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Home , Alcyonidium (bryozoan), Alcyonidium diaphanum, Anthozoa, Ascophora, Bryozoa, Callopora

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Zeitschrift/Journal: Denisia

Jahr/Year: 2005

Band/Volume: 0016

Autor(en)/Author(s): Ryland John S.

Artikel/Article: : an introductory overview 9-20 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

Bryozoa: an introductory overview

J.S. RYLAND

Introduction REED (1991) and, comprehensively, by MUKAl et al. (1997), whose survey should be Bryozoa, sometimes called Ectoprocta, consulted by those seeking information on constitute a in which there are zooidal soft-part , cells, and ul- probably more than 8,000 extant trastructure in extant bryozoans of all - (the much quoted figure of 4000, made es. The account also includes much original nearly 50 years ago (HYMAN 1959), is cer- description based on the phylactolaemate tainly a serious underestimate). Some au- Asajirella (formerly ) gelaanosa. thorities regard the phylum to This work essentially provides the English be related to Bryozoa, but the evidence is language update for HYMAN's (1959) classic conflicting and opinion divided (see text, incorporating a thorough review of 40 NIELSEN 2000). The bryozoans are a widely years' significant research. The linkage of distributed, aquatic, group of the Bryozoa with Brachiopoda and Phoroni- whose members form colonies com- da, as 'lophophorates' (following HYMAN posed of numerous units known as . 1959) may no longer be tenable; certainly, Until the mid 18th century, and particular- the feeding mechanisms may not be as simi- ly the publication of John ELLIS' "Natural lar as once supposed (NIELSEN & RllSGÄRD History of the Corallines" (1755), bry- 1998, and references therein). ozoans, like and hydroids, were re- garded as . This is reflected both in the name of the phylum, which translates as General features: size range ' animals' and in the term 'zoophyte' and diversity of structure which was used by LINNAEUS (1758) to em- Bryozoan colonies vary in size. Among brace both bryozoans and hydroids. Seven- , colonies of Monobryozoon, ty-five years after ELLIS, bryozoan zooids which live between particles of marine sand, were distinguished from those of cnidarians consist of little more than a single feeding by possessing both a mouth and an (DE less than one millimetre in height. BLAINVILLE 1820) and, a decade later, Colonies of the coralline Pentapcrra of EHRENBERG (1831) formalized the distinc- European , however, can reach 1 m or tion by introducing the names Bryozoa and more in circumference; in the warm-water . Bryozoans are separated into Zoobotryon, which hangs from harbour pil- three classes: (freshwater ings, and the phylactolaemate Pectinateüa, dwelling); (exclusively ma- massive colonies may exceed 0.5 m in diam- rine); and Gymnolaemata (mostly marine). eter. Colonies that form crusts generally cov- The (class Gymno- er only a few square centimetres; erect laemata), containing over 600 genera, is the colonies may rise only 2-5 cm, though the ge- most successful bryozoan group. General ac- latinous Akyonidium (Fig. 1), washed ashore counts of the phylum have been provided by during autumn gales, may exceed 15 cm. CORI (1941), HYMAN (1959), BRIEN (1960), RYLAND (1970), and WOOLLACOTT & ZIM- The texture of colonies is variable. Some, MER (1977), though all are now, in certain especially in and on seashores, are respects, outdated. More specific but impor- gelatinous or membranous; others are tufted, tant reviews have been provided by RYLAND with flat, leaf-like or whorls of slender Denisia 16, zugleich Kataloge (1976a), MCKINNEY & JACKSON (1989), der OÖ. Landesmuseen branches, whose horny texture results from Neue Serie 28 (2005), 9-20 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at

opens into a digestive tract that is divided into several regions and terminates at an anus, which is outside (but near) the tenta- cles (hence the name alternative name Ec- toprocta, meaning 'outside anus'). If zooids are disturbed, they withdraw their inside the . Only if the zooids have transparent walls, as in the gymnolae- mate genera Eowerbanlaa and Membranipo- ra, is the digestive tract visible. The internal living parts of each zooid - i.e., the nervous and muscular systems, the tentacles, and the digestive tract - are called the polypide, while the surrounding walls and their asso- ciated tissues constitute the cystid (Fig. 2).

Form and function: zooids

Fig. 1: Erect, gelatinous colonies of lightly calcified zooid walls. Still other Although zooid appearance and struc- diaphanum (). colonies are hard and have strongly calcified ture vary considerably from class to class, Many zooids in the colonies contain . Such colonies may form rough-sur- and even between orders, all conform to a clusters of developing oocytes and/or larvae in zooidal brood chambers derived faced patches or may rise in slender branch- common basic plan (Fig. 2). The predomi- from the sheath. Scale bar 5 x 1 ing twigs (such as those that form a network nant, feeding zooid in a bryozoan is cm. Origin: west coast of Scotland, Junde in the 'lace corals', e.g. Reteporelia). the autozooid. Autozooids are rarely longer 1998. than one millimetre and the primitive shape The colonies, diverse and complex in appears to have been cylindrical (as e.g. in structure, are composed of individual mod- Fig. 6). The is external, ranging ules, or zooids, each of which has consider- from a thin cuticle to a thick, calcified lay- able individuality. A bryozoan colony usual- er. The tentacles, collectively termed the ly has many zooids, which may be of one , can be raised above the zooid type or of types that differ both functionally on a slender extension of the body wall (the and structurally. Neighbouring zooids are usually firmly joined and communicate via introvert or tentacle sheath clearly apparent tiny pores in the dividing walls. Zooids ca- in Fig. 6) and outspread for feeding. If dis- Fig. 2: A stained zooid of pable of feeding have a protrusible ring of turbed, the tentacles can be withdrawn into membranacea, the polypide brown and slender tentacles at their distal end, on the body cavity in a movement that in- the cystid walls pale. Mural pore chambers which are found cilia that propel tiny parti- volves inrolling the tentacle sheath, with can be seen (Preparation made by Dr. the mouth and tentacles being pulled down Genevieve Lutaud). cles of food toward the mouth. The mouth within it by the action of paired retractor muscles. Eversion of the withdrawn tenta- cles is effected by raising the hydrostatic pressure of the body fluid, so compressing the tentacle sheath; but the precise mecha- nism differs from class to class. Phylactolae- mates have a muscular and contractile body wall to achieve this function; in gymnolae- mates the wall is non-muscular but in whole or part flexible, so that it can be pulled in- ward by the body musculature associated with it (parietal muscles). In most extant gymnolaemates the zooids are not cylindri- cal but flat, with rigid side walls as seen in Fig. 9. The upward facing or frontal wall ei- ther remains flexible or has concealed below its calcified surface a membranous cavity,

10 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at the ascus (sac), which can be inflated with to the autozooids, as in Schizoporelia. In water, thereby compressing the body flu- the avicularia are movable on short id. At the free end of a cylindrical zooid or stalks and closely resemble miniature birds' near the distal end of a flat zooid is an open- ; hence the name avicularium (cp. ing known as the orifice, through which the contribution of WÖSS, this volume). An- tentacle sheath and tentacles emerge; in other specialized form of zooid is the vibrac- cheilostome gymnolaemates the orifice has ulum, in which the operculum has become a a closable lid, the operculum. Stenolaemate whip-like seta. The functions of avicularia zooids are different, and the walls form a and vibracula are not clearly known, but slender tube, no part of which both types of zooids may help to keep the can be inflected to evert the tentacles; in- colony free from particles and epizoites (i.e., stead, body fluid is forced from one part of organisms that attach to the surface of the the zooid to another by muscles (NIELSEN & colony but do not parasitize it). A recent PEDERSEN 1979). summary may be found in McKlNNEY & JACKSON (1989). The alimentary canal forms a deep loop (Fig. 2); the , ciliated distally, de- scends to the stomach, the anterior part of Form and function: colonies which is termed the cardia or forms a Despite their ill-defined shape, colonies, in a few genera, such as the gymnolaemate at least in extant bryozoans, are not just ag- Bowerbankia (MARKHAM & RYLAND 1987); gregations of zooids but whole organisms the main stomach section is the caecum, having a physiology and behaviour that ap- and the slender posterior region, which is pear to be coordinated to some extent. Inte- ciliated, the pylorus; the rectum continues gration is made possible by a system of in- from the pylorus; and the anus is situated terzooidal pores (Fig. 2) and the cells that just outside the lophophore. A detailed and traverse them (see BOBIN 1977 and MUKAI fully illustrated account of the lophophore et al. 1997 for details). Most conspicuous are and gut has been provided by MUKAI et al. those of the funiculus, which in gymnolae- (1997). Respiratory, circulatory, and excre- mates becomes a colonial network capable tory systems are absent in bryozoans. The re- of distributing nutrients to nonfeeding productive organs (, testes) are situat- zooids (such as ovicells or gonozooids) or ar- ed on the lining of the body wall or on the eas (such as the growing edge). The zooidal funiculus, a cord of tissue that links the of bryozoans consists of a stomach to the lining of the body wall (and small ganglion positioned between the often also links zooids throughout the mouth and the anus that supplies nerves to colony, see below). The polypide degener- the various organs. In some bryozoans a ates periodically during the lifetime of a colonial network, that unites the zooids zooid, and a compact mass, called a brown through the interzooidal pores, has been body, is either expelled or remains alongside demonstrated. A stimulus that causes the the new polypide which soon differentiates lophophore to withdraw in a zooid of the from living cells of the cystid (GORDON gymnolaemate Membranipora almost instan- 1977). taneously evokes the same response nearby; and nerve impulses can at that time be Zooid polymorphism exists among recorded. Nevertheless, to a large extent the cheilostomate colonies in particular, having colony is not individualistic; for example, it given rise to several types of heterozooid usually has no definite shape, can grow in (SlLEN 1977). The operculum seems to have any direction, and can be partially destroyed been significant in the of some without harm to the rest. It may live a few types of specialized zooids in this order. The months or a couple of years, or it may be avicularium type of zooid has a small body theoretically immortal, its of continual and a rudimentary polypide; the operculum, terminated only by some catastro- however, is proportionally larger, has strong phe. The high of bryozoans adductor muscles, and has become, in effect, and the remarkable adaptive radiation of a jaw. Avicularia are found among normal the Cheilostomatida during the zooids, but usually are smaller and attached

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reproduction, topics that have been ex- plored by MCKINNEY & JACKSON in their book "Bryozoan Evolution" (1989).

Reproduction and life cycles

Bryozoans, like other modular animals, have a life cycle that incorporates phases of asexual and (Fig. 4). in larger invertebrate animals (e.g., sea anemones) may, by , produce genetically identical progeny, which separate to form clones. In bryozoans, as in hydroids and corals, the progeny (the zooids) are produced by asexual budding and almost invariably remain in intimate con- tact, giving rise to a colony. Some bryozoan Fig. 3: Erect, foliose colony of and Tertiary, have been attributed by RY- species, however, also propagate colonies foliacea (Cheilostomatida) supporting LAND (1979) to the unique combination of asexually. The cheilostome Discoporella colonies of (: white) as small, non-attached, saucer-like colonies and Scrupocellaria (Cheilostomatida: zooidal individuality combined with a so- brown). No source information; frame size phisticated system for metabolic integration on the sea floor. Groups of zooids at the approximately 9 x 6.5 cm. (provided by the funiculus-interzooidal pore colony rim detach at special fracture zones system), which have facilitated the evolu- and grow into new colonies. The statoblasts tion of heterozooids and replicated patterns (dormant buds) of freshwater bryozoans of heterozooids - which may be interzooidal constitute another means of asexual repro- or variously aggregated on a bearer auto- duction, and probably evolved initially as a zooid to form cormidia BEKLEMISHEV (1969) means of surviving adverse conditions (e.g. Fig. 4: Life cycle in Celleporella (a cheilo- - that make up a colony. The several dis- winter or drying out) in situ rather than for stomate). Reading clockwise from the left, dispersal. Asexual reproduction typically, tinctive basic patterns evolved by colonies the diagram shows an ancestrula, the whether leading to a clone, a colony, or a pattern of early budding, a selection of of Bryozoa (encrusting crusts, erect fronds, clone of colonies, is a means of perpetuating fully developed zooids (autozooids, small spirals, free-living disks, and so on (Fig. 1,3) males, and ovicellate females), and the and locally increasing a successful genetic are related to the habitats they occupy, and coronate (Various sources, from constitution (genotype) rather than one for RYLAND 1989). to the requirements of obtaining food and of colonising new territories (WILLIAMS 1975).

Budding. A bryozoan colony originates from either a primary zooid (ancestrula) or a statoblast. The ancestrula is formed by the of a sexually produced larva (ZlMMER & WOOLLACOTT 1977). The ances- trula is frequently smaller and/or morpholog- ically different from the budded zooids (Fig. 4). New zooids bud from the ancestrula to produce colonies of definite or indefinite shape and characteristic growth habit (ZlM- MER & WOOLLACOTT 1977). The process of colony formation and differentiation is known as astogeny (in contrast to the mor- male phogenesis and ageing of a zooid, which is ontogeny). Early astogeny often progresses through a gradation of metric or morpholog-

feeang ZOOKS ical changes until the typical (ephebic, see RYLAND 1970) zooid form is achieved (BOARDMAN & CHEETHAM 1969, 1973). In phylactolaemates, the primitive zooids are

12 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at cylindrical in form, and astogeny results in a hermaphroditic (i.e., both male and female branched colony. In more highly evolved reproductive organs occur in the same phylactolaemates, colonies are more com- zooid); small are attached in clusters pact, and discrete zooids can be recognized to the membrane that lines the body wall or only with difficulty. New polypides, which the polypide. In a few species the individual originate by ingrowth of the superficial zooids are of one sex only. In these circum- layer, or , remain suspended with- stances, female zooids are usually larger in a common colonial , or body cavi- (e.g., in the cheilostomate Repmdeoneüa), ty (generally regarded as a coelom). Among male zooids may be simpler or just have few- living members of the primitive (and mainly er tentacles in the lophophore (e.g., in the ) marine stenolaemates, the long and ctenostomate Alcyonidium nodosum and the slender zooids have calcified tubular skele- cheilostomate Hippoporidra (RYLAND 2001), tons. A larva metamorphoses into a hemi- or female and male reproductive zooids each spherical primary disk (pro-ancestrula). A may be distinguishable from ordinary feed- cylindrical extension grows from the pro-an- ing zooids (e.g., in the cheilostomate Cdie- cestrula, and the matrix of the colony then is poretia, Fig. 4). are discharged built up by repeated divisions of the zooidal through the terminal pore found in all ten- walls. Internal walls of the colony are called tacles, or just through the dorso-medial pair septa. The growth and budding zones of the (between and below which the nerve gan- colony are found at its outer edges. Cells glion is situated), and must be dispersed from the surface epithelium push inward to through the enveloping water before enter- produce the polypide, and the septa create a ing another zooid (SlLEN 1972). Experimen- chamber (cystid) around it. In the gymno- tal evidence is accumulating that cross, or laemates, in which the zooids frequently are between colony, fertilization is the norm for flattened, budding occurs as transverse septa bryozoans, irrespective of the mode of em- form and cut off parts of the primary zooid bryonic development (RYLAND & BlSHOP (or any other parent zooid). As each bud en- • 1993; TEMKIN 1996; HUGHES et al. 2002). larges to become a zooid, a polypide forms Among living stenolaemates most zooids inside. In the order Cheilostomatida, bud- contain only testes. The few female zooids ding usually produces rows of identical enlarge to form spacious brood chambers, zooids that radiate from the primary zooid. which are called gonozooids. During devel- The rows divide periodically to keep pace opment, a remarkable form of asexual bud- with the increasing circumference of the ding () takes place: young em- colony and to maintain 'hexagonal close bryos squeeze off groups of cells that form packing' organisation that maximizes the secondary ; these in turn may form number of feeding per unit area tertiary embryos. In this way, many larvae (THORPE & RYLAND 1987). Successive can develop in a single brood chamber. The zooids in a row are separated by transverse unique features of reproduction in stenolae- septa, but adjoining rows are separated by mates may be related to the usually small double walls. Interzooidal pores are present size of both zooids and colonies, resulting in both in the walls and in the septa (Fig. 2). scarcity of sperm (RYLAND 1996, 2000).

Sexual reproduction. Sexual reproduc- Among the phylactolaemates, the fertil- tion, by the production and subsequent fis- ized develops in an internal sac; sion of , generates the genetic vari- a larva, which already contains the' first ability necessary for a species to survive in a polypide, is formed there, then liberated. habitat that varies from place to place and Phylactolaemates also produce asexual sta- from time to time (WILLIAMS 1975; RYLAND toblasts, which develop on the funiculus, a 1981; JACKSON 1986). As the colony con- cord of tissue that links the stomach to the tinues its growth by budding, some zooids lining of the body wall. As it grows, each become sexually mature, producing and statoblast is surrounded by a hard protective spermatozoa. Fertilized eggs develop into case that may also include an air-filled float larvae (Fig. 4), which disperse and found and slender, hooked spines. Statoblasts usu- new colonies. Mature gymnolaemate and ally develop in late summer and are liberat- phylactolaemate zooids are most commonly ed as the colony disintegrates with the ap-

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zooid (OSTROVSKY & SCHÄFER 2003) - in which the embryo develops (Fig. 5). The egg at transfer generally has sufficient to nourish its ; but in the cheilostomes Bugula and Celleporella the egg, which is small at transfer, establish- es a pseudo- with tissues of the mother zooid and receives nourishment as the embryo develops (general review by STROM 1977). The ciliated larvae, sub- spherical and often about 0.25 mm in diam- eter, are liberated when fully developed and may swim first toward the light and thus away from the parent colony; later, howev- er, the larvae avoid light as they seek a place in which to settle (RYLAND 1976b, 1977). Metamorphosis of larvae to adults occurs within a few hours after larvae are liberated Fig. 5: Encrusting colony of proach of winter. Statoblasts survive dry and (metamorphosis and early astogeny re- unicornis (Cheilostomatida). Many zooids in freezing conditions and can initiate a new viewed by ZIMMER & WOOLLACOTT 1977). the central band support ovicells, a colony when favourable climatic conditions majority containing pinkish-red embryos. In certain genera (e.g., Membrarüpora and Frame approximately 18x12 mm. Origin: recur. some species of Alcyonidium) of the class west coast of Scotland, May 1996. In most gymnolaemates one oocyte at a Gymnolaemata, each zooid sheds many tiny, time enlarges and bursts from the ovary into fertilized eggs directly into the sea. These de- the coelom, probably then being fertilized velop into oval or triangular, bivalved larvae, by exogenous sperm already present. The known as cyphonautes, which for several oocyte grows and is transferred to a brood weeks live among, and feed on, . Larvae from brood chambers (termed 'coro- chamber. This may be an undifferentiated nate') and cyphonautes settle in a similar part of a zooid; in some ctenostomates, for way; i.e., both locate a suitable surface and example, one or more late oocytes pass explore it with sensory cilia (R.YLAND 1976b). through the supraneural pore into a space Attachment is achieved by flattening a sticky created by the tentacle sheath (as in Fig. 1). Fig. 6: Cylindrical zooids of Bowerbankia holdfast, which pulls the larva down on top imbricata (Ctenostomatida) with expanded Usually among cheilostomates, however, of it. As metamorphosis proceeds, larval or- lophophores. Scale not recorded but each oocyte passes into a special globular or expanded zooids are about 0.25 mm ganization degenerates and the first polypide hooded ovicell (or ooecium) - usually, if not diameter. Origin: west coast of Scotland, develops - with reversed polarity - inside the May 1985. invariably, produced from the next distal primary zooid (RYLAND 1976b, 1977; ZlMMER & WOOLLACOTT 1977).

Food and feeding Bryozoans feed on minute planktonic particles that are captured by the (8-30) ten- tacles, which, in marine species, spread as a funnel with the mouth at its vertex (Fig. 6, 7, 9). The beating of long lateral cilia draws water into the top of the funnel and propels it out between the tentacles. Particles are projected toward the mouth; it was suggested by STRATHMANN (1973) that those leaving the funnel between the tentacles would be flicked back into it by reversed beat of the lateral cilia, though some of STRATHMANN'S interpretations were unsupported by the

14 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at work of BEST & THORPE (1983). Recent work suggests, moreover, that the lateral cil- ia function more as passive sieves (RllSGÄRD & MANRJQL'EZ 1997; NIELSEN &. RIISGÄRD 1998; LARSEN & RllSGÄRD 2002). More study on mechanisms is needed. Shorter cil- ia on the inner face of the tentacles may as- sist in the transport of food particles toward the mouth without the involvement of mu- cus; from there they are sucked into the pharynx. shell valves are separated or broken in the gizzard, when present (MARKHAM & RYLAND 1987). Digestion and absorption occur in the stomach, and indi- gestible remains are compacted by rotation and expelled as faecal pellets. Freshwater bryozoans generally have more tentacles, dis- posed in a crescentic lophophore, the ends of which project behind the mouth. VSKY (2002). In a further development, tor Fig. 7: Encrusting colony of Flustrellidra example in species of Hippoporidra and in the hispida (Ctenostomatida) with expanded The bryozoan method of feeding, espe- lophophores. Coast of Wales but no further ctenostomate Alcyonidium nodosum, the hy- details recorded; the expanded lopho- cially in extensively spreading colonies of drodynamic system evolved to promote feed- phores have a diameter of about 1 mm to optimally packed zooids, imposes colonial ing efficiency has been utilized in reproduc- the point of out-curving (bright in the organization as well as appropriate zooidal tion. In both bryozoans the zooids are single photograph). behaviour. Filtered water accumulates below sex rather than hermaphroditic, and small Fig. 8: Colony of Membranipora the expanded lophophores, which are held male zooids are clustered on the summits of membranacea (Cheilostomatida) on a above the colonial surface. Hydrodynamics the mammillae, so that sperm are discharged (Laminaria) . The direction of growth requires that this water, very viscous at the is to the right, bounded by a wide in the strong outflow (RYLAND 2001). marginal budding zone (rapid growth scale of individual zooids and often far from rate). In the older part the regularly spaced the colony margin, be removed without di- darker spots indicate the positions of luting the food-bearing inflow (GRÜNBAUM exhalant chimneys (see text). Actual size 1995; LARSEN & RIISGÄRD 2001). The solu- not recorded. Locality: Shetland, June 2001. tion has been the formation of regularly spaced 'exhalant chimneys' first described in the flat spreads of Membranipom (BANTA et al. 1974; LARSEN & RIISGÄRD 2001; Fig. 8, 9). Each 'chimney' is essentially a space, sometimes centred on a non-functional zooid (Fig. 9), enlarged by the divergent pos- ture of the surrounding lophophores. Exha- lant water enters the base of the 'chimney' and outflows to well above the height of the surrounding lophophores. The efficiency of the system is often enhanced, as in the cheilostomate genus Hippoporidra, by the colony surface being regularly mammillated, each summit coinciding with and elevating the 'chimney'. The colony-wide to feeding have been comprehensively re- viewed by MCKINNEY & JACKSON (1989), though further important contributions to our understanding of and the need for and functioning of, chimneys have been made by ECKMAN & OKAMURA (1998), LARSEN & RI- ISGÄRD (2001), and SHUNATOVA & OsTRO-

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Ecology Freshwater bryozoans. Freshwater bry- ozoans live mainly on leaves, stems, and tree roots in shallow water. Before drinking wa- ter was filtered, they regularly polluted wa- ter supply pipes. Though not uncommon, freshwater bryozoans are often inconspicu- ous in pools, lakes, or gently flowing rivers, especially in slightly alkaline water. Marine bryozoans. The most familiar marine bryozoans are those that inhabit shores, though they occur in greater num- bers below tidemarks. Dredge hauls of stones and shells yield colonies in abundance. Colonies also occur on the bed, even at great depths, but the frequently muddy bottom of the oceanic abyss is an un- Fig. 9: ZOOIÜS ui iviemuranipora Distribution and abundance favourable habitat. A few species tolerate membranacea with expanded lophophores. hypersaline or brackish waters. The predom- At the bottom centre is an "empty" zooid Bryozoan colonies are found in both which will become the focus of a chimney. inantly marine Gymnolaemata have a few fresh and salt waters, most commonly as Zooids measure about 0.4 mm length. freshwater representatives, e.g. Paludicelia. Locality: west of Scotland. growths or crusts on other objects (Fig. 3, Shallow, sheltered channels that have 10). Freshwater bryozoans live among vege- currents but are protected from severe waves tation in clear, quiet, or slowly flowing wa- are typical bryozoan habitats. Open coast- ter. Marine species range from the shore to lines support fewer species, but non-calcare- the ocean depths but are most plentiful in ous species (e.g. of Akyonidium, Bower- the shallow waters of the continental shelf. bankia (Fig. 6) and Flustrellidra (Fig. 7)) oc- They cover seaweeds, form crusts on stones cur abundantly on intertidal in tem- and shells, hang from boulders, or rise from perate waters. A familiar gymnolaemate the seabed. Bryozoans readily colonize sub- genus is Membranipora (Fig. 8), which is merged surfaces, including ship hulls and found throughout the world and is well the insides of water pipes. A few form free- adapted to living on kelp weeds at, and just living or apparently non-attached popula- below, low water mark. Although the zooid tions on sandy seabeds. walls of Membranipora colonies are calcified (Fig. 9), they contain flexible joints, which Fig. 10: Encrusting colony of (Cheilostomatida). This species The zooid walls, which constitute the allow the colony to bend as the alga sways in has a porous frontal wall, a very large most permanent portion of the colony, are the waves. Membranipora, which may cover orifice, and (unusually) lacks ovicells, the generally calcareous, giving bryozoans a fos- large areas with a million or more zooids, al- embryos developing internally. Zooids ways grows predominantly toward the approximately 0.8 x 0.4 mm. Origin: west sil record that dates from the coast of Scotland, May 1985. onward (i.e., from about 500 My ago). youngest part of an algal frond (Fig. 8). Overhangs, which form when soft rock erodes along a shoreline, floating pontoons, and the shaded pilings of jetties and piers, are other favoured habitats. Since bryozoans do not require light and can grow in dark places, they can avoid competition from al- gae that could smother them. Opistho- branch sea slugs and pycnogonids appear to be the principal predators of bryozoans.

Evolution and palaeontology The Bryozoa have a long history. From the Lower Ordovician (500-430 My ago)

16 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at onward, most formations, espe- The ctenostomates (class Gymnolaema- cially those with shale alternations, are rich ta) have left a sparse fossil record. During the in bryozoan . The skeletons of calci- Late they apparently gave rise to the fied bryozoans are easily preserved. Steno- complex and successful cheilostomes. These laemates are abundant fossils; and, after had encrusting flat zooids similar to some of their appearance in the Upper Jurassic (140 their contemporary ctenostomates but with My ago), cheilostomate fossils also are abun- side walls that were calcified. This type of or- dant. The soft-bodied phylactolaemates, on ganization, termed anascan (meaning with- the other hand, have left no fossil record, out an ascus), permitted inflexion of the and fossilized ctenostomates are rare (usual- front wall to evert the lophophore but ly in the form of moulds resulting from im- seemed to offer little protection. The as- muration; VOIGT 1979) but long antedate cophoran (ascus bearing) organization the cheilostomates. evolved in the Late Cretaceous by calcifying The most ancient bryozoans are steno- the membranous front but preserving its hy- laemates from the Lower Ordovician of the drostatic function by a flexible infolding (as- United States and Russia (Arenig series, cus) below the wall. The parietal muscles at- about 499 My old); both cystoporate and tach to the ascus and pull its lower surface in- trepostome stenolaemates have been found. to the coelom to evert the lophophore, while The ceramoporoids, a group belonging to the ascus itself fills with seawater. the order Cystoporata, flourished during the Ordovician and evidently were the progeni- Classification tors of a more advanced group, the fistuli- poroids, which were successful until the end Although both colony type and zooid of the (280-225 My ago). morphology are used to classify bryozoans, zooidal characters are more reliable. Howev- Dominant among the early Palaeozoic er, the cylindrical zooids of stenolaemates are (570-225 My ago) stenolaemates, however, of rather uniform appearance, making classi- was the order Trepostomata, which evolved fication difficult; wall structure and the mor- rapidly during the Ordovician and attained phology of the embryo chambers are impor- its peak during the upper part of the same tant taxonomic characters. In cheilostom- period. The long, slender zooids of trepos- ates the skeletal features of the zooids, par- tomes grew together to form large, solid, ticularly the presence, extent, and structure colonies. As a zooid grew longer and longer, diaphragms (or transverse partitions) were of the frontal wall - together with shape of deposited. The trepostomes declined in im- the orifice, type of ooecia, and zooid poly- portance after the Ordovician, perhaps as a morphism - provide the most important dis- result of competition from the cryptostomes, tinguishing taxonomic criteria. A simple di- and were extinct by the close of the Permi- vision of cheilostomates into two suborders, an (225 My ago). Anasca and , is now recognized as being an over-simplification, though these Cryptostomes evolved rapidly during former taxa certainly represent grades of or- the Ordovician. They were similar to the ganization. The Ascophora, in particular, are trepostomes but evolved freely erect, leaf- certainly polyphyletic, the frontal wall-sub- like, branching or lacy colonies in the ptilo- mural ascus combination having evolved in dictyoids, or branching in rhabdomesoids, a number of separate ways (GORDON 2000). and were the dominant bryozoans from the Among ctenostomates and phylactolae- start of the until the Permian mates, whose zooids lack skeletal features, (395-225 My ago). For reasons not yet clear, colony form is more important. Statoblasts the cryptostomes dwindled and became ex- are of taxonomic value. Internal characters tinct soon after the end of the Palaeozoic have been used less but, in ctenostomates, Era (225 My ago). the presence or absence of a. gizzard, number The Cyclostomatida arose in the of tentacles, and colour of developing em- Palaeozoic, flourished during the Jurassic bryos are of taxonomic significance. (190-136 My ago) and Lower Cretaceous, and still survive.

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Phylum Bryozoa lophophore; zooids separated by septa; new zooids produced by division of septa; limited Sedentary, aquatic that polymorphism; marine; Ordovician to pres- form colonies of zooids by budding; each ent; about 550 genera. zooid with circular or crescentic lophophore surrounding a mouth from which slender, Order Cyclostomatida ciliated tentacles arise; anterior part of body Orifice of zooid circular; lophophore cir- forming an introvert within which the lo- cular; no epistome; zooids interconnected by phophore can be withdrawn; alimentary ca- open pores; sexual reproduction involves nal deeply looped; anus opening near mouth polyembryony, usually in special reproduc- but outside lophophore; excretory organs tive zooids (gonozooids); all seas; Ordovi- and a blood vascular system absent; each cian to present; about 250 genera. zooid secretes a rigid or gelatinous wall to support colony; at least 8,000 extant species. Order Cystoporata Zooid skeletons long and tubular, inter- The classification of bryozoans began in connected by pores and containing di- 1837 when the freshwater and marine Bry- aphragms (transverse partitions); cystopores ozoa were separated into the classes now (not pores but supporting structures be- known as Phylactolaemata and Gymnolae- tween the zooid skeletons) present; Ordovi- mata: later a third class, Stenolaemata, was cian to Permian; about 80 genera. separated from the Gymnolaemata. The cy- clostomates and the fossil trepostomes were Order Trepostomata placed in the new class (for a recent review, Colonies generally massive, composed see BOARDMAN 2002). In recent years, the of long tubular zooid skeletons with lamel- cryptostomes have also been placed in the late calcification; without interzooidal Stenolaemata. The most satisfactory system, pores; orifices polygonal; sometimes with therefore, separates the bryozoans into three numerous diaphragms, zooid walls thin classes, distinct since the beginning of the proximally, thicker distally; Ordovician to fossil record. Permian; about 100 genera.

Most of the bryozoan orders were named Order many years ago (though the suffixes have Colonies mostly with foliaceous or retic- been changed to accord with a more logical ulate fronds or with branching stems; zooid hierarchy): Cheilostomatida; Ctenostomati- skeletons tubular, shorter than in trepos- da, and Cyclostomatida in 1852; Trepostom- tomes; without pores; with diaphragms; ata in 1882; and Cryptostomata in 1883. proximal portions thin walled, distal por- Cystoporata was introduced in 1964 to in- tions funnel-like, and separated by exten- clude the Palaeozoic ceramoporoids and fis- sive calcification; Ordovician to ; tuliporoids. about 130 genera.

Class Phylactolaemata Class Gymnolaemata Zooids basically cylindrical, with a cres- Zooids cylindrical or squat; with a circu- centic lophophore and an epistome (hollow lar lophophore; no epistome; body wall flap overhanging mouth); body wall non- sometimes calcified; non-muscular; eversion calcareous, muscular, used for averting the of lophophore dependent on deformation of lophophore; coelom continuous between body wall by extrinsic muscles; zooids sepa- zooids; new zooids arising by replication of rated by septa or duplex walls; pores in walls polypides; special dormant buds (stato- plugged with tissue; new zooids produced blasts) are produced; zooids monomorphic; behind growing points by formation of exclusively freshwater; cosmopolitan; appar- transverse septa; polymorphic; mainly ma- ently primitive, but with no certain fossil rine; all seas; probably Ordovician to pres- record; about 12 genera. ent; abut 650 genera.

Class Stenolaemata Order Ctenostomatida Fossil except for some Cyclostomatida; Zooids cylindrical (Fig. 6) to flat; walls zooids cylindrical; body wall calcified, with- not calcified; orifice terminal or nearly so, out muscle fibres; not used for everting the often closed by a pleated collar; no ooecia or

18 © Biologiezentrum Linz/Austria; download unter www.biologiezentrum.at avicularia; Ordovician (on basis of immured ECKMAN J.E.& OKAMURA B. (1998): A model of parti- casts; see VOIGT 1979) to present; about 40 cle capture by bryozoans in turbulent flow: significance of colony form. — Amer. Nat. genera. 152:861-880. Order Cheilostomatida EHRENBERG G.C. (1831): Symbolae physicae, seu Zooids generally shaped like a flat box, icones et desciptiones corporum naturalium. — Zoologica. 4, Animalia Evertebrata exclusis walls calcified; frontal membranous (Fig. 9) Insectis. Berolini. or calcified (Fig. 10); orifice frontal; closed ELUS J. (1755): An Essay Towards a Natural History by a hinged operculum; specialized zooids, of the Corallines. — Published by the author, such as avicularia, commonly present; em- London: 1-103. bryos often developing in ooecia (ovicells or GORDON D.P. (1977): The aging process in bry- brood chambers). Upper Jurassic to Present; ozoans. — In: WOOLLACOTT R.M. S R.L. ZIMMER at least 600 genera.. A simple subdivision (Eds.): Biology of Bryozoans. Academic Press, into suborders Anasca and Ascophora is no New York: 335-376. longer sustainable. GORDON D.P. (2000): Towards a phylogeny of cheilostomes - morphological models of frontal wall/shield evolution. — In: HERRERA th References CUBILLA A. & J.B.C. JACKSON (Eds.): Proc. 11 In- tern. Bryozool. Association Conf.. Smithson- BANTA W.C., MCKINNEY F.K. & R.L ZIMMER (1974): ian Tropical Research Institute, Balboa, Re- Bryozoan monticules: excurrent water out- public of Panama: 17-37. lets? — Science, N.Y. 185: 783-784. GRÜNBAUM D. (1995): A model of feeding currents BEKLEMISHEV W.N. (1969): Principles of Comparative in encrusting bryozoans shows interference of Invertebrates. 1. Promorphology. between zooids within a colony. — J. Theo- — Oliver & Boyd, Edinburgh: 1-490. ret. Biol. 174: 409-425.

BEST M.A.& J.P. THORPE (1983): Effects of particle HUGHES R.N., WRIGHT P. & P.H. MANRIQUEZ (2002): Pre- concentration on clearance rate and feeding dominance of obligate outbreeding in the si- current velocity in the marine bryozoan Flus- multaneous Celleporella trellidra hispida. — Mar. Biol. 77: 85-92. hyalina senso lato. — In: WYSE JACKSON P.N., BOARDMAN R.S. (2002): Colony life then and now: BUTTLER C. & SPENCER JONES M.E. (Eds.): Bry- Lower trrepostomes (500-300 mya) ozoan Studies 2001. Proc. 12th Intern. Bry- and living cyclostomes: a review. — In: WYSE ozool. Assoc. Swets & Zeitlinger, Lisse: 159- JACKSON P.N., BUTTLER C. & SPENCER JONES M.E. 162. (Eds.): Bryozoan Studies 2001. Proc. 12th In- HYMAN L.H. (1959): The Invertebrates: Smaller tern. Bryozool. Assoc. Swets & Zeitlinger, Coelomate Groups. — McGraw-Hill, New Lisse: 41-51. York: 1-783.

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NIELSEN C. (2000): The phylogenetic position of En- RYLAND J.S. & J.D.D. BISHOP (1993): Internal fertilisa- toprocta and Ectoprocta.— In: HERRERA CUBILLA tion in hermaphroditic colonial invertebrates. A. & JACKSON J.8.C. (Eds.): Proc. II«1 Intern. — Oceanogr. Mar. Biol. Ann. Rev. 31:445-477. Bryozool. Conf. Smithsonian Tropical Re- SHUNATOVA N.N. & A.N. OSTROVSKY (2002): Group au- search Institute, Baiboa: 66-73. tozooidal behaviour and chimneys in marine NIELSEN C. & K.J. PEDERSEN (1979): Cystid structure bryozoans. — Mar. Biol. 140: 503-518. and protrusion of the polypide in Crisia (Bry- SiliN L. (1972): Fertilization in the Bryozoa. — ozoa, ). — Acta Zool. (Stockh.) Ophelia 10: 27-34. 60: 65-88. SILEN L. (1977): Polymorphism. — In: WOOLLACOTT NIELSEN C.& H.U. RIISGARD (1998): Tentacle structure R.M. & R.L. ZIMMER (Eds.): Biology of Bryo- and filter feeding in Crisia eburnea and other zoans. Academic Press, New York: 184-231. cyclostomatous bryozoans, with a review of upstream collecting mechanisms. — Mar. STRATHMANN R.R. (1973): Function of lateral cilia in Ecol. Prog. Ser. 168: 163-186. suspension feeding of lophophorates (Bra- chiopoda, Phoronida, Ectoprocta). — Mar. Bi- OSTROVSKY A.N. & P. SCHÄFER (2003): Ovicell struc- ture in dumerilii and C. lineata ol. 23: 129-136. (Bryozoa: Cheilostomatida). — Acta Zool. STRÖM R. (1977): Brooding patterns of bryozoans. (Stockh.) 84: 15-24. — In: WOOLLACOTT R.M. & R.L. ZIMMER (Eds.): Bi-

REED C.G. (1991): Bryozoa. — In: GIESE A.C., PEARSE ology of Bryozoans. Academic Press, New J.S. & V.B. PEARSE (Eds.): Reprod. Mar. Inverte- York: 23-55. br. 6. Boxwood Press, Pacific Grove: 85-245. TEMKIN M.H. (1996): Comparative fertilization biol- RIISGARD H.U.& P. MANRIQUEZ (1997): Filter-feeding ogy of gymnolaemate bryozoans. — Mar. Bi- in fifteen marine ectoprocts (Bryozoa): parti- ol. 127: 329-339. cle capture and water pumping. — Mar. Ecol. THORPE J.P. & J.S. RYLAND (1987): Some theoretical Prog. Ser. 154: 223-239. limitations on the arrangement of zooids in RYLAND J.S. (1970): Bryozoans. — Hutchinson, Lon- encrusting Bryozoa. — In: Ross J.R.P. (Ed.): don: 1-175. Bryozoa: Present and Past. Western Washing- ton University, Bellingham: 277-283. RYLAND J.S. (1976a): Physiology and ecology of ma- rine bryozoans. — Adv. Mar. Biol. 14: 285-443. VOIGT E. (1979): The preservation of slightly on non-calcified fossil Bryozoa (Ctenostomata RYLAND J.S. (1976b): Behaviour, settlement and ands Cheilostomata) by bioimmuration. — In: metamorphosis of bryozoan larvae: a review. LARWOOD G.P & M.B. ABBOTT (Eds.): Advances in — Thalass. jug. 10: 239-262. Bryozoology. Academic Press, London: 541- RYLAND J.S. (1977): Taxes and tropisms of bry- 564. ozoans. — In: WOOLLACOTT R.M. & ZIMMER R.L (Eds.): Biology of Bryozoans. Academic Press, WILLIAMS G.C. (1975): Sex and Evolution. — Prince- New York: 411-436. ton University Press, Princeton: 1-200. WOOLLACOTT R.M. S R.L. ZIMMER (1977): Biology of RYLAND J.S. (1979): Structural and physiological as- pects of coloniality in Bryozoa. — In: LARWOOD Bryozoans. — Academic Press, New York: 1- G.P. & B.R. ROSEN (Eds.): Biology and Systemat- 566. ics of Colonial Organisms. Academic Press, ZIMMER R.L. S R.M. WOOLLACOTT (1977): Metamor- London, New York: 211-242. phosis, ancestrulae, and coloniality in bry- RYLAND J.S. (1981): Colonies, growth and repro- ozoan life cycles. — In: WOOLLACOTT R.M. & R.L. duction. — In: LARWOOD G.P. & NIELSEN C. (Eds.): ZIMMER (Eds.): Biology of Bryozoans. Academ- Recent and Fossil Bryozoa. Olsen & Olsen, ic Press, New York: 91-142. Fredensborg: 221-226. RYLAND J.S. (1989): Moss animals: Phylum Bryozoa. — The New Encyclopaedia Britannica - Macropaedia: Knowledge in Depth 24: 375- 379(1986). RYLAND J.S. (1996): Polyembryony 'paradox': the case of cyclostomate bryozoans. — Trends Ecol. & Evol. 11:26.

RYLAND J.S. (2000): Gonozooid placement and branching patterns in some species of Crisia Address of author: (Cyclostomatida). — In: HERRERA CUBILLA A. & J.B.C. JACKSON (Eds.): Proc. 11th Intern. Bryozo- John S. RYLAND ol. Conf. Smithsonian Tropical Research Insti- Emeritus Professor of tute, Balboa: 343-354. School of Biological Sciences RYLAND J.S. (2001): Convergent colonial organiza- University of Wales Swansea, tion and reproductive function in two bry- ozoan species epizoic on gastropod shells. — Swansea SA2 8PP, U.K. J.Nat. Hist. 35: 1085-1101. E-Mail: [email protected]

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