the Cyclostomata, as traditionally conceived, are paraphyletic and gave rise to the other, essentially Paleozoic, stenolaemate orders.

Origin of the cheilostomes is much clearer. A family of uniserial, encrusting ctenostomes with pyriform zooids is known from bioimmured (entombed while alive) representatives as old as Middle Jurassic; some Jurassic specimens have D-shaped orifices, which is normally a cheilostome rather than a ctenostome attribute. This family (arachnidiid ctenostomes) apparently gave rise to the cheilostomes. The earliest known cheilostomes were Late Jurassic, encrusting colonies of simple, uniserial to loosely pleuriserial, pyriform to elliptical feeding zooids with mineralized lateral walls.

The Phylactolaemata are probably phylogenetically most closely related to the Ctenostomata. At present all phylactolaemates live in fresh water, and their earliest fossils consist of small asexual reproductive bodies found in Jurassic fresh-water deposits. The gelatinous nonmineralized colonies in a fresh-water environment have reduced probability of preservation as fossils. The only other fresh-water bryozoans are some ctenostomes, but it is unclear whether phylactolaemates evolved from fresh-water ctenostomes or whether they originated in the oceans and later migrated into fresh water and then disappeared from the oceans.

 

Evolutionary paleoecology

 

Maximum diversity and abundance of bryozoans has historically been on middle to outer shelves and similar conditions on epeiric sea floors, inferred to be several tens of meters deep. Bryozoan-rich deposits in the Paleozoic were built up by trepostomes, cystoporates, and cryptostomes and developed in shallow equatorial to cold-temperate (midlatitude) environments. However, post-Paleozoic bryozoan-rich deposits were generated early on by cyclostomes and then by cheilostomes, and almost all formed in middle latitudes, seldom in tropical environments. This shift in pattern is probably biologically driven, rather than driven by physical or chemical changes of the world oceans. The “Mesozoic marine revolution” saw the proliferation of several groups of vigorous predators in the tropics, as well as the rise in importance in the tropics of competing organisms such as scleractinian corals and certain algae that grew much more rapidly than bryozoans. While some cheilostomes and a few cyclostomes have reached enormous sizes during the post-Paleozoic, similar large sizes were reached by Paleozoic trepostomes and cystoporates, and on average Paleozoic bryozoans, especially trepostomes and cystoporates, were larger than their post-Paleozoic relatives.

During the Paleozoic, erect growth habits became progressively more abundant; whereas during the post-Paleozoic, encrusting growth habits became progressively more abundant. These contrasting patterns have been interpreted to result in part from an increase in predation during the post-Paleozoic, because slow-growing erect bryozoans cannot as easily recover from partial predation as can encrusting forms. Among erect bryozoans during the Paleozoic and also during the post-Paleozoic, species characterized by narrow, unilaminate branches increased in importance from a trivial percentage to the most numerous. The unilaminate, narrow-branched growth habit allows food–bearing water to be processed much more efficiently than in any of the other colony morphologies, and this efficiency has been inferred to provide an adaptive advantage.

Bryozoans are competitively inferior in overgrowth interactions (so they tend to be overgrawn by other taxa) to most other encrusting organisms such as sponges, ascidians, cnidarians, and algae, and this may have been part of the reason for their relative unimportance in the post-Paleozoic tropics. Among post-Paleozoic bryozoans, cheilostomes consistently have been superior in overgrowth interactions with cyclostomes, due to multiple differences such as, on average, higher growth rates, higher colony margins, and stronger feeding currents in cheilostomes. Simultaneously, cheilostomes have evolved a larger average colony size and have undergone two vigorous stages of diversification (Late Cretaceous and, after recovery from the end-Cretaceous mass extinction, Paleogene), while cyclostomes have declined slowly from their peak diversity in Late Cretaceous and now have on average smaller colony sizes than in the Cretaceous.

The relatively small size of most bryozoan colonies and their slow growth rates, plus the general competitive inferiority of encrusting bryozoans, has relegated them to a minor role in construction of reefs and other organic buildups through geological time. There have been exceptions. During the Mid-Ordovician, encrusting bryozoans were the primary framework builders on reefs and, in many instances, erect bryozoans contributed the bulk of the skeletal debris to the reef flanks. From Silurian through Carboniferous, reef frameworks were locally predominated by bryozoans, and fenestellinid bryozoans grew abundantly on certain organic buildups during the Carboniferous and Permian. In the post-Paleozoic, multilaminar encrusting to massive cyclostome bryozoans built a few small Mesozoic reefs, and cheilostomes similarly built small reefs a few meters wide and high during the Cenozoic. Beyond these exceptions in which reefs were largely or partly built by bryozoans, bryozoans occur widely in reefs as cryptic organisms inhabiting the undersides of corals and small-scale caves.

Throughout their geological history, bryozoans have been much more common on ephemeral substrata that are available for months or years than on persistent substrata that are available for several years and longer (such as reefs). They are widespread, and diverse on brachiopod shells in Paleozoic rocks and on bivalve shells in Jurassic to Neogene deposits. Various life history strategies have evolved to utilize the relatively ephemeral, often mobile shell substrata. Short-lived colonies may live preferentially on undersurfaces of shells and develop only a few zooids before brooding embryos. In contrast, colonies of some species can effectively occupy the entire exposed shell surface and continue to live and expand time after time as the shell or small rock is overturned, so that the original substrate is buried deeply in multiple layers of bryozoan zooids of a colony that can live and function in any orientation with respect to the sea floor.

Repetitive evolution of similar colony morphologies has been the hallmark of bryozoan history. Cheilostomes have evolved unique combinations of characteristics in their successful invasion of soft substrata, where they are either free-lying or live attached by specialized zooids that resemble roots. But otherwise, similar colony morphologies have evolved convergently in many different orders. The limitations on bryozoan morphologies (including constraints on branch sizes and shapes) have been due to the basic organization of bryozoans. Zooids have always been small (almost always much less than 1 mm2 in surface area), feeding bryozoans must be at the colony surface and have access to nutrient-bearing water, and the water that is drawn toward the colony surface must find a nearby outlet away from the colony after it is filtered. Paleozoic stenolaemates collectively, post-Paleozoic cyclostome stenolaemates, and cheilostome gymnolaemates have all developed similar-appearing encrusting, massive, and erect colonies. Consequently, any given bryozoan fossil commonly must be examined closely in order to place it in the correct taxonomic order.

Frank K. McKinney

 

 

Bibliography

 

 

• D. P. Gordon, A. M. Smith, and J. A. Grant-Mackie (eds.), Bryozoans in Space and Time, 1996
• P. J. Hayward, J. S. Ryland, and P. D. Taylor (eds.), Biology and Palaeobiology of Bryozoans, 1994
• A. Herrera and J. B. C. Jackson (eds.), Proceedings of the 11th International Bryozoology Association Conference, 1999
• F. K. McKinney and J. B. C. Jackson, Bryozoan Evolution, 1989
• R. A. Robison (ed.), Treatise on Invertebrate Paleontology, Part G, rev.1983
• alifazeli=egeology.blogfa.com