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21 Lophophorates

Anyone who starts looking at bryozoans

will continue to do so, for their biology is
full of interest and unsolved mysteries.
J. S. Ryland,
Bryozoans, 1970

M ost of the rest of the book is devoted to seven phyla that make up
an evolutionary clade known as the deuterostomes: Echino-
dermata, Chaetognatha, Hemichordata, Chordata, and the three
lophophorat groups: Phoronida, Ectoprocta, and Brachiopoda. Some of the fea-
tures that define the deuterostomes are shared by other taxa (such as radial cleav-
age in the cnidarians), but the clade is distinguished by the synaphomorphies of
enterocoelic development, and a tripartite bauplan, and the mouth deriving from
the blastopore (except in phoronids) (see Chapters 4 and 24). Although the varia-
tions on this theme have not led to the extreme diversity of species we saw
among the protostomes, they have resulted in several fundamentally different
and distinct groups of animals. In fact, there are greater differences among the
major taxa of deuterostomes than among the major taxa of protostomes. Thus, at
least at higher taxonomic levels, the deuterostome bauplan has proved both evo-
lutionarily labile and highly successful in a wide range of lifestyles.

The Lophophorates: An Overview

In his 1977 address introducing a symposium on the biology of lophophorates,
Joel W. Hedgpeth referred to these creatures as an “aggregation of animals that
possess a feeding structure known as a lophophore.” Although the term aggrega-
tion is certainly not a valid taxonomic category, it is an appropriate description in
this case and reflects disagreement about the relationships of the lophophorates
to each other and to other phyla.
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Traditionally included as lophophorates (Greek, Zoophyta, a misconception that persisted into the 1700s.
“crest-bearers”) are three phyla: Phoronida, Brachio- Peyssonal (1729) finally established the animal nature of
poda, and Ectoprocta (= Bryozoa). At first glance, the ectoprocts, and Jussieu (1742) noted the compartmental-
members of these groups may seem to have little in com- ized condition of the colonies and coined the term polyps
mon (see Figures 21.1, 21.5, 21.6, and 21.17). However, to refer to the individual animals. Still, most well-
they do display a number of important similarities. They known workers of the day (e.g., Linnaeus and Cuvier)
are allied with the deuterostomes and are built along a insisted on allying them with the cnidarians in the
trimeric (= tripartite) bauplan wherein the body is divid- group Zoophyta.
ed into an anterior prosome, a middle mesosome, and a Eventually, de Blainville (1820) noted the complete
posterior metasome. In most cases, at least developmen- gut of the ectoprocts and “raised” them above the
tally, each of these regions contains a separate, often cnidarians. By 1830, two names had been coined for
paired, coelomic compartment: protocoel, mesocoel, these animals—Bryozoa (by the German zoologist
and metacoel, respectively (see Chapter 4). Furthermore, Ehrenberg) and Polyzoa (by the Englishman Thomp-
the lophophorates all have a U-shaped gut and very sim- son). Just about the time the ectoprocts (under one or
ple, often transient reproductive systems. Nearly all se- the other name) were being recognized as a separate
crete outer casings in the form of tubes, shells, or com- group, concurrent events confused the issue further. The
partmented exoskeletons. Even though these features entoprocts (= Kamptozoa) were described, and most
represent shared similarities among the lophophorates, workers included them with the ectoprocts (under the
none is unique to them. Their most significant common name Bryozoa), while others recognized a relationship
feature is the lophophore itself, which, simply put, is a between ectoprocts and other lophophorates. All of this
ciliated, tentacular outgrowth arising from the meso- became terribly entangled in Milne-Edwards’s (1843)
some and containing extensions of the mesocoel. It sur- concept of a taxon Molluscoides, which he established
rounds the mouth but not the anus. to include the ectoprocts and compound ascidians (see
The tentacular crown of pterobranchs (Chapter 23) Chapter 23).
also possess mesosomal tentacles with a coelomic The brachiopods were known, at least from fossils, in
lumen. The homology between pterobranch tentacles the 1600s and were allied with the molluscs. This mis-
and a “true” lophophore is invalidated only because in taken view was held until late in the nineteenth century.
the former case the tentacles do not fully surround the Phoronids were first described from their larvae by
mouth. Thus, we view the lophophore as a unique Müller in 1846, who thought they were adults and
synapomorphy of members of the phyla Phoronida, named them Actinotrocha brachiata. Not long after,
Ectoprocta, and Brachiopoda and treat the three groups Gegenbaur (1854) recognized these animals as larval
as a monophyletic clade. However, a deep-level homol- stages. The adults were found and described by Wright
ogy, or perhaps parallel evolution, is probable between (1856), who named them Phoronis. Finally, the renowned
pterobranchs and lophophorates. To be sure, there are embryologist Kowalevsky (1867) studied the metamor-
some problems with this hypothesis, some of which are phosis of “Actinotrocha” and established the relationship
discussed later. between the two stages. The name “actinotroch” per-
With the exception of a few freshwater ectoprocts, the sists as a general term for the phoronid larva.
lophophorates are exclusively marine. All are benthic, In 1857 Hancock recognized the relationship between
living either in tubes (phoronids) or in secreted shells, or brachiopods and bryozoans, but the whole matter was
casings. The phoronids are a small group, comprising mixed up with confusion over the entoprocts and
only two genera and about 20 species of solitary or gre- Milne-Edwards’s Molluscoides. Nitsche (1869) made a
garious worms. Ectoprocts, on the other hand, make up valiant attempt to separate the entoprocts and ecto-
a diverse taxon of about 4,500 species of colonial forms. procts, and in 1882 Caldwell first put forth the idea of a
The brachiopods, or lamp shells, include about 335 ex- relationship between the brachiopods, phoronids, and
tant species. However, the brachiopods have left a bryozoans. This view was supported by Hatschek
record of over 12,000 fossil species as evidence of a (1888), who suggested the establishment of a phylum
greater past. They were well established by the early Tentaculata to include the classes Phoronida, Brachio-
Cambrian. These animals flourished in both abundance poda, and Ectoprocta (but excluding the entoprocts).
and diversity from the Ordovician through the Since that time several attempts to unite some or all of
Carboniferous, but they have declined in numbers and these animals into a single taxon have been made, in-
kinds ever since. cluding Schneider’s (1902) Lophophorata (for
phoronids and bryozoans). Hyman (1959) rejected these
Taxonomic History ideas and retained separate phylum status for the three
The lophophorates have had a long and torturous taxo- groups, an arrangement that has remained popular ever
nomic history. The earliest records of any lophophorate since.
are of various ectoprocts reported in the sixteenth centu- Recently, however, some of the earlier views have
ry. With few exceptions, the early zoologists treated reemerged with new evidence and new vigor. On one
them as plantlike and included them in the taxon front, Nielsen (1971, 1977) has revived the idea of a pos-
 LOPHOPHORATES 3

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sible entoproct–ectoproct affinity and argued that the
two groups are closely related (even though entoprocts BOX 21A Characteristics of the
are fundamentally protostomous and are not trimeric in Phylum Phoronida
their body plan). Although this hypothesis has found its
way into several recent texts, we find it untenable in 1. Trimeric, enterocoelic, vermiform lopho-
light of the evidence. In support of lophophorate unity, phorates
some recent authors have again suggested that a single 2. Body divided into flaplike epistome (prosome),
phylum or “superphylum” should be formally estab- lophophore-bearing mesosome, and elongate
lished for the three groups. Most recently, 18S rDNA se- trunk (metasome), each with associated
quence data has suggested that the lopophorates are al- coelom
lied with the protostomes—in a grouping known as the 3. Gut U-shaped, anus close to mouth
lophotochozoa. This controversial idea is discussed in
4. One pair metanephridia in metasome
Chapter 24. Below, we provide classifications and dis-
cussions for the lophophorate phyla. 5. Closed circulatory system
6. Dioecious or hermaphroditic, with transient
peritoneal gonads
The Lophophorate Bauplan 7. With mixed or indirect life histories; usually
with an actinotroch larva
In spite of the obvious diversity in external form among
the lophophorates, there is a fundamental unity here. 8. Radial, indeterminate cleavage; coeloblastulae
The diversity, great or small, in any monophyletic lin- gastrulate by invagination; blastopore becomes
mouth (in contrast to all other deuterostomes)
eage is a reflection of evolutionary variations on a cen-
tral theme—the theme being the bauplan. Among the 9. Marine benthic tube dwellers
deuterostomes, the general theme consists of those fea-
tures of ontogeny that define the lineage and the result-
ing trimeric body plan with its tripartite coelomic sys-
tem. Impose upon this plan the lophophore, and the of valves or shells that encase and protect the body, in-
result is a unique clade derived from the main deuteros- cluding the lophophore (Box 21C). Thus, instead of ex-
tome line. Couple this single synapomorphy with a posing the lophophore in the water, as phoronids and
number of other shared features, and the lophophorate ectoprocts do, the brachiopods draw water into their
bauplan begins to emerge as a set of characters more mantle cavity for suspension feeding, an action analo-
easily explained as arising from common ancestry than gous to that in bivalve molluscs. Sessile animals with
resulting from convergence. soft parts (e.g., the lophophore), living on benthic sur-
All lophophorates are built for benthic life and sus- faces, are exposed to potentially high levels of preda-
pension feeding, the latter being a primary function of tion—thus the selective advantage of the brachiopod
the lophophore itself. The anterior body region, or pro- shell is clear. The phoronids are motile to the extent that
some, is reduced to a small, flaplike epistome (or lost in their bodies can be retracted within their tubes, protect-
some) associated with an overall reduction of the head, ing the soft parts. Ectoprocts are entirely anchored in
the elaboration of the mesosome as the lophophore, and their casings, but the lophophore itself is retractable into
a sessile lifestyle. As in most deuterostomes, the meta- the body, as the result of a unique arrangement of mus-
some houses the bulk of the viscera. The U-shaped gut cles and hydraulic mechanisms.
is clearly advantageous for living encased in tubes, com-
partments, and shells; such animals do not “foul their
nests,” as it were. We have seen similar adaptations in Phylum Phoronida: The Phoronids
some other groups with comparable habits, such as the
recurved gut of sipunculans and the ciliated fecal-re- Phoronids are all tube dwellers; their chitinous tubes are
moval grooves of some tube-dwelling polychaetes. In usually either cemented (often in clusters) to hard sub-
lophophorates, this condition not only prevents fecal ac- strata, or buried vertically in soft sediments (Figure
cumulation in the encasement, but generally brings the 21.1). They are assigned to only two genera: Phoronis
anus close to rejection currents produced by the cilia on and Phoronopsis. The phylum name was apparently de-
the lophophore. rived from the Latin term Phoronis, the surname of Io
The phoronids most clearly display the above traits, (who, according to mythology, was changed into a cow
and retain the vermiform shape of the probable ances- and roamed the Earth, eventually to be returned to her
tral form (Box 21A). Evolutionarily, the ectoprocts have former body). Recall that these worms were first de-
exploited asexual reproduction, colonialism, and small scribed from larval stages drifting in the sea, and only
size (Box 21B). Relieved of long-distance internal trans- much later were the adults recognized as part of the
port problems, the ectoprocts have lost the circulatory same life cycle. Adult phoronids are known from inter-
and excretory systems. The brachiopods evolved a pair tidal mud flats to depths of about 400 meters.
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Figure 21.1 Phoronids. (A)
General external form of a
phoronid (Phoronis architechta). (B)
Phoronis psammophila encrusted
with sand grains and shell frag-
ments. (C) A phoronid viewed from
the lophophoral end. The tentacles
have been cut in cross section. (D)
Phoronis vancouverensis in a tidal
flat. (E) Exposed lophophores of a
colony of Phoronis hippocrepia.
(F) The lophophore of Phoronis
hippocrepia.

(D) (F)

(E)
The Phoronid Bauplan
Phoronids range from about 5 to 25 cm in length. The
vermiform body shows little regional specialization, ex-
cept for the distinct lophophore and a modest inflation
of the end bulb, which houses the stomach and also
aids in anchoring the animals in their tubes. The slitlike
mouth is located between the tentacle-bearing lopho-
phoral ridges and is overlaid by a flap, the epistome.
The lateral aspects of the ridges are distinctly coiled and
flank the dorsal anus and paired nephridiopores (Figure
21.1). Using the terms anterior and posterior when refer-
ring to phoronids can be misleading. During metamor-
 LOPHOPHORATES 5

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Figure 21.2 Phoronid internal anatomy. (A) The trunk

of a phoronid (cross section). Note the body wall layers
and coelomic partitioning. (B) A tentacle of the lopho- the epidermis are sensory neurons and various gland
phore in cross section. (C) The digestive tract. (D) The cir- cells, the latter responsible for the production of mucus
culatory system. (E) The major internal organs in the and chitin (Figure 21.2A). The epidermis of the lopho-
lophophoral and stomachic ends. phore is densely ciliated. Internal to the epidermis and
its basement membrane is a thin layer of circular muscle
and a thick layer of longitudinal muscle. A peritoneum
phosis the true anterior (mouth-bearing) and posterior lines the longitudinal muscles and forms the outer
(anus-bearing) ends are brought very close together by boundary of the coelom.
rapid growth and enlargement of the ventral surface The coelom is clearly tripartite. The protocoel is limit-
(see Figure 21.4). The dorsal surface is reduced to only ed to a single small cavity within the epistome. The un-
the small area between the adult mouth and anus. paired mesocoel comprises a coelomic ring in the lopho-
Because of these conditions, we refer to the “ends” of phoral collar and extensions into each tentacle (Figure
the adult worm as the lophophoral end and the stom- 21.2B). The protocoel and mesocoel are connected to one
achic end. another along the lateral aspects of the epistome. The
metacoel forms the main trunk coelom, which is sepa-
Body Wall, Body Cavity, and Support rated from the mesocoel by a transverse septum. Onto-
The phoronid body wall includes an epidermis of genetically, the metacoel is an uninterrupted cavity with
columnar cells overlaid by a very thin cuticle. Within only one, midventral, mesentery. However, secondary
6 CHAPTER TWENTY-ONE

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mesenteries form later in development, yielding four so, and much of the movement of food is by ciliary ac-
longitudinal spaces (Figure 21.2A). The coelomic fluid tion. A middorsal strip of densely ciliated cells arises in
contains several kinds of freely wandering cells, or the prestomach and extends into the stomach, and it is
coelomocytes, including phagocytic amebocytes. probably responsible for directing food along that por-
Body support is provided by the hydrostatic qualities tion of the gut. Gland cells occur in the esophagus but
of the coelomic chambers and by the tube. The muscles their function remains uncertain. Transitory syncytial
of the body wall are rather weak, particularly the circu- bulges in the stomach walls are the site of intracellular
lar layer, and once removed from their tubes phoronids digestion in that organ.
are capable of only limited movement. Normally, how-
ever, the body wall of the end bulb is pressed against the Circulation, Gas Exchange, and Excretion
tube, holding the worm in place. When disturbed, the Phoronids contain an extensive circulatory system com-
animal simply contracts into the tube; the lophophore it- prising two major longitudinal vessels between which
self is not retractable. blood is exchanged in the lophophoral and stomachic
The tube is secreted by epidermal gland cells. When ends of the body (Figure 21.2D,E). Various names have
first produced, the chitinous secretion is sticky; but been applied to these vessels relative to their positions
upon contact with water it solidifies to a flexible parch- in the body. These terms are often confusing because the
ment-like consistency. Sand grains and bits of other ma- positions of vessels vary along the length of the trunk,
terial adhere to the tube during the sticky phase of its and they are not clearly dorsal, medial, lateral, or ven-
formation in those phoronids that inhabit soft substrata tral as the names imply. We prefer the terms afferent
(e.g., Phoronopsis harmeri). In some species the tubes in- and efferent vessels, which refer to the direction of
tertwine with one another, with the whole tangled blood flow relative to the lophophore.
aggregation attached to a substratum or actually em- The afferent vessel extends unbranched from the re-
bedded in calcareous stone or shells (e.g., Phoronis hippo- gion of the end bulb to the base of the lophophore. For
crepia). most of its length it lies more or less between the de-
scending and ascending portions of the gut. In the
The Lophophore, Feeding, and Digestion mesosome the afferent vessel forks, forming an afferent
The tentacles of the lophophore are hollow, ciliated out- “ring” vessel (U-shaped) at the base of the lophophoral
growths of the mesosome, and each contains a blind- tentacles. A series of lophophoral vessels, one in each
ended blood vessel and a coelomic extension (Figure tentacle, arises from the afferent ring. Each of these ves-
21.2B). The tentacles are in a double row, arising from sels joins with an efferent “ring” vessel (also U-
two ridges. The ridges lie close to one another and form shaped), which drains blood from the lophophore. Thus
a narrow food groove in which the slitlike mouth is lo- the afferent and efferent blood rings lie against one an-
cated (Figure 21.1C). Because the sides of the lopho- other, and generally share openings into the lopho-
phoral ridges are coiled, many tentacles are compacted phoral tentacles within which blood moves back and
into a small area. forth, there being but a single vessel in each tentacle.
Phoronids are ciliary–mucous suspension feeders. Backflow into the afferent ring is largely prevented by
The lophophoral cilia generate a water current that tiny, one-way, flap valves.
passes down between the two rows of tentacles and The arms of the efferent ring unite to form the main
then out between the tentacles. Food particles are efferent blood vessel, which extends through the trunk.
trapped in mucus lining the food groove and then This vessel gives off numerous branches or simple blind
passed along the groove by cilia to the mouth. As the diverticula called capillary ceca, which bring blood
water current passes between the tentacles and out of close to the gut wall and other organs. In the end bulb,
the area of the food groove, some is directed over the surrounding the stomach and first part of the intestine,
anus and nephridiopores away from the animal (Figure blood flows from efferent to afferent vessels through
21.1C). spaces composing the hemal (stomachic) plexus
The digestive tract is U-shaped, but rather simple (Figure 21.2D,E). Blood actually leaves the vessels here
and not coiled (Figure 21.2C). The mouth is overlaid by and flows through spaces between the organs and their
the epistomal flap and leads inward to a short buccal bordering layers of peritoneum. Thus, technically
tube, which is followed by an esophagus and a narrow speaking, the system is open at this point; however,
prestomach. Within the end bulb the gut expands into a blood flow is directed within the confines of these pas-
stomach, from which emerges the intestine. The intes- sages. Blood is moved through the circulatory system
tine bends up toward the lophophore and leads to a largely by muscular action of the blood vessel walls.
short rectum and the anus. The gut is supported by The intimate association of blood and the stomach
peritoneal mesenteries (Figure 21.2A). wall suggests that nutrients are picked up from the
The entire digestive tract is apparently derived from stomach by the circulatory fluid and transported
endoderm. Some parts are muscular, but only weakly throughout the body. The tentacles of the lophophore are
 LOPHOPHORATES 7

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also probably the most important site of gas exchange. in the metasome. In addition, a bundle of sensory neu-
Oxygenated blood flows from the lophophore into the rons extends from the nerve ring to each of the
efferent vessel and from there is distributed to all parts of lophophoral organs (see below).
the trunk. The blood contains nucleated red corpuscles, Phoronids possess one or two longitudinal giant
with hemoglobin as the respiratory pigment. motor fibers in the trunk (absent in the very small
A pair of metanephridia lies in the trunk, and each Phoronis ovalis). When only one longitudinal fiber is
bears two nephrostomes opening to the metacoel (Figure present, it lies on the left side. Actually, this fiber origi-
21.2E and 21.3A). In each nephridium, the nephros- nates within the right side of the nerve ring, through
tomes—one large and one small—join a curved nephrid- which it passes to emerge on the left side. This nerve
ioduct, which leads to a nephridiopore adjacent to the fiber is intraepidermal except where it extends inward
anus. Although virtually nothing is known about excre- along the left nephridium. In those species where two
tory physiology in phoronids, particulate crystalline longitudinal fibers are present, the right one originates
matter has been observed exiting the nephridiopores on the left side of the nerve ring and extends to the op-
and probably represents precipitated nitrogenous waste posite side of the body.
products. The nephridia also function as pathways for
the release of gametes. Being marine, osmoregulatory Reproduction and Development
problems are presumably insignificant in phoronids. Asexual reproduction by transverse fission or by a form
of budding has been documented in a few species.
Nervous System Phoronids are also capable of regenerating lost parts of
The nervous system of phoronids is rather diffuse and the body, and are known to autotomize various parts of
lacks a distinct cerebral ganglion. This condition is relat- the lophophoral end.
ed to the sedentary lifestyle and overall reduction in Both dioecious and hermaphroditic species of
cephalization in these worms. Most of the nervous sys- phoronids occur, and in the latter case some are simulta-
tem is intimately associated with the body wall, being neous hermaphrodites (e.g., Phoronis vancouverensis).
either intraepidermal or immediately subepidermal. The gonads are transient and form as thickened areas of
The body is everywhere supplied with a layer of nerve the peritoneum around the hemal plexus. The resulting
fibers between the epidermis and the circular muscle mass of gamete-forming tissue and blood sinuses is
layer. Simple sensory neurons arise from this layer, ei- sometimes called vasoperitoneal tissue (Figure 21.2E).
ther singly or in bundles, and extend to the body surface Gametes are proliferated into the metacoel and typically
as the only receptor structures. Motor neurons extend are carried to the outside via the nephridia. In Phoronis
inward to the muscle layers. ovalis, females autotomize their lophophoral ends and
The central nervous system comprises a simple in- release eggs through the torn opening. Fertilization is
traepidermal nerve ring, which lies at the base of the usually external, except in Phoronopsis harmeri and
lophophore and is continuous with the subepidermal
nerve layer. It is slightly swollen middorsally. The nerve
ring supplies the tentacles with nerves as well as giving Figure 21.3 (A) A phoronid metanephridium (from
rise to motor nerves to some of the longitudinal muscles Phoronis australis). Note the paired nephrostomes. (B) The
lophophore of Phoronis vancouverensis. Note the accessory
lophophoral organs. (C) Spermatophore of Phoronopsis
harmeri. (D) Spermatophore of Phoronis vancouverensis.
8 CHAPTER TWENTY-ONE

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Phoronis vancouverensis. In these species, the males’ placement of the blastomeres because of the tightness of
lophophoral organs produce spermatophores (Figure the fertilization membrane. Otherwise, early cleavage is
21.3 B–D) that are transferred to the tentacles of the fe- clearly radial and has been shown to be indeterminate.
males. In these females the lophophoral organs are A coeloblastula forms and gastrulates by invagination.
called nidamental glands and serve as brooding areas. Mesoderm arises from the presumptive archenteron,
The complicated internal fertilization process in and coelom formation is by a modified enterocoelous
Phoronopsis harmeri (= P. viridis) has been elucidated by method. The only protostome-like feature is the forma-
Zimmer (1972). Spermatophores on the tentacles of fe- tion of the mouth from the blastopore.
males rupture, releasing ameboid masses of sperm. The With the exception of Phoronis ovalis, all phoronids
sperm enter the lophophoral coelom by lysis of the ten- produce distinctive actinotroch larvae (Figure 21.4A).
tacular wall and then proceed to digest their way Earlier works alleging similarities between actinotrochs
through the septum separating the mesocoel and meta- and trochophores are no longer given credence; the
coel into the trunk coelom, where fertilization occurs. actinotroch is clearly a tripartite stage and lends addi-
Although fertilization has not actually been observed, tional support to the deuterostome affinity of the
Zimmer’s experimental data, coupled with the fact that phoronids. The fully formed actinotroch bears a preoral
fertilized ova occur internally, suggest that this scenario hood, or lobe, over the mouth. The hood houses the
is the only tenable explanation. protocoel and becomes the epistome. A partial ring of
Developmental strategy differs among species, the larval tentacles contains the mesocoel and eventually
particular pattern depending in part on the size of the forms the lophophore. As the actinotroch develops, an
egg and on whether fertilization is internal or external. inpocketing (called the metasomal sac) forms on the
The ova of free-spawning species contain little yolk and ventral surface. At settlement and metamorphosis this
develop quickly to planktotrophic actinotroch larvae sac everts, extending the ventral surface such that the
(Figure 21.4). In species that possess nidamental glands, anus and mouth remain close to one another as the gut
fertilization is followed by brooding until release at the is drawn out into the characteristic U-shape (Figure
actinotroch stage. The eggs of these species are moder- 21.4). It is during this metamorphic growth that the lar-
ately rich in yolk, providing nutrients for the embryos val worms settle and begin secreting their tubes.
during the brooding period. Phoronis ovalis lacks nida-
mental glands, but the yolky eggs are shed into the ma-
ternal tube, where they are brooded. Development in P. The Ectoprocts
ovalis does not include a typical actinotroch; instead, the
embryos emerge as ciliated, sluglike larvae that have a Members of the phylum Ectoprocta (Greek ecto, “out-
short, planktonic life. side”; procta, “anus”) are sessile colonies of zooids living
Despite continuing reference in some texts to in marine and freshwater environments (Box 21B). In
phoronids as protostome-like in their early develop- most cases each colony is the product of asexual repro-
ment, it has been convincingly established that such is duction from a single, sexually produced individual
not the case (e.g., Zimmer 1973, 1980). Early reports of called an ancestrula. The colony form differs greatly
spiral cleavage probably resulted from mechanical dis- among species, but their general plantlike appearance
earned these animals the common name “moss ani-
mals,” from which the old name Bryozoa was coined.
Figure 21.4 Phoronid larvae and metamorphosis. (A) Marine ectoprocts are known from all depths and lati-
An actinotroch larva. (B,C) Stages in the metamorphosis of tudes, mostly on solid substrata. One recently discov-
an actinotroch. The gut is drawn into a U-shape, leaving
the mouth and anus at the anterior end.
 LOPHOPHORATES 9

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ered Antarctic species forms gelatinous colonies on
floating pieces of ice! A few species occur in fresh and BOX 21B Characteristics of the
brackish water. The bizarre gelatinous Pectinatella mag- Phylum Ectoprocta
nifica is frequently encountered in streams east of the
Mississippi River. Littoral regions in most parts of the 1. Trimeric, enterocoelic, colonial lophophorates
world harbor luxuriant growths of ectoprocts that often 2. Epistome and protocoel absent in most species
cover large areas of rock surfaces. Some species have
3. Lophophore circular or U-shaped
coral-like growth forms that can create miniature
“reefs” in some shallow-water habitats. Others form 4. Gut U-shaped, anus close to mouth
dense bushlike colonies or gelatinous spaghetti-like 5. Typical circulatory and excretory structures
masses. Many encrusting forms grow on the shells or absent
exoskeletons of other invertebrates and some bore into
6. Colonies produced by asexual budding; zooids
calcareous substrata. Three classes are generally recog- within a colony often polymorphic
nized, as described below.
7. Zooids usually hermaphroditic, but some con-
tain males and females in a single colony;
PHYLUM ECTOPROCTA gametes usually arise from transient patches of
germinal tissue on peritoneum or funiculus
CLASS PHYLACTOLAEMATA: Freshwater ectoprocts.
Colonies with chitinous or gelatinous coverings; zooids cylin- 8. Radial, holoblastic cleavage; indirect or mixed
drical, large, and monomorphic; epistome with protocoel development; blastopore does not form mouth
present; lophophore large and horseshoe-shaped; body wall
muscles well developed; metacoel extensions interconnect 9. Sessile in marine and freshwater habitats
zooids; a cord of tissue, the funiculus, extends from the gut to
the body wall, but not between zooids; most produce asexu-
al bodies called statoblasts. (e.g., Cristatella, Hyalinella, Lopho-
phus, Lophopodella, Pectinatella, Plumatellae.)
The Ectoproct Bauplan
CLASS STENOLAEMATA: Marine ectoprocts. Zooids housed
in tubular, calcified skeletal compartments; zooids cylindrical A special terminology has evolved among ectoproct
or trumpet-shaped, some polymorphic; epistome and proto- specialists, especially concerning the morphology of the
coel absent; lophophore circular; body walls inflexible, lacking
well developed musculature; without special coelomic exten- zooids. The colony itself is called a zoarium and the se-
sions between zooids, but adjacent zooids connected by creted exoskeleton the zoecium. Early workers mistak-
pores; funiculus does not extend between zooids; with a enly thought that ectoproct zooids were actually com-
unique membranous sac housing the internal parts of the posed of two organisms, the exoskeletal compartment
polypide; reproduction involves unique polyembryony, where- and the internal soft parts, which they named the cystid
by single embryos reproduce asexually; one extant order, Cy-
clostomata. (e.g., Actinopora, Crisia, Diaperoecia, Disporella, Id- and polypide, respectively. These terms were redefined
modronea, Tubulipora) by Hyman (1959) and now have some meaning relative
to the functional morphology of ectoprocts. The cystid
CLASS GYMNOLAEMATA: Highly diverse group of primarily
marine ectoprocts. Colony form is extremely variable, soft or comprises the outer casing, or zoecium, and the at-
calcified, encrusting to arborescent; body wall lacks muscles; tached parts of the body wall—that is, the nonliving and
zooids variably modified from basic cylindrical form; zooids living housing of each zooid. The polypide includes the
usually polymorphic; lophophore circular, epistome and pro- lophophore and soft viscera that are movable within the
tocoel absent; zooids joined by pores through which cords of housing (Figure 21.5). The opening in the cystid through
tissue extend and join with each funiculus; two orders, Ctenos-
tomata and Cheilostomata. which the lophophore extends is termed the orifice and
often bears a flaplike covering, or operculum.
ORDER CTENOSTOMATA: Colonies vary in shape; skele- The nature of the exoskeleton differs among ecto-
ton leathery, chitinous, or gelatinous, not calcified; open-
ings through which zooids protrude lack opercula; without procts, as does the form of the colony. The outer cover-
ovicells for brooding embryos; without avicularia. (e.g., ing may be gelatinous or chitinous, as it is in the Phy-
Aethozoon, Alcyonidium, Alcyonium, Amathia, Bowerbankia, lactolaemata and Ctenostomata, or calcified, as it is in
Flustrellidra, Nolella, Tubiporella, Victorella) the Stenolaemata and Cheilostomata. The different
ORDER CHEILOSTOMATA: Colony form varies, but gen- growth patterns among ectoprocts result in a great vari-
erally of box-shaped zooids with calcareous walls; openings ety of colony shapes. Most phylactolaemates display ei-
usually with opercula; zooids often polymorphic; embryos ther lophopodid or plumatellid colony forms. In the
usually brooded in ovicells. (e.g., Bugula, Callopora, Car- former case, the gelatinous covering forms an irregular
basea, Cellaria, Conopeum, Cornucopina, Cribrilaria, Crypto-
sula, Cupuladria, Electra, Eurystomella, Flustra, Hippothoa, clump from which the zooids protrude, as seen in
Membranipora, Metrarabdotos, Microporella, Pentapora, Lophophus (Figure 21.5B). Plumatellid colonies are usual-
Porella, Pyripora, Rhamphostomella, Schizoporella, Thalamo- ly erect or prostrate, and often are highly branched, like
porella, Tricellaria) Plumatella. One remarkable phylactolaemate, Cristatella,
10 CHAPTER TWENTY-ONE

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(D)

(E)
Figure 21.5 Ectoprocts. (A) A single zooid of Plumatella
(cutaway view). Note the distinction between cystid and
polypide. (B) A colony of Lophophus. Note the confluent
coelomic cavities. (C) A motile colony of Cristatella mucedo
crawling over a plant stem. (D) A colony of Eurystomella.
(E) A colony of the freshwater ectoproct Cristatella.

grows in a distinct gelatinous strip, somewhat sluglike

in form, and is capable of locomotion, creeping at rates
of over 1 cm a day (Figure 21.5C).
The Stenolaemata and Gymnolaemata include a be-
wildering array of colony forms that may be generally
categorized as stoloniferous or nonstoloniferous.
Stoloniferous colonies are characteristic of some mem- onies may be encrusting, arborescent, discoidal, and so
bers of the order Ctenostomata, in which the zooids on (Figure 21.6), but in all cases, the zooids are compact-
arise separately from horizontal “runners,” or stolons ed and adjacent to one another, rather than arising sepa-
(e.g., Bowerbankia; Figure 21.6A). Nonstoloniferous col- rately and at some distance from one another.
 LOPHOPHORATES 11

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(B)

(C)

(D)

(E)

Figure 21.6 Ectoproct colonies. (A) A stolonifer-

ous colony of Bowerbankia. (B) Arborescent colonies
In addition to variation in overall form of the of Bugula; (C) Patches of an encrusting ectoproct,
Membranipora. (D) The fleshy bryozoan Alcyonium
colonies, zooids of many gymnolaemates and some
verilli. (E) Conopeum seurati. (F) Part of a colony of
stenolaemates are polymorphic (within a colony). the encrusting ectoproct Schizoporella. (G) Leaflike
Typical lophophore-bearing individuals are called auto- colony of Flustra. (H) Cabbage-like colony of
zooids and are responsible for feeding and digestion. Pentapora. (I) Discoidal colony of Cupuladria.
12 CHAPTER TWENTY-ONE

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Figure 21.7 SEMs of (A) (B)
some bryozoan colonies.
(A,B) Idmodronea; portion
of a branching colony. (C)
Cribrilaria, shown growing on
Idmodronea. (D) Disperella
(whole specimen). (E)
Rhamphostomella argentea,
with ovicells and avicularia.
(F) Thalamoporella; portion of
colony with brood chambers.

(C) (D)

(E) (F)
 LOPHOPHORATES 13

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All other individuals of a colony are collectively referred
to as heterozooids, of which there are several types, all
incapable of feeding. Kenozooids are reduced individu-
als modified for attachment to a substratum; various
types of attachment discs, “holdfasts,” and stolons are
in this category.
Many gymnolaemates possess avicularia, each of
which bears an operculum modified as a movable
mandible (or jaw), which articulates against a rigid ros-
trum ( or palate). Zooids that possess avicularia defend
the colony against small organisms and keep the surface
clean of debris (Figure 21.7E and 21.8A). The latter func-
tion is also facilitated by another type of heterozooid
called a vibraculum (Figure 21.8B). These individuals
are thought to be modified avicularia, and they have a
flagellum-like operculum that sweeps over the colony
surface. They may help remove sediment particles and
other material, but convincing evidence for this function
is wanting.

The Body Wall, Coelom, Muscles,

and Movement
The body wall comprises the outer secreted zoecium,
the underlying epidermis, and the peritoneum. Sheets
of circular and longitudinal muscles are present be-
tween the epidermis and peritoneum in phylactolae-
mates, but these muscle sheets are absent or greatly re-
duced in the other groups and are replaced by various
muscle bands. Ectoprocts differ from other lophophor- Figure 21.8 Ectoproct heterozooids. (A) An avicularium
ates in their ability to retract their lophophores into their from Bugula. (B) A vibraculum.
zoecial casings, a clear protective device for these tiny
sessile animals, whose soft parts would otherwise be
continuously exposed to grazing predators. chambers. Thus, when the metacoel is compressed the
Many ectoprocts possess ornate and species-specific polypide is partially forced out of the cystid, thereby
surface sculpturing including spines, pits, and protuber- protracting the lophophore. At the same time, coelomic
ances (Figure 21.7). Experiments by Harvell (1984) indi- fluid is moved into the mesocoel and erects the tenta-
cate that the cheilostomate Membranipora undergoes a cles. Various retractor muscles serve to pull the polypide
rapid growth of new protective surface spines after back within the cystid. Generally, these methods of
grazing by predators (e.g., nudibranchs). Some ecto- lophophore action are common to all ectoprocts, but the
procts also produce chemicals used as defense against mechanisms involved differ considerably. Below we de-
would-be predators. scribe a few examples of how these movements are ac-
The mechanisms of lophophore retraction and pro- complished and at the same time illustrate variations on
traction differ among ectoproct species. The specific the basic ectoproct bauplan.
mechanism depends largely upon the arrangement of Phylactolaemates protract their lophophores by con-
muscles, the degree of rigidity of the zoecium, and the traction of the circular muscles of the flexible body wall
hydraulic qualities of the coelomic compartments. around the metacoel. This action imposes pressure di-
Recall the morphological distinction between the cystid rectly on the coelomic fluid and is similar to the mecha-
and the polypide; extension and retraction of the nisms we have seen in many other coelomate animals.
lophophore basically involves movement of the latter These ectoprocts possess a ring-shaped, muscular di-
relative to the former. aphragm just internal to the orifice through which the
In all ectoprocts the main coeloms provide fluid- lophophore protrudes. The diaphragm dilates as the
filled spaces on which muscles act directly or indirectly lophophore is protracted and serves to partially close off
to increase hydraulic pressure for protraction of the the orifice after the lophophore is withdrawn by retrac-
lophophore. The epistome and protocoel (present only tor muscles, which extend from the body wall to the
in the phylactolaemates) play no part in this process. base of the lophophore (Figures 21.5A and 21.15).
The septum between the mesocoel and metacoel is per- Stenolaemate ectoprocts (Cyclostomata) have erect,
forated, so the fluid is continuous between the two tubular zooids surrounded by heavily calcified zoecia
14 CHAPTER TWENTY-ONE

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Figure 21.9 Ectoproct anatomy and operation of

the lophophore. (A,B) Two zooids of a stenolaemate,
with the lophophore retracted (A) and protracted (B).
(C,D) The ctenostomate Bowerbankia with the
lophophore protracted (C) and retracted (D).
region of the exosaccal cavity, thereby protracting the
polypide (Figure 21.9B). In addition, the wall of the
membranous sac houses numerous, separate bands of
(Figure 21.9A,B). The inflexibility of the body wall and circular muscles that are thought to aid in lophophore
the absence of well-developed sheets of muscles pre- extension by increasing pressure in the entosaccal
clude use of the direct compression action of the phylac- coelom.
tolaemates. Stenolaemates have evolved a mechanism Several methods of lophophore action have evolved
of lophophore protraction unique among the ectoprocts. among the gymnolaemates. Members of the order
The structural features associated with this mechanism Ctenostomata possess an uncalcified, flexible zoecium
comprise a synapomorphy on which this group was es- composed of gelatinous, chitinous, or leathery material.
tablished as a separate class. The key structure is a Retraction of the lophophore is accomplished by the
membranous sac attached by ligaments to the body usual retractor muscle, which is aided by longitudinal
wall and formed of a thin epithelial layer separating the parietal muscles that pull in the atrial chamber. When
metacoel, or entosaccal coelom, from an outer exosaccal the lophophore is fully retracted, a sphincter contracts,
cavity. Distally, the exosaccal space lies between the closing the orifice and, in some species, folding a pleat-
outer body wall and a thick layer of atrial dilator mus- ed collar over the end of the zooid (Figure 21.9D).
cles. When a zooid is retracted, the atrial dilators are re- Contraction of transverse parietal muscles pulls the
laxed and a special atrial sphincter effectively closes the cystid walls inward, thereby causing an increase in
inner end of the atrium. The retracted polypide presses coelomic pressure that then protracts the lophophore
against the membranous sac, thereby forcing fluid into (Figure 21.9C).
the distal region of the exosaccal cavity (Figure 21.9A). Cheilostomate ectoprocts are housed in zoecia that
Protraction of the lophophore involves relaxation of the have various amounts of calcium carbonate deposited
retractor and atrial sphincter muscles, and contraction between the epidermis and an outer chitinous zoecial
of the atrial dilators. The contracted muscles press out- layer (Figure 21.10). The problem of creating changes in
ward against the atrial wall and force fluid into the basal coelomic pressure has been solved here by the retention
 LOPHOPHORATES 15

UNCORRECTED PAGE PROOFS

of special uncalcified parts of the cystid wall upon which coelomic fluid (Figure 21.9A,B). The funiculus is con-
muscles can act. Each zoecium is more or less boxlike tained within the entosaccal space with the rest of the
(rather than erect or tubular). The outer surface of the viscera and attaches the gut to the body wall.
box that bears the orifice is called the frontal surface. In Stoloniferous gymnolaemates (e.g., Bowerbankia;
many cheilostomates the frontal membrane is uncalci- Figure 21.9C,D) have septa spaced along the stolons be-
fied and flexible (Figure 21.10). Contraction of parietal tween the zooids. A cord of tissue passes along the
protractor muscles pulls the frontal membrane inward, stolons and through pores in each septum. This cord,
thus increasing coelomic pressure and pushing out the called a stolonal funiculus, connects with the funiculus
lophophore. There are variations on this general theme, of each zooid arising from the stolon. In most non-
some of which are discussed by Perez and Banta (1996). stoloniferous gymnolaemates the cystid walls of adja-
Nearly all cheilostomates possess a calcified opercu- cent zooids are pressed tightly together, producing what
lum that closes over the orifice when the polypide is re- are called duplex walls (Figure 21.10A,J). These double
tracted, but the exposed frontal membrane presents a walls bear pores with tissue plugs, which, again, usual-
weakness in their defense against predation, and many ly connect with the funiculus of associated zooids.
species have evolved additional protective devices. It is clear, then, that ectoproct zooids are interconnect-
Some forms, known as the cribrimorph ectoprocts, bear ed structurally, either by direct sharing of coelomic
hard spines that project over the membrane and in some spaces or by funicular tissue. Functionally, these connec-
cases actually meet and fuse to form a cage above the tions provide a means of distributing materials through
vulnerable area (Figure 21.10B,C). In others a calcified the colony, and perhaps other communal activities as
partition, called the cryptocyst, lies beneath the frontal well. Some workers (Carle and Ruppert 1983) even sug-
membrane, separating it from the soft parts within. The gest that the funiculus is homologous to a blood vessel.
cryptocyst bears pores through which the protractor Perhaps these tissues are remnants of the circulatory
muscles extend (Figure 21.10F,G). system in other lophophorates. Other special functions
The most drastic modifications are seen in the so- of the funiculus are discussed later in the chapter.
called ascophoran cheilostomates, wherein the entire
frontal surface is calcified except for a small opening. This The Lophophore, Feeding, and Digestion
opening, called the ascopore, leads inwards to a blind sac Ectoprocts are unique among lophophorates in that the
called the compensation sac, or ascus; this structure is an lophophore is retractable, by mechanisms already ex-
inwardly pouched, flexible portion of the body wall on plained. The lophophore is horseshoe-shaped in the
which the protractor muscles insert (Figure 21.10H–J). phylactolaemates (except for the primitive Fredericella)
Contraction of these muscles pulls the wall of the com- and circular in the other two classes; the tentacular epi-
pensation sac inward as the ascopore allows water to dermis is ciliated. Ectoprocts are typically suspension
enter the sac. Thus, pressure is exerted on the coelom and feeders, although supplemental methods occur. They ap-
the lophophore is protracted. The ascophorans are the parently feed largely on protists and invertebrate larvae
most diverse and successful group of ectoprocts. of appropriate size. The crescentic lophophore of phylac-
tolaemates bears at its base a food groove that leads to
Zooid Interconnections the mouth and functions in a way similar to that de-
Before continuing, there are some aspects of ectoproct scribed for phoronids. Feeding in other groups is some-
colony organization that must be addressed. As dis- what different and has been more extensively studied.
cussed in Chapter 3, clear definitions of the term colony Upon protraction, the tentacles of the circular
are somewhat elusive. This difficulty arises because it is lophophores of stenolaemates and gymnolaemates are
not always easy to tell where one individual ends and erected in a funnel or bell-shaped arrangement around
another begins or because the degree of structural and the mouth (Figure 21.11A). Each tentacle bears three cil-
functional communication among individuals is uncer- iary tracts along its length, one frontal tract and two lat-
tain or variable. Ectoproct zooids, at least autozooids, eral tracts (Figure 21.11B). During normal suspension
are clearly demarcated by the elements of the polypide feeding, the lateral cilia create a current that enters the
(lophophore, gut, and so on), but the way in which the open end of the funnel, flows toward the mouth, and
zooids are interconnected differs among groups. then out between the tentacles (Figure 21.11C). Some
In phylactolaemates the metacoel is continuous food particles are carried directly to the area of the
among zooids, uninterrupted by septa (see Figure mouth by the central flow of water. Other potential food,
21.5A). Each zooid bears a tubular tissue cord, which is however, moves peripherally with the current toward
called a funiculus and extends from the inner end of the the intertentacular spaces. When a particle contacts later-
curved gut to the body wall. All other ectoprocts lack al cilia, a localized reversal of power stroke direction is
extensive coelomic connections, and the zooids are sep- initiated in those cilia, and the particle is tossed onto the
arated by various sorts of structural components. The frontal edge of the tentacle. The particle is repeatedly
walls of adjacent zooids of stenolaemates bear inter- bounced in this fashion, from lateral to frontal, and is
zooidal pores that allow communication of exosaccal moved toward the mouth under the influence of a cur-
16 CHAPTER TWENTY-ONE

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Figure 21.10 (A) A portion of a colony of Electra,

with a cutaway view of one zooid (cheilostomata).
(B,C) Two species of Callopora. Note the calcareous
spines projecting over the frontal membrane. (D–I)
Parietal muscles and frontal membranes in cheilosto-
mates. (D, F, and H are cross sections; E, G, and I are
longitudinal sections.) (D,E) Zooid with unprotected
frontal membrane. (F,G) Zooid with porous cryptocyst
beneath frontal membrane. (H,I) Ascophoran zooid
with compensation sac and calcified frontal mem-
brane. (J) Internal anatomy of an ascophoran
cheilostomate zooid with an ovicell.
 LOPHOPHORATES 17

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Figure 21.11 Ectoproct feeding mechanisms. (A) The lophophoral crown
(longitudinal section). Arrows indicate the general flow of the feeding current.
(B) A lophophoral tentacle (cross section). (C) The lophophore of Flustrellidra
(cross section). Arrows indicate the flow of water between tentacles. (D) Path
of a food particle along a single tentacle.

rent generated by the frontal cilia (Figure 21.11D). cles are actually passed from zooid to zooid and then
Many ectoprocts augment suspension feeding by dumped into an excurrent chimney (Figure 21.12D).
various means that allow them to capture relatively As in all lophophorates, the digestive tract of ecto-
large food particles, including live zooplankton. procts is U-shaped (Figures 21.5, 21.9, 21.10, and 21.13).
Winston (1978) demonstrated that many species engage The mouth lies within the lophophoral ring, and in the
in flicking movements of individual tentacles with Phylactolaemata it is overlaid by an epistome. Ciliary
which a food particle has come in contact. By this means tracts lead into the mouth from the surrounding peris-
a single tentacle curls and strikes at the particle, moving tomial field. Internal to the mouth is a muscular phar-
it to the mouth. At least one species (Bugula neritina) is ynx. A valve separates the lower end of the pharynx
capable of trapping zooplankton by folding its tentacles from the descending portion of the stomach, which is
over the prey and pulling it to the mouth. A number of called the cardia and in some species is modified as a
ectoprocts rock or rotate the entire lophophore, appar- grinding gizzard. The cardia leads to a central stomach
ently “sampling” reachable water for food material from which arises a large cecum; the funiculus attaches
(Figure 21.12A). to the cecum. The ascending portion of the stomach, or
In some ectoprocts the zooids of the colony function pylorus, also arises from the central stomach and leads
together in feeding and rejection of waste or nonfood to a proctodeal rectum and the anus, which lies outside
materials. In many genera (e.g., Cauloramphus and the lophophoral ring. The flow of material from the py-
Hippothoa) groups of zooids “cooperate” to produce gen- lorus to the rectum is controlled by a sphincter. In phy-
eral currents that bring water to several clustered zooids lactolaemates an esophagus precedes the stomach, and
and then flow away via “excurrent chimneys” between the hindgut is elongated as an intestine.
the clusters (Figure 21.12B,C). Such currents, which Ingestion is accomplished by the sweeping action of
move larger amounts of water over the lophophores the peristomial and oral cilia and by muscular contrac-
than could be moved by individual zooids, may be espe- tions of the pharynx. Digestion begins extracellularly in
cially important to colonies inhabiting quiet water. The the cardia and central stomach, and is completed intra-
generation of strong excurrent water flow away from the cellularly in the cecum. Food is moved through the gut
colony surface helps to push nonfood material and feces by peristalsis and cilia. Undigested material is rotated
far enough to reduce the possibility of recycling. In some and formed into a spindle-shaped mass by the cilia of
ectoprocts, such as Cauloramphus spiniferum, large parti- the pylorus and then passed to the rectum for expulsion.
18 CHAPTER TWENTY-ONE

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Figure 21.12 (A) Lophophoral movements in some

ectoprocts are a method of “scanning” for food sources.
The lophophore is protracted, held erect, rocked and
rotated, and then withdrawn. (B,C) Interzooidal “coopera-
tion” in the production of feeding currents, including
“excurrent chimneys.” (B) Hippothoa. (C) Cauloramphus.
(D) Cooperative rejection of a large particle
(Cauloramphus). The particle is passed to an excurrent
chimney.

Circulation, Gas Exchange, and Excretion the brown body is housed within the gut of the new
Circulation of metabolites in single zooids is by diffu- zooid and is then expelled via the anus. Note that the
sion, because there is no structural system for this pur- new polypide forms entirely from the tissue compo-
pose. Given the small size of these animals, intrazooid nents of the cystid—that is, from the epidermis and
diffusion distances are small, and the coelomic fluid peritoneum of the body wall. In most stoloniferous
provides a medium for passive transport. Interzooid cir- ctenostomates the old cystid with its brown body drops
culation is facilitated by the confluent coelom in phylac- from the colony, and an entire new zooid regenerates
tolaemates, the cystid pores in stenolaemates, and the from the stolon. Cyclostomates and some other ecto-
funicular cords of most gymnolaemates. Gas exchange procts tend to form brown bodies within the coelom. In
occurs across the walls of the protracted parts of the all cases, it is presumed that metabolic wastes are pre-
polypide, particularly the lophophore, the tentacles pro- cipitated and concentrated in the brown bodies and
viding a very high surface area. Ectoprocts contain no thus eliminated or at least rendered inert.
respiratory pigments, and gases are carried in solution.
Metabolic waste products are accumulated and Nervous System and Sense Organs
transported by phagocytic coelomocytes. The elimina- In concert with their sessile lifestyle and the general re-
tion of these wastes is not fully understood, but appar- duction of the anterior end, the ectoproct nervous sys-
ently it occurs in part by the formation of structures tem and sense organs are predictably reduced. A neu-
called brown bodies. The appearance of brown bodies ronal mass, or cerebral ganglion, lies dorsally in the
is usually associated with the degeneration of polypides mesosome near the pharynx. Arising from this structure
in adverse or stressful conditions; this degeneration is is a circumenteric nerve ring. Nerves extend from the
followed by reformation of a new polypide. In most ring and ganglion to the viscera, and motor and sensory
gymnolaemates a brown body is left within the cystid nerves extend into each tentacle. Interzooidal nerve
following polypide degeneration, but in some cheilosto- fibers occur in some species, but their function remains
mates the new polypide regenerates in such a way that unclear. The only known receptors are tactile cells on the
 LOPHOPHORATES 19

UNCORRECTED PAGE PROOFS

usually have well developed ocelli and are positively
phototactic while free swimming. Settlement is often
accompanied by a shift to a negative phototaxis.

Reproduction and Development

As in most colonial animals, asexual reproduction is
an indispensable part of the life history of ectoprocts
and is responsible for colony growth and regeneration
of zooids. Except for the unique cases of polyembry-
ony in stenolaemates (see below), each colony begins
from a single, sexually produced, primary zooid called
the ancestrula (Figure 21.14A). The ancestrula under-
goes asexual budding to produce a group of daughter
zooids, which themselves subsequently form more
buds, and so on. The initial group of daughter zooids
may arise in a chainlike series, a plate, or a disc; the
budding pattern determines the growth form of the
colony and is highly variable among species.

Asexual reproduction
Budding involves only elements of the body wall. In
most gymnolaemates a partition forms that isolates a
small chamber, the developing bud, from the parent
Figure 21.13 Digestive tract of Cryptosula pallasiana. zooid. The bud initially includes only components of
The arrows show food movement caused by ciliary action.
the cystid and an internal coelomic compartment. A
new polypide is then generated from the living tissues
of the bud (the epidermis and the peritoneum). The epi-
dermis and peritoneum invaginate, the former produc-
lophophore and on avicularia. The planktonic larvae of ing the lophophore and the gut. The peritoneum pro-
at least some ectoprocts exhibit a marked negative geot- duces all of the new coelomic linings and the funiculus.
axis prior to settling. Experiments suggest that this geo- Budding in phylactolaemates and stenolaemates is sim-
taxis is a direct response to gravity, but the mechanism ilar, except that the polypide develops first and is then
mediating this phenomenon is unknown. Larvae also encased by a new cystid wall.

Figure 21.14 Asexual reproduction in ectoprocts.

(A) Initial colony formation by repeated budding from
the ancestrula in Metrarabdotos. (B) The hooked stato-
blast of Cristatella. (C) Germination of new zooids
from the statoblast of Lophopus.
20 CHAPTER TWENTY-ONE

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Figure 21.15 General anatomy of a phylactolae-
mate zooid. Note the positions of the bud, stato-
blasts, gonads, and brood pouch.

of zooids of one sex or, more commonly, may include

both male and female individuals. Gametes usually
arise from transient patches of germinal tissue devel-
oped from special areas of the metacoel peritoneum or
the funiculus (Figures 21.9, 21.10, and 21.15). Only in the
stenolaemates is any real “organ” present; that is, the
testis is surrounded by a discrete cellular lining.
Gametes are proliferated into the metacoel and migrate
to the mesocoel prior to release. Sperm migrate into the
coelomic lumina of the tentacles and, at least in some
species, escape through special coelomopores on partic-
ular tentacles. A few cheilostomates (e.g., Electra and
Membranipora) exhibit free spawning of eggs as well as
of sperm, and fertilization and development are fully
external. In all other ectoprocts thus far studied, the ova
are retained by the parental zooids and brooded at least
during early ontogeny.
In those gymnolaemates that release their ova to the
sea water or to some external brooding area, the eggs
are shed from the mesocoel through an opening called
the supraneural pore located between the bases of two
tentacles. In some species this pore is elevated on a
pedestal called the intertentacular organ (Figure
21.10A). A few ctenostomates (e.g., Nolella and Victorella)
retain the ova within the coelom, where development
takes place. Stenolaemates and phylactolaemates brood
their embryos, the former in special individuals called
gonozooids that are modified by loss of the polypide,
and the latter in embryo sacs produced by invagina-
In addition to budding, freshwater ectoprocts (Phy- tions of the body wall (Figure 21.15).
lactolaemata) reproduce asexually by the formation of A variety of brooding methods occurs among gym-
statoblasts (Figures 21.5, 21.14B,C, and 21.15). These nolaemates, usually involving the formation of an exter-
structures are extremely resistant to drying and freez- nal brooding area called an ovicell, or ooecium (see
ing, and are often produced in huge numbers during Figure 21.7E). The most detailed and complete studies
adverse environmental conditions. Statoblasts generally on the formation and functioning of these structures
form on the funiculus of an autozooid and include peri- have been done by R. M. Woollacott and R. L. Zimmer
toneal and epidermal cells plus a store of nutrient mate- (see references) on the cheilostome Bugula neritina. In
rial. Each cellular mass secretes a pair of chitinous pro- this species, and probably many others, the ovicell de-
tective valves, differing among species in shape and velops from evaginations of the body wall of the parent
ornamentation. The parent colony usually degenerates, autozooid. One of these evaginations is the ooecial vesi-
freeing the statoblasts. Some statoblasts sink to the bot- cle, the lumen of which is confluent with the coelom of
tom, but others float by means of enclosed gas spaces. the maternal zooid. The other evagination is called the
Some bear surface hooks or spines and are dispersed by ooecial fold; this structure forms a hoodlike covering of
passive attachment to aquatic animals or vegetation. the ovicell. The embryo develops between the ooecial
With the return of favorable conditions, the cell mass vesicle and fold (Figure 21.16). In many species the
generates a new zooid, which sheds its outer casing and coelomic connection probably provides an avenue for
attaches as a functional individual. nutrient transfer from parent to embryo. In B. neritina an
actual tissue union develops between the epithelium of
Sexual Reproduction. the ooecial vesicle and funicular extensions of the parent
Most ectoprocts are hermaphroditic, and each zooid is autozooid, producing a kind of placental system.
capable of producing sperm and eggs. The colonies of Ectoprocts undergo radial, holoblastic, nearly equal
dioecious species (e.g., some chelostomates) may consist cleavage to form a coeloblastula. Subsequent develop-
 LOPHOPHORATES 21

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In phylactolaemates the coeloblastula develops into a
cystid-like stage lacking endoderm and then generates a
polypide in a fashion similar to bud formation. This
zooid precursor is ciliated and escapes the embryo sac
for a short swimming life before settling and attaching.
The embryos of stenolaemates cleave to form a hollow
ball, probably homologous to a coeloblastula. At this
point, however, the embryo undergoes a budding
process, forming secondary embryos, which in turn bud
tertiary embryos. In some cases hundreds of small,
solid, asexually produced embryos may result from a
single primary ball of cells. This phenomenon of poly-
embryony is unique to these animals and may represent
a heterochronic displacement of the usual asexual bud-
ding process of other ectoprocts. Each embryo develops
cilia and escapes as a simple “larva,” which settles and
undergoes a metamorphosis similar to that described
below for gymnolaemates.
Figure 21.16 An ooecium (ovicell) of Bugula neritina. The coeloblastulae of gymnolaemates undergo gas-
Note the tissue connection and coelomic communication
trulation by delamination; in this process four cells di-
with the parent zooid. See also Figure 21.9).
vide such that one of each pair of daughter cells is
shunted to the blastocoel as presumptive endoderm and
mesoderm. Free-swimming larvae are eventually pro-
ment differs greatly among groups, but in all cases it in- duced. Many of the species that free spawn have a char-
volves a free-swimming dispersal form. Thus, develop- acteristic, flattened, triangular larva called a cypho-
ment is either fully indirect (in those few species that nautes (Figure 21.17A). These larvae have a functional
free spawn) or mixed, with a planktonic stage following gut and may remain in the plankton for months, where-
a period of brooding. Very little solid information exists as the larvae of brooding species lack a digestive tract
on the derivation and fates of germ layers in ectoprocts. and lead very short, pelagic lives (Figure 21.17B,C).
This is especially true for mesoderm and coelomic lin- Despite these differences, gymnolaemate larvae have
ings. It appears certain, however, that there is no indica- some fundamental similarities. For example, they char-
tion of a 4d mesentoblast precursor for mesoderm, or acteristically possess a sensory pyriform organ complex
any other convincing evidence of a protostome affinity. and a pouchlike adhesive sac, both of which are impor-
tant in settling and metamorphosis (Figure 21.17). Some
ctenostomate ectoprocts produce nonfeeding vesicular-
iform larvae (see Zimmer and Woollacott 1993).
As mentioned earlier, ectoproct larvae are at first pos-
itively phototactic, and most possess pigment spots that

Figure 21.17 Ectoproct larvae. (A) The cyphonautes

larva of Membranipora. The arrows indicate the direction
of the feeding currents. (B) Nonfeeding larva of
Alcyonidium. (C) Nonfeeding larva of Bugula.
22 CHAPTER TWENTY-ONE

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are thought to be light sensitive. The pigment spots are The Brachiopods
ciliary in origin, supporting further the deuterostome al-
liance of the ectoprocts. Following a planktonic phase, Members of the phylum Brachiopoda (Greek brachium,
the larvae usually become negatively phototactic and “arm”; poda, “feet”) are called the lamp shells (Box 21C
swim toward the bottom. Once in contact with the sub- and Figure 21.18). All are solitary, marine, benthic crea-
stratum, the pyriform organ complex is apparently used tures. The body, including the lophophore, is enclosed be-
to test for chemical and tactile cues reflecting the suit- tween a pair of dorsoventrally oriented valves. Most bra-
ability of the substratum for settling. Once a proper sur- chiopods are attached to the substratum by a fleshy
face has been “selected,” the adhesive sac everts and se- pedicle (Figure 21.18). Some species lack a pedicle (e.g.,
cretes sticky material for attachment. After attachment, Crania), and these usually cement themselves directly to a
there is a remarkable reorganization of tissue positions hard substratum. On the other hand, some species that
accompanied by histolysis of various larval structures. possess a pedicle do not form permanent attachments,
The metamorphosed larva then generates the primary such as Magadina cumingi, which lies free, and Lingula,
zooid, or ancestrula. The most detailed account of this which anchors in loose sand (Figure 21.18B). A few
process is, again, by Woollacott and Zimmer (1971) for species possess both unattached and attached popula-
Bugula neritina. tions (e.g., Neothyris lenticularis and Terebratella sanguinea).

(A) (B)
(C) (D)

(E)

(F)

(H)

(G)

Figure 21.18 Representative brachiopods.

(A) Laqueus (class Articulata), with its valves
gaping and revealing the lophophore. (B) Glottidia
(class Inarticulata), removed from its burrow. (C)
Lingula (class Inarticulata) in feeding posture. The
arrows indicate the direction of water flow. (D) The
articulate Hemithyris. (E,F) Inarticulates Discinisca
and Pelagodiscus. (G) Marginifera, a spinose
Permian brachiopod. (H) Terebratalia (Articulata).
 LOPHOPHORATES 23

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The shells are usually unequal, except in some In-
articulata like Lingula and Glottidia, and are attached to BOX 21C Characteristics of the
one another posteriorly either by a tooth-and-socket Phylum Brachiopoda
hinge (Articulata) or simply by muscles (Inarticulata).
Brachiopods normally “sit” ventral side up, the pedicle 1. Trimeric, enterocoelic, coelomate lophophorates
arising from the ventral or pedicle valve; the dorsal 2. Epistome present, with or without coelomic
shell is called the brachial valve (Figures 21.19A and lumen
21.21A).
3. Body enclosed between two shells (valves), one
Most brachiopods measure 4 to 6 cm along the great- oriented dorsal and one ventral
est shell dimension, but range from 1 mm to over 9 cm
in extreme cases. Although they are known from nearly 4. Usually attached to the substratum by a stalk,
or pedicle
all ocean depths, they are most abundant on the conti-
nental shelf. The approximately 335 living species repre- 5. Valves lined (and produced) by mantle lobes
sent a small surviving fraction of the more than 12,000 formed by outgrowths of the body wall and
extinct species that have been described. Their rich fossil creating a water-filled mantle cavity
record dates back at least 600 million years. Brachio- 6. Trimeric condition partially obscured by modi-
pods, especially articulates, were among the most abun- fied body form
dant animals of the Paleozoic, but they declined in num- 7. Lophophore circular to variably coiled, with or
bers and diversity after that time. Thayer (1985) has without internal skeletal support
presented experimental evidence that competition with
8. Gut U-shaped; anus present or absent
epibenthic bivalve molluscs was at least partly responsi-
ble for the reduction in brachiopod diversity following 9. One or two pairs of metanephridia
their Paleozoic success. 10. Circulatory system rudimentary and open
11. Most are dioecious and undergo mixed or indi-
PHYLUM BRACHIOPODA rect life histories, with lobate larva
Class Inarticulata: Valves not hinged, attached by muscles only; 12. Gametes develop from transient gonadal tissue
valves of organic composition, including chitin, or else cal- on peritoneum of metacoel
careous; pedicle (absent in a few species) usually with intrin-
sic muscles and a coelomic lumen; epistome with coelomic 13. Cleavage holoblastic, radial, and nearly equal;
channels confluent with lophophoral mesocoel; lophophore Coeloblastulae usually gastrulate by invagina-
without internal skeletal support; anus present. Two orders, tion; blastopore closes and mouth forms secon-
Lingulida and Acrotretida, comprising about 45 extant species. darily (as does anus)
(e.g., Crania, Discinisca, Glottidia, Lingula, Pelagodiscus) 14. Solitary, benthic, marine
Class Articulata: Valves articulate by tooth-and-socket hinge;
valves composed of scleroprotein and calcium carbonate;
pedicle usually present, but lacking muscles and coelomic
lumen; epistome small and tissue filled; lophophore generally tae, extending from their inner surfaces nearly to the pe-
with internal supportive elements; gut ends blindly, anus lack-
ing. Three extant orders: Rhynchonellida, Terebratulida, and riostracum and containing tiny tissue extensions of the
Thecideidina, with just over 290 species. (e.g., Argyrotheca, mantle (Figure 21.19B). The function of these mantle
Dallina, Gryphus, Hemithyris, Lacazella, Laqueus, Liothyrella, papillae is unknown, but some workers have suggested
Magellania, Thecidellina, Terebratalia, Terebratella, Terebratuli- that they might serve as areas for food storage and gas
na, Tichosina) exchange, or in some way deter the activities of borers.
Shells that lack perforations are termed impunctate.
The Body Wall, Coelom, and Support The soft mantle lobes line and are attached to the
The shells of brachiopods comprise an outer organic pe- shells and form the water-filled mantle cavity, which
riostracum and an inner structural layer or layers com- houses the lophophore. The mantle edges often bear
posed variably of calcium carbonate, calcium phosphate, chitinous setae, which may protect the fleshy tissue and
scleroproteins, and chitinophosphate. Various spines are perhaps serve to prevent the entrance of large particles
present in some species as outgrowths of the perios- into the mantle cavity.
tracum and serve to anchor the animals in place (Figure The epidermal cells of the mantle lobes and general
21.18). In a fashion similar to that of molluscs, brachio- body surface vary from cuboidal to columnar and are
pod shells are secreted by mantle lobes, which are densely ciliated on the lophophore. Beneath the epider-
formed as outgrowths of the body wall (Figure 21.19). mis is a connective tissue layer of varying thickness,
The periostracum is secreted by the mantle edges, and which houses longitudinal muscle fibers where the
the inner shell layer by the general mantle surface. The body is not attached to the valves. The inner surface of
shells of many brachiopods bear perforations, or punc- the body wall is lined by peritoneum, which forms the
24 CHAPTER TWENTY-ONE

UNCORRECTED PAGE PROOFS

(B)
Setae

Dorsal
shell valve

Mantle

Mantle
vessels
Lophophores

Adductor
muscle

Digestive
gland

Adjustor
muscle

Gonad

Figure 21.19 Anatomy of brachiopods. (A) The articu- Intestine

late brachiopod Terebratalia(cutaway view). (B) The inartic-
ulate brachiopod Lingula (ventral valve removed). (C) The
edge of the shell and mantle of an articulate (longitudinal Diductor muscle
Pedicel
section). (D) The mantle edge of Notosaria (inside view).
 LOPHOPHORATES 25

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Figure 21.20 Feeding currents in
brachiopods. (A) Feeding currents
(arrows) of Waltonia. (B) Lophophoral
tentacles (section). The water (arrows)
passes over lateral ciliary bands. (C) A
portion of a lophophore. Food particles
are transported along tentacles and the
brachial food groove (arrows).

outer boundary of the coelom. Being folds of the body

wall, the mantle lobes contain extensions of the coelom,
called mantle canals (Figure 21.19C).
The pedicle is an outgrowth of the body wall, arising
from the posterior area of the ventral valve (Figure
21.18 and 21.19A). In inarticulates it contains all the
usual layers beneath the epidermis, including connec-
tive tissue, muscles, and a coelomic lumen. However,
the pedicle of articulates lacks muscles and a coelomic
cavity. In the latter case the pedicle is operated by ex-
trinsic muscle bands from the body wall itself. In bra-
chiopods that attach firmly, the tip of the pedicle bears open the valves (Figure 21.21A). The tooth-and-socket
papillae or finger-like extensions that adhere tightly to hinges prevent a large gape. The adductor muscles in-
the substratum. clude both striated and smooth fibers such that the valves
The coelomic system of brachiopods includes the can be quickly closed and then held together for long pe-
typical mesocoel and metacoel as the lophophoral and riods of time. Inarticulates lack a hinge and do not pos-
body coeloms, respectively. The epistome is solid in the sess diductor muscles. Instead, the gape is produced by
articulates, but in inarticulates it contains a protocoel retraction of the body, an action that increases the internal
that is confluent with mesocoel. The coelomic fluid in- pressure in the coelomic fluid and forces the valves apart.
cludes various coelomocytes, some of which contain Adductor muscles are used to close the valves.
hemerythrin. Feeding currents are generated by the lophophoral
cilia. Specific incurrent and excurrent flow patterns
The Lophophore, Feeding, and Digestion occur, varying with shell morphology and the shape and
Like that of phoronids and ectoprocts, the lophophore orientation of the lophophore. In any case, water is di-
of brachiopods comprises a ring of tentacles surround- rected over and between the tentacles before passing out
ing the mouth. In brachiopods however, the lophophore of the mantle cavity (Figure 21.20A). Each tentacle bears
is produced as a pair of tentacle-bearing arms that ex- lateral and frontal ciliary tracts (Figure 21.20B). The later-
tend anteriorly into the mantle cavity. The overall shape al cilia of adjacent tentacles overlap and redirect food
of the lophophore varies among taxa from a simple cir- particles from the water to the frontal cilia by beat rever-
cular or U-shape to those with highly coiled arms sal. The frontal cilia beat toward the base of the tentacles,
(Figure 21.19 and 21.20). The brachiopod lophophore helping to direct trapped food. The lophophoral ridge,
also differs in that it is always contained within the pro- or brachial axis, bears a brachial food groove within
tection of the valves and is essentially immovable. In which food material is moved to the mouth (Figure
inarticulates, the lophophore and tentacles are held in 21.20C). Brachiopods feed on nearly any appropriately
position by coelomic pressure, whereas in articulates the small organic particles, especially phytoplankton.
tentacle-bearing ridge includes supportive skeletal ele- The digestive system is U-shaped (Figure 21.19, and
ments. In addition, the dorsal valve often bears inward- 21.21B,C). The mouth is followed by a short esophagus,
ly directed ridges and grooves that help support and which extends dorsally and then posteriorly to the
position the lophophore. stomach. A digestive gland covers most of the stomach
In order to pass a water current through the mantle and connects to it via paired ducts. The intestine extends
cavity, the two valves must be opened slightly. The mech- posteriorly, where it ends blindly in articulates or re-
anisms of valve operation differ between members of the curves as a rectum terminating in an anal opening in
two classes. Articulate brachiopods possess several sets inarticulates. In the latter case the anus opens either me-
of muscles including a pair of diductor muscles, which dially or on the right side of the mantle cavity. The ab-
26 CHAPTER TWENTY-ONE

UNCORRECTED PAGE PROOFS

Figure 21.21 (A) An articulate brachiopod (ventral side
up; cutaway view). Note the major muscles that operate
the valves. (B) The complete gut of an inarticulate. (C) The
blind gut of an articulate. (D) The nervous system of
Magellania. Note the dorsal and ventral aspects on the left
and right sides of the drawing, respectively.

sence of an anus is almost certainly a secondary loss in Brachiopods possess one or two pairs of meta-
the articulates, and may be associated with the evolu- nephridia, with the nephrostomes opening to the meta-
tion of the articulate hinge, which restricts the posterior coel. The nephridioducts exit through pores into the
flow of water from the mantle cavity. mantle cavity. The nephridia function as gonoducts as
Little is known about digestion in brachiopods, but well as discharging phagocytic coelomocytes that have
some work on Lingula (Chuang 1959) indicates that it accumulated metabolic wastes.
occurs intracellularly in the digestive gland.
Nervous System and Sense Organs
Circulation, Gas Exchange, and Excretion The nervous system of brachiopods is somewhat reduced.
The brachiopod circulatory system is open, much re- A dorsal ganglion and a ventral ganglion lie against the
duced, and largely unstudied. A contractile heart lies in esophagus and are connected by a circumenteric nerve
the dorsal mesentery just above the gut (Crania possess- ring. Nerves emerge from the ganglia and nerve ring and
es several “hearts”). Leading anteriorly and posteriorly extend to various parts of the body, especially the muscles,
from the heart are channels bounded only by mesentery mantle, and lophophore (Figure 21.21D).
peritoneum, thus no true vessels are present. These As usual, the array of sense organs in these animals is
channels branch to various parts of the body, but the compatible with their lifestyle. The mantle edges and
pattern of circulation is not fully understood. It appears setae are richly supplied with sensory neurons, proba-
that the blood is separate from the coelomic fluid, al- bly tactile receptors. There is also evidence that bra-
though both contain certain similar cells. The function chiopods are sensitive to dissolved chemicals, perhaps
of the circulatory system is thought to be largely restrict- through surface receptors on the tentacles or mantle
ed to nutrient distribution. edge. Members of at least one species of Lingula possess
Gas exchange probably occurs across the general a pair of statocysts, which are associated in this burrow-
body surface, especially the tentacles and mantle. These ing form with orientation in the substratum.
structures not only provide large surface areas but are
also sites over which water moves and is brought close Reproduction and Development
to underlying coelomic fluid. This general arrangement Asexual reproduction does not occur in brachiopods.
and the presence of hemerythrin in certain coelomo- Most species are dioecious, with gametes developing
cytes suggest that the coelomic fluid, not the blood, is from patches of transient, gonadal tissue derived from
the medium for oxygen transport. the metacoel peritoneum. Gametes are released into the
 LOPHOPHORATES 27

UNCORRECTED PAGE PROOFS

Figure 21.22 Brachiopod lobate
larvae and metamorphosis. (A) Larva
of the inarticulate Lingula. (B) Lingula
larva at the time of settlement but
before extension of the pedicle. (C–F)
Articulates. (C) Larva of Waltonia. (D)
Larva of Argyrotheca. (E) Newly set-
tled Terebratella after flexion of the
mantle lobes and initial shell produc-
tion. (F) Events in the metamorphosis
of an articulate. The mantle lobes
flex to cover the visceral mass and
the developing lophophore.

metacoel and escape through the nephridia. In most plied the term lobate larva—in reference to the body re-
cases both eggs and sperm are shed freely and fertiliza- gions visible as primordia at this stage and to the exist-
tion is external. A few species, however, brood their em- ing terminology traditionally used to describe these re-
bryos until the larval stage is reached. In these cases gions. The larvae of articulates and inarticulates differ
sperm are picked up in the water currents of females morphologically and in the events at the time of settling.
and the eggs are retained in a brooding area, where they In inarticulates, such as Lingula, the larva is constructed
are fertilized. Argyrotheca, for example, broods its em- much like the adult, except the pedicle is curled inside
bryos in the enlarged nephridia. Others retain their em- the mantle cavity and the body and lophophoral lobes
bryos on the arms of the lophophore, in special regions are disproportionately large compared with the mantle
of the mantle cavity, or in modified depressions in a lobes (Figure 21.22A,B). Thus the lophophore can be
valve. protruded out from between the mantle lobes and func-
Cleavage is holoblastic, radial, and nearly equal; it tion to propel and feed the larva. The mantle lobes lie
leads to the formation of a coeloblastula. Gastrulation is dorsoventrally on the body. Shell secretion commences
by invagination, except in the brooding form Lacazella, early and, with added weight, the larva sinks, the pedi-
where it apparently occurs by delamination. The blasto- cle is extended, and the juvenile brachiopod assumes
pore closes and the mouth forms secondarily. The anus, benthic life. Thus, there is no drastic metamorphosis at
when present, breaks through late as the gut grows and the time of settling.
approaches the body wall. Mesoderm and coelom for- The free-swimming larva of articulates is regional-
mation are clearly enterocoelic. All of these develop- ized into an anterior lobe, a mantle lobe, and a pedun-
mental features bear witness to the deuterostome affini- cular, or pedicle, lobe (Figure 21.22C,F). The mantle
ties of the Brachiopoda. flaps are reflexed posteriorly along the sides of the pre-
Whether the developmental pattern is mixed or fully sumptive pedicle, rather than anteriorly over the body
indirect, all brachiopods eventually enter a free-swim- as seen in inarticulates. After a short larval life of 1 or 2
ming larval stage (Figure 21.22), to which we have ap- days, the larva settles and metamorphoses. As the pedi-
28 CHAPTER TWENTY-ONE

UNCORRECTED PAGE PROOFS

cle attaches to the substratum, the mantle lobes flex for- That ancestor may have been a trimeric, coelomate, in-
ward over the anterior lobe. The now- exterior surfaces faunal burrower. In any case, the ancestor probably
of the mantle lobes commence secretion of the valves, evolved during the Precambrian as one evolutionary ex-
while the anterior lobe differentiates into the body and periment with a coelomate bauplan. The first lopho-
the lophophore. phorate was probably phoronid-like and became adapt-
ed to tube dwelling and feeding above the substratum.
Modern phoronids may have changed little from this
Lophophorate Phylogeny tube-dwelling protolophophorate.
The origin of the Ectoprocta clearly involved a reduc-
Despite continuing arguments, we remain convinced tion in body size and the development of colonial
that the lophophorates are a monophyletic clade and habits. The epidermal secretions became compartmen-
that they are deuterostomes. In addition to the lopho- talized, with the exploitation of asexual budding as a
phore, the phyla Phoronida, Ectoprocta, and Brachio- means of colony formation. The acquisition of a re-
poda are united by their possession of U-shaped diges- tractable lophophore allowed protection of the soft ten-
tive tracts, peritoneal gonads, metanephridia (absent in tacles. The absence of nephridia and circulatory struc-
ectoprocts), a diffuse nervous system, epistemial flaps, tures provides space for the retraction of the polypide;
and a tendency to secrete outer casings. We view these short diffusion distances are associated with small size
features as homologous within this clade but plesiomor- and the disappearance of these systems. Without
phic or convergent with similar conditions in some nephridia as a means of gamete release, other avenues
other phyla. As discussed later in this section, each of of egg and sperm escape arose in the form of coelomo-
the three lophophorate phyla displays enough derived pores from the mesocoel and communication between
character states to merit separate taxon status, but the the metacoel and the mesocoel.
idea of a “superphylum” (perhaps Lophophorata) may The origin of the brachiopods is marked by the ap-
be warranted. pearance of several novel features largely associated
Zimmer (1973) has critically made the case for the with the evolution of mantle folds, their secretion of
deuterostome nature of the lophophorates. They all show valves, and the enclosure of the lophophore and body
radial cleavage, enterocoely, and (except for the proper within the mantle cavity. The lophophore lost
phoronids) a mouth that is not derived from the blasto- most of its hydraulic qualities and became more or less
pore. In addition, the body plan and coelomic arrange- stationary, held by various structural support mecha-
ment is clearly trimerous or obviously derived therefrom. nisms. The circulatory system was reduced. The origin
An alliance between the groups Ectoprocta and of a pedicle allowed a means of attachment in these soli-
Entoprocta, proposed by Nielsen, is rejected on the basis tary animals, supporting the body off the substratum.
of incompatibility with the idea of lophophorate unity The first brachiopods may have been lingulid types that
and on direct comparative grounds. Entoprocts do not used the pedicle for anchorage in soft substrata.
possess a lophophore as we have defined it. Further- Valentine (1973, 1975) has attempted to support a
more, they lack any vestiges of a coelom and trimeric polyphyletic origin for the brachiopods, but he does rec-
body plan. The feeding currents are virtually opposite ognize a monophyletic lophophorate clade, somewhat
in the two groups, and the methods of food capture and as we have described here. However, Rowell’s (1982)
transport are entirely different. Entoprocts possess duct- cladistic treatment of the brachiopods, living and ex-
ed gonads, ectoprocts do not. Cleavage in entoprocts is tinct, presents a convincing case for monophyly, al-
spiral, whereas it is radial in ectoprocts. Larval forms though his subgroups do not correspond exactly with
and particularly metamorphosis are clearly different in the Articulata–Inarticulata division.
the two groups. More important, if the two groups are The origin of the lophophore allowed various av-
related, then they must share common (homologous) enues of escape from the infaunal life of their
characteristics—that is, synapomorphies. The similari- Precambrian ancestor and the exploitation of three dif-
ties pointed out by Nielsen are superficial and common ferent lifestyles, all involving suspension feeding.
to many colonial sessile animals (e.g., budding, meta- However, in spite of the differences among the three
morphosis, and life cycles). The U-shaped guts are con- phyla, and the unique qualities of each, evolution within
vergent adaptations to zooid life in “boxes”—no other the lophophorate clade remains obscure. Without mak-
condition would function. Thus, in the absence of unify- ing assumptions about the first lophophorate, the three
ing synapomorphies and the presence of multiple and taxa appear to have emerged separately from a com-
significant differences, we can only consider one conclu- mon, lophophore-bearing ancestor (Figure 21.23A).
sion: the two groups are unrelated. Only by designating additional ancestral features can
The origin of the lophophorates is puzzling, largely we eliminate the trichotomy. For example, if we assume
because it is tied, in part, to the origin of the entire that the ancestral lophophorate was phoronid-like, with
deuterostome lineage, which is itself very uncertain. a complete circulatory system, then the ectoprocts and
Most workers agree that the phoronids show the least brachiopods may form a distinct clade defined by the
amount of change from the presumed ancestral form. reduction and loss of the circulatory system (Figure
 LOPHOPHORATES 29

UNCORRECTED PAGE PROOFS

(A) (B)
Phoronida Ectoprocta Brachiopoda Phoronida Ectoprocta Brachiopoda
6
5 9
4 8
3 7

1
1

Figure 21.23 Lophophorate phylogeny. (A) Without the circulatory system (2). The ectoprocts and brachiopods
assumptions about the ancestral form, other than the ori- are subsequently defined by their unique synapomorphies.
gin of the lophophore (1), a trichotomy results where each For ectoprocts these are: (3) colonial lifestyles, (4) retract-
group arises independently from the ancestor. (B) Assum- able lophophore, (5) loss of nephridia, and (6) production
ing a phoronid-like ancestor, the ectoprocts and bra- of brown bodies. For brachiopods: (7) unique mantle and
chiopods form a clade defined in part by the reduction of shell, (8) lophophoral skeleton, and (9) pedicle.

21.22B). Such assumptions carry implications about the closely aligned with the protostomes than the deuteros-
deuterostome lineage in general and are explored more tomes, despite embryological and anatomical evidence
in Chapter 24. to the contrary (Halanych et al. 1995; Mackey et al.
There remain, of course, many questions and alterna- 1996). Some other workers (see Jeffries 1986) view the
tive hypotheses on the matter of lophophorate evolu- lophophorates as somewhat intermediate between the
tion. Not all zoologists are convinced that these animals protostomes and deuterostomes (see Chapter 23). No
are deuterostomes. For example, recent 18S rDNA mol- doubt these debates will continue at least until the third
ecular studies suggest that the lophophorates are more edition of this book appears.

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