AccessScience from McGraw-Hill Education Page 1 of 9 www.accessscience.com

Demospongiae

Contributed by: Klaus R utzler,¨ Willard D. Hartman

Publication year: 2014

A class of the phylum Porifera, including with a skeleton of one- to four-rayed siliceous spicules or of spongin fibers, or both. Three subclasses can be distinguished: Homoscleromorpha,

Tetractinomorpha, and Ceractinomorpha. Several genera lack a skeleton, and it is through a study of these seemingly primitive forms that the complicated structure of most adult Demospongiae may be understood. The

Demospongiae constitute the most abundant and widely distributed group of sponges, occurring in the sea from the tidal zone down to abyssal depths [at least to 5500 m (18,000 ft)]. They contain an estimated 6000 accepted species (85% of all sponges) in about 13 well-defined orders, 88 families, and 500 genera. Three families have invaded freshwater. The species vary in size from thin encrustations that are several centimeters in diameter to huge cake-shaped forms that may measure up to as much as 2 m (6.6 ft) in diameter. Other common shapes are tubular, columnar, arborescent (treelike), cuplike, flabellate (fan-shaped), and excavating (living in galleries bored in limestone). The shallow-water species tend to be more plastic in form than the deep-water species, which usually exhibit little intraspecific variation in shape. See also: PORIFERA .

Biology and morphology

Like most sponges, Demospongiae are filter feeders; however, in this group, at least one family (Cladorhizidae, order Poecilosclerida) occurs that includes carnivorous species. Larvae are mostly parenchymellas, but in some groups they are blastula-like (clavablastulas, cinctoblastulas). Metamorphosis from the larval condition in the

Demospongiae characteristically involves a transitory rhagon stage with a simple leuconoid canal system. During further development, the choanocyte (“flagellated”) chambers are isolated between the inhalant and exhalant canals to produce leuconoid canal systems of varying complexity ( Fig. 1 ).

Ultrastructural studies of the choanocytes and choanocyte chambers of representative genera have revealed differences between the orders of the class. In some genera of the order (now including the suborder Petrosina), belonging to the subclass Ceractinomorpha, the choanocyte chambers lie across the inner ends of the inhalant canals ( Fig. 2 ) and are separated from them by a pinacocyte layer that is perforated beneath the prosopyles to allow water to pass from the inhalant canal into the chamber. Between the chamber and the exhalant canal lies a pore that allows water to escape from the choanocyte chamber into an aphodus (Fig. 1 b ) of the exhalant canal system. This pore is surrounded by a ring of cells (called cone cells from their shape) that are part of the choanocyte chamber. As far as is known at present, this quite complicated structure is restricted to in Haplosclerida. AccessScience from McGraw-Hill Education Page 2 of 9 www.accessscience.com

WIDTH:BFig. 1 Types of leuconoid canal systems. ( a ) Eurypylous chambers opening directly into exhalant canal. ( b ) Aphodal chambers; a narrow canal or aphodus leads from the chamber to the exhalant canal. ( c ) Diplodal chambers; a narrow canal or prosodus intervenes between the inhalant canal and chamber, as well as between the chamber and exhalant canal. Arrows show the direction of water flow.

WIDTH:BFig. 2 Section of choanocyte chamber of ficiformis (Haplosclerida), showing the pathway of water flow from the end of an inhalant canal through the chamber to aphodus.

Skeleton

The skeletal system of Demospongiae consists of siliceous spicules (sclerites), spongin fibers, or both. AccessScience from McGraw-Hill Education Page 3 of 9 www.accessscience.com

WIDTH:BFig. 3 Skeleton formation in Demospongiae. ( a ) Diactinal megasclere forming within sclerocyte. ( b ) Amphidisc in sclerocyte. ( c ) Chela in sclerocyte. ( d ) Sigma in sclerocyte. ( e ) Spongin fiber in the process of formation by spongocyte.

Spicules. The spicules are intracellular secretions of sclerocytes, which are cells derived from archeocytes. Each monaxonid spicule is laid down within a single cell by continuous deposition of hydrated silicon dioxide around an organic axial fiber. Above a minimal concentration of silica in the surrounding medium, the length of spicules is independent of the amount of silica present. However, the thickness of the spicules varies up to a maximal value in correlation with silica concentration. Tetraxonid spicules are apparently also formed in individual sclerocytes. Microscleres are formed in special sclerocytes; they require a higher minimal content of silica for formation than do megascleres ( Fig. 3 ).

Fibrous skeletal elements. The reticulum of prominent spongin fibers that forms the skeleton of members of the order Dictyoceratida (bath sponges and related forms) is composed of a feltwork of collagen fibrils, without periodic striation, laid down by specialized cells called the spongioblasts (Fig. 3 e ). Similar spongin fibers enclose or join together siliceous spicules in sponges of the orders Poecilosclerida and Haplosclerida. Intercellular collagen fibrils occur in Demospongiae as well. Laid down by collencytes, lophocytes, or pinacocytes, these

fibrils have a periodic striation and are oriented in a parallel fashion in loose fascicles.

Homoscleromorph skeletal elements. In species where it occurs, the homoscleromorph skeleton consists of unusual tetractines (calthrops) and their derivatives; they vary in size classes, but cannot be separated into megascleres and microscleres.

Tetractinomorph skeletal elements. Tetractinomorph sponges of the orders Spirophorida and Astrophorida have little or no spongin, and almost always have some tetraxonid siliceous megascleres to which may be added monaxonid AccessScience from McGraw-Hill Education Page 4 of 9 www.accessscience.com

types. When triaenes are present, they usually occur in tracts radiating from the central part of the to the surface.

The order Hadromerida is characterized by a skeleton of monaxonid siliceous megascleres accompanied by varying quantities of spongin. The spicules characteristically occur in tracts radiating from the central regions of the sponge; alternatively, in the case of those with an abundance of spongin, a plumose arrangement is found.

Microsclere types include asters, with numerous rays diverging from a central point; streptasters (spiny rods), often twisted spirally; sigmas; and raphides.

Ceractinomorph skeletal elements. Among the ceractinomorph sponges, spongin tends to be of common occurrence.

In the orders Dictyoceratida (bath sponges), Dendroceratida, and Verongida, spicules are absent and the skeleton is formed of spongin fibers only. In the orders Poecilosclerida and Haplosclerida, varying quantities of spongin occur along with siliceous monaxonid spicules. In some species, a network of spongin fibers occurs in which the spicules are embedded; in others, spongin serves as an interspicular cement. In the order Halichondrida, spongin is rarer in occurrence, but is always present in the form of short tracts or as a cement. The cement helps to unite the irregularly arranged siliceous monaxonid spicules.

Ceractinomorph microscleres are commonly anchor-shaped (chelas), barbell-like (amphidiscs), C- or S-shaped

(sigmas), bow-shaped (toxas), or fine and hairlike (raphides).

Systematics

Comparative studies (in the 1950s) of the embryology and early attached stages of sponges of the class

Demospongiae suggested two evolutionary lines within this group. New data on more species as well as cladistical and molecular studies showed polyphyletic trends that required separation of a third line and indicate possible additional corrections in the future. Thus, three subclasses are so far recognized on the basis of larval morphology, reproductive strategy, and geometry of megascleres and microscleres.

Homoscleromorpha. The Homoscleromorpha subclass (with only one order so far, Homosclerophorida) is distinguished by its larva (cinctoblastula), viviparous mode of reproduction, and tetraxonic siliceous spicules of one or several size classes (but not definable as megascleres or microscleres). The skeletonless Oscarella has a primitive structure. Cleavage results in a solid mass of cells (morula), which later becomes hollow by cytolysis of the interior cells, rich in food reserves. Upon being freed from the parent, the hollow larva is made up of a single layer of flagellated cells and is known as an amphiblastula-like cinctoblastula ( Fig. 4 a ). After a short free-swimming period, the larva attaches to the substrate by its anterior pole and flattens out (Fig. 4 b ).

Gastrulation occurs at this point as the anterior half of the larva invaginates (Fig. 4 c ). The blastopore closes as the edges of the now double-layered larva push together against the substratum (Fig. 4 d ). The internal layer of cells is now thrown into folds that pinch off to form cavities, which will become the flagellated chambers.

Simultaneously, a depression forms in the apical ectoderm and the rudiment of the exhalant canal system appears AccessScience from McGraw-Hill Education Page 5 of 9 www.accessscience.com

WIDTH:BFig. 4 Oscarella (Homosclerophorida). ( a ) Free-swimming cinctoblastula larva. ( b ) Newly settled larva. ( c ) Gastrulation begins by invagination of flagellated hemisphere. ( d ) Later stage of gastrulation; blastopore closing. ( e ) Formation of osculum. ( f ) Young leuconoid stage is formed.

(Fig. 4 e ). The depression deepens to form a cavity, giving off branches that push their way among the flagellated chambers (Fig. 4 f ). The latter finally open into these cavities, which become the exhalant canals. Inhalant canals push in from the surface of the sponge and join the flagellated chambers. The metamorphosed larva of Oscarella assumes the leuconoid grade of construction from the start, with isolated flagellated chambers communicating with inhalant and exhalant canals. The adult Oscarella and a related genus, Plakina , with two-, three-, and four-rayed spicules, retain the simple leuconoid structure. The sponge consists of a folded wall, with each fold made up of a dermal layer and a group of choanocyte chambers opening into an exhalant canal. In a more complicated stage, as seen in Plakortis , the dermal membrane spreads over the outer ends of the folds, and subdermal cavities are developed.

Tetractinomorpha. Demospongiae in subclass Tetractinomorpha have parenchymella or blastula-like (clavablastula) larvae, are generally oviparous, and have monaxonic or tetraxonic megascleres (or both) and astrose-type microscleres. The skeleton has radial structure. In many species of Tetractinomorpha, an extensive cortex is AccessScience from McGraw-Hill Education Page 6 of 9 www.accessscience.com

developed, consisting of a network of fiber cells that in some cases is overlaid by a thick gelatinous layer containing amebocytes and microscleres. In form, the species of these orders may be thinly encrusting or massive, but often they have spherical or ovoid shapes. Branching species rarely occur.

The orders of Tetractinomorpha are Spirophorida (with triaene megascleres and sigmaspire microscleres),

Astrophorida (with diactinal and tetractinal megascleres, astrose microscleres), Hadromerida (with monaxonic megascleres, diverse shapes of microscleres, including spirasters), and Chondrosida (with fibrillar collagen cortex and astrose microscleres, or no spicules at all). The old order Lithistida is polyphyletic and has been abandoned; most of its members show affinities with Astrophorida, and some with Hadromerida.

Ceractinomorpha. Demospongiae in subclass Ceractinomorpha have parenchymella larvae, exhibit viviparous reproduction, and have spicules and spongin fibers, or only fibers, or neither, often forming complex skeleton architectures (for example, reticulate). Spicules are monactinal (styles) or diactinal (oxeas, strongyles) megascleres and a great variety of microscleres (chelae, microxea, toxas; never astrose). The orders are

Poecilosclerida [monactinal or diactinal (or both) megascleres; spongin fibers; and chelae, sigmas, toxas, and similar forms as micro- scleres], Halichondrida (oxeas, styles, and strongyles as megascleres; plumoreticulate, dendritic, or confused spongin fibers; microxea-type microscleres, if any), Agelasida (verticillately spined monactin megascleres, partly embedded in robust fibers of spongin network; no microscleres), Haplosclerida

(diactin megascleres connected by or embedded in spongin fibers that form complex reticulations; rare sigma- or toxa-type microscleres), Dictyoceratida (complex network of spongin fibers, with or without embedded sediment particles, without proper spicules), Dendroceratida (dendritic and anastomosing pithed spongin fibers, without mineralized spicules), Halisarcida (skeleton of fibrous spongin, without fibers or spicules), and

Verongida (spongin skeleton forming polygonal meshes of uniform fibers with central fibrous pith and laminar bark, without spicules).

Among the Ceractinomorpha, the genus Halisarca , lacking skeletal elements, used to be considered a primitive form and was subject to several studies. The larva of Halisarca is a parenchymella-like dispherula with an outer layer of flagellated cells and an inner mass of presumptive ectomesenchymal cells ( Fig. 5 a ). The outer flagellated cells lose their flagella, migrate into the interior (Fig. 5 b and c ), and later differentiate into choanocytes. Other cell types characteristic of the adult sponge differentiate, and inhalant canals begin to form. The young sponge soon develops a single internal cavity lined with choanocytes (Fig. 5 d ), and an oscular opening breaks through at the apex (Fig. 5 e ). At this stage of development, called the rhagon stage, the young Halisarca is essentially identical with the asconoid grade of construction found in some Calcarea. Later, folds in the choanocytal layer lead to the formation of choanocyte (“flagellated”) chambers, and a transitory syconoid grade of construction exists. Eventually, the choanocyte chambers are isolated from one another through the appearance of exhalant canals, which converge on the oscula. The adult sponge has a simple leuconoid structure, with elongate

flagellated chambers having wide openings into exhalant canals and communicating with the surface pores by means of an inhalant canal system. Aplysilla , a closely related genus of sponges with a branching, AccessScience from McGraw-Hill Education Page 7 of 9 www.accessscience.com

WIDTH:BFig. 5 Development of ceractinomorph sponges. ( a ) Free-swimming parenchymella-like larva (dispherula) of Halisarca . ( b –e ) Metamorphosis of Halisarca (Halisarcida): ( b ) newly settled parenchymella; external flagellated cells migrate internally; ( c ) internal cavity appears; ( d ) choanocytes line the central cavity; and ( e ) osculum breaks through and young asconoid stage is formed. ( f –i ) Metamorphosis of Aplysilla (Dendroceratida): ( f ) newly settled parenchymella; external flagellated cells migrate internally; ( g ) islands of choanocytes form in the internal mass of cells; ( h ) choanocyte chambers and inhalant canals appear; and ( i ) choanocyte chambers join the exhalant canal system, which opens through the osculum; young syconoid sponge is formed.

nonanastomosing fibrous skeleton, has a similar developmental history (Fig. 5 f –i ), except that the earliest rhagon stage is syconoid in structure with a folded choanocytal layer. See also: CALCAREA .

Lithistid sponges. Some species of Demospongiae are characterized by the presence of spicules called desmas ( Fig.

6 ). These are formed by the secondary deposition of silica around ordinary monaxonid or tetraxonid spicules.

Supplementary knobby branches often develop and articulating processes may occur, by which neighboring desmas become interlocked to form a stony or lithistid skeleton. Because of the rigidity of the skeletons of lithistid sponges, they are commonly preserved as fossils and are the best-known Demospongiae in the fossil record.

Paleontologists have tended to classify such sponges in an order Lithistida. It is apparent from studies of Recent species with a lithistid skeleton that this modification has arisen many times in the evolution of the Demospongiae AccessScience from McGraw-Hill Education Page 8 of 9 www.accessscience.com

WIDTH:BFig. 6 Discodermia ornata , a lithistid sponge: ( a ) whole sponge; ( b ) desma.

and that the order Lithistida has no validity. However, unless developmental stages of the peculiarly modified spicules are present, it is difficult to place fossil lithistids among the several orders of the class Demospongiae.

Klaus R utzler,¨ Willard D. Hartman

Keywords

Demospongiae; ; Homoscleromorpha; Tetractinomorpha; Ceractinopmorpha; choanocyte chamber; canals; spicule; spongin fiber

Bibliography

N. Boury-Esnault and K. R utzler¨ (eds.), Thesaurus of sponge morphology, Smithson. Contrib. Zool. , 596:1–55,

1997 DOI: http://doi.org/10.5479/si.00810282.596

L. De Vos et al., Atlas of Sponge Biology ∕ Atlas de Morphologie des Eponges , Smithsonian Institution Press,

Washington, D.C., 1991

J. N. A. Hooper and R. W. M. van Soest, Class Demospongiae Sollas, 1885, pp. 16–18, in J. N. A. Hooper and R. W.

M. van Soest (eds.), Systema Porifera: A Guide to the Classification of Sponges , Kluwer Academic ∕ Plenum

Publishers, New York, 2002

M. Maldonado and P. R. Bergquist, Phylum Porifera, pp. 21–50, in C. M. Young (ed.), Atlas of Marine

Invertebrate Larvae , Academic Press, San Diego, 2002

R. W. M. van Soest, Demosponge higher taxa classification re-examined, pp. 54–71, in J. Reitner and H. Keupp

(eds.), Fossil and Recent Sponges , Springer-Verlag, Berlin ∕ Heidelberg, 1991 AccessScience from McGraw-Hill Education Page 9 of 9 www.accessscience.com

Additional Readings

C. Borchiellini et al., Molecular phylogeny of Demospongiae: Implications for classification and scenarios of character evolution, Mol. Phylogenet. Evol. , 32:823–837, 2004 DOI: http://doi.org/10.1016/j.ympev.2004.02.021

A. V. Ereskovsky, The Comparative Embryology of Sponges , Springer, New York, 2010

D. Erpenbeck et al., Towards a DNA of Caribbean demosponges: A gene tree reconstructed from partial mitochondrial CO1 gene sequences supports previous rDNA phylogenies and provides a new perspective on the systematics of Demospongiae, J. Mar. Biol. Assoc. U.K. , 87:1563–1570, 2007

D. Erpenbeck et al., Order level differences in the structure of partial LSU across demosponges (Porifera): New insights into an old taxon, Mol. Phylogenet. Evol. , 32:388–395, 2004

DOI: http://doi.org/10.1016/j.ympev.2004.02.014

D. Erpenbeck et al., Insights into the evolution of freshwater sponges (Porifera, Demospongiae, Spongillina):

Barcoding and phylogenetic data from Lake Tanganyika endemics indicate multiple invasions and unsettle existing taxonomy, Mol. Phylogenet. Evol. , 61(1):231–236, 2011 DOI: http://doi.org/10.1016/j.ympev.2011.05.021

J. N. A. Hooper and R. W. M. van Soest (eds.), Systema Porifera: A Guide to the Classification of Sponges ,

Kluwer Academic ∕ Plenum Publishers, New York, 2002

P. Willenz, Bibliography of class Demospongiae, pp. 19–51, in J. N. A. Hooper and R. W. M. van Soest (eds.),

Systema Porifera: A Guide to the Classification of Sponges , Kluwer Academic ∕ Plenum Publishers, New York,

2002

Porifera Tree of Life Project

Sponge Barcoding Project

World Porifera Database