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Barentsiidae and Loxosomatidae




Sin Ki Debbie Leung 2020

Summary

Entoprocta (Greek entos, “inside”; proktos, “anus”), also known as Kamptozoa (Greek kamptos, “bent”), is a small phylum of microscopic, sessile, filter-feeding, largely marine goblet worms that comprise of around 180 species in four families: Barentsiidae, Loxokalypodidae, Loxosomatidae and Pedicellinidae (Iseto et al., 2008). Since both Barentsiidae (Figure 1) and Loxosomatidae (Figure 2) occur in eastern Australia, this species page will give a broad overview of this phylum with particular focus on comparing and contrasting between the two families (Table 1).


Introduction to Entoprocta


Category

Barentsiidae

Loxosomatidae

Physical Appearance

Calyx and stalk in zooids are clearly separated by a cuticular septum and with discontinuous musculature; stalks have stiff segments and muscular joints; contains stolon as an attachment structure

Calyx and stalk in zooids are connected by continuous musculature

Ecology

Coloniality; encrusting living and non-living substrata

Solidarity; in commensal relationships with specific hosts 

Life History

Sexual reproduction: gonochoristic and/or hermaphroditic zooids and/or colony

Asexual reproduction: budding from stolon

Sexual reproduction: protandrous hermaphrodites

Asexual reproduction: budding from calyx

Behaviour

Able to regenerate calyces and change sex based on external conditions

Some capable of movement after adulthood; only Loxosomella antarctica  can regenerate calyx

Development

Organs rotate 180 degrees upon settlement of trochophore larvae; stalk is differentiated into muscular basal and non-muscular distal portion

Some trochophore larvae do not rotate; also produce appropriately oriented asexual buds

Anatomy

Contains star cell complex near the stalk-calyx junction and accessory glial cells; ingested nutrients not shared between zooids within the colony; subenteric ganglion with paired lateral lobes 

Lacks star cell complex; subenteric ganglion with two separate lateral lobes 


Distribution

Widely distributed especially in North America, Europe and Indo-Pacific; found in both Coral Triangle and southeast Australia

Widely distributed especially in Europe; found in Coral Triangle and northern Australia

Systematics

Phylum: Entoprocta (Nitsche, 1869)

Family: Barentsiidae (Emschermann, 1972)

Paraphyletic; includes 2 genus (Barentsia and Urnatella) with 20 species

Phylum: Entoprocta (Nitsche, 1869)

Family: Loxosomatidae (Hincks, 1880)

Paraphyletic; with 5 genus (Loxosoma, Loxosomella, Loxomitra, Loxocorone and Loxomespilon) over 140 species

Conservation

IUCN Status: Not evaluated/threatened

IUCN Status: Not evaluated/threatened

Table 1. Summary table of the main differences between the Barentsiidae and Loxosomatidae families within Entoprocta

1
Figure 1
2
Figure 2

Physical Description

Entoprocts include both colonial and solitary species that consist of individual zooids attached to the substratum or a stolon with a stalk. Though technically bilateral, each zooid assumes a functionally radial form as it is a globular to flattened body where the ventral side is a cuplike calyx with a crown of ciliated tentacles. The tentacles, ranging from 8 to 30 and usually of the same length, are evenly spaced throughout the crown, giving it a bilateral symmetry. The body contains a U-shaped ciliated gut with a funnel-shaped oesophagus, c tubular rectum, a conical intestine and a circular stomach. The mouth is located at the base of the tentacles on the anterior side of the cavity, with the anus on the opposite side at the rim of the tentacle crown (Nielsen, 2013). The vestibule, also called atrium, is the concavity between the mouth and the anus. A band of separate cilia encircles the mouth to form a food grove along the tentacle bases with extensions on the atrial side of the tentacles. The band of compound cilia surrounding the atrium onto each tentacle follows the food groove to the mouth at the anal side of the atrium. The body also contains a dumbbell-shaped neural ganglion situated at the upper side of the stomach near the oesophagus as well as paired gonads and protonephridia just behind the ganglia. The stalk, which varies greatly within the phylum, is an outgrowth of the calyx (Brusca and Brusca, 2003). 


The distinguishing features between entoproct families are the arrangement of the body musculature, the form of the attachment structure, and budding patterns (Emschermann, 1985; Iseto, 2002). Barentsiidae are a colonial species with a muscular swelling at the base of the stalk (Figure 3a). Individuals in this colonial species may be several millimeters long (Nielsen, 2013). They also have a characteristic star-cell complex at the narrow transition between the body and stalk, with tips of the rays attached to the ectoderm. The stack of star-shaped cells in the complex contain pulsating myofilaments, creating movement in the narrow fluid-filled primary body cavity (Nielsen, 2010). Stalks differentiated into wide, muscular nodes and narrow, rigid, non-muscular rods. The stolons are cylindrical with incomplete septa between areas with zooids and areas without. On the other hand, Loxosomatidae encompasses all solitary species, which are usually less than 1mm long (Figure 3b). Some species have four longer tentacles at the oral end of the crown. The stalk ends basally in a muscular sucker, a elongate foot with two types of glands that are cemented to the substratum (Nielsen, 2013).



3
Figure 3

Ecology

Entoprocts display a bi-level functionality in marine food chains. They capture phytoplankton, diatoms, algae and organic particles via filter feeding through the water current using the cilia along their tentacles and they are fed on by larger marine animals such as nudibranchs, flatworms, crustaceans, sea urchins and mollusks (Canning and Carlton, 2000).


Barentsiidae are found naturally-occurring on diverse living and non-living benthic substrata, encrusting algae, dead corals, seaweed, rocks, stones, shells, and living animals like ascidians and bryozoans (Iseto, 2003; Wasson, 2002). For example, Barentsia hildegardae grows abundantly on solitary ascidians. In contrast, Loxosomatidae are often found on the body surfaces or inside the burrows or tubes of bottom dwelling marine invertebrates that produce water currents, for example ascidians, spiculids, polychaetes, sponges and bryozoans (Nielsen, 1964). A marked host specificity is characteristic of most epizoic Loxosomatidae species (Emschermann, 1993). For example, while the genus Loxosoma lives associated with polychaetes, Nielsen (1996) describes Loxosoma davenporti settling only inside the tubes of the polychaete Clymenella zonalid but never in Clymenella torquata. Other specific associations have also been proposed: Loxosomella antarctica in the brittle star Ophiurolepsis gelida (Emschermann, 1993), Loxosomello plakorticola in coral-reef demosponge Plakortis sp. (Sugiyama et al., 2010), and  Loxosomella nordgaardi in bryozoa Tegella armifera (Tamberg et al., 2013). The ecology of this relationship is said to be commensal where the host provides both mechanical shelter that protects the entoprocts from overgrowth by predators and other fouling organisms (Iseto 2005) and water current supplying food and oxygen for respiration and removing detritus for their minute symbionts (Iseto, 2005; Nielsen, 1964). 


Life History and Behaviour

Reproduction

Entoprocts have two reproductive modes: sexual reproduction via a larval stage and asexual budding. For sexual reproduction, sperms released into the water enter the female reproductive tract and fertilize the eggs in the ovaries or oviducts. During the passage of the zygote along the oviducts, they are covered with the secretion from the eosinophilous glands, forming a loose membrane. Cement glands then secrete stalks that adhere to the wall of the brood chamber in the anus by which the embryos get attached to (Brusca and Brusca, 2003).  Some females brood their fertilised eggs in the ovary, providing nutrition to the developing embryos from their placental cells. When they develop into trochophore-like larvae, they are released into the water column. The planktonic duration and dispersal distance of larvae remains unknown (Sugiyama et al., 2010). Most entoproct species are hermaphrodites, with colonial forms having either hermaphroditic or dioecious zooids where colonies may contain one or both sexes (Brusca and Brusca, 2003). In particular, Barentsiidae are reported to have three contrasting modes of sex: (1) comprehensively gonochronistic at both zooid and colony levels, (2) hermaphroditic at the colony level with gonochric zooids and (3) simultaneously hermaphroditic the zooid level (Wasson, 1997). On the other hand, Loxosomatidae species are generally protandrous hermaphrodites, with a discrete male stage followed by a female phase (Nielsen, 1971).

Asexual reproduction in entoprocts occurs through budding. Gut and atrial epithelium develop from ectodermal invaginations while the ectoderm of the bottom of the atrium give rise to ganglion and protonephridia (Nielsen, 2013). In Barentsiidae, colonial growth occurs by budding at the base of zooids, on various branches of the stalk or from the growing tips of stolons as zooids. Some even make hibernacula, which are thick-walled mono-or multilocular resting cytes at the ends of the short stolons that form zooids at germination (Nielsen, 2013). On the contrary, Loxosomatidae produce buds at a pair of laterofrontal or frontal areas of the stomach and release them from the parental calyx when all the organs are fully developed (Sugiyama et al., 2010). Surprisingly, some species of Loxosomella  and Loxosoma bud even at the larval stage. It is said that the larval epithelium above the prototroph gives rise to the buds, which detach from the larval body when fully grown. The body then disintegrates (Nielsen, 2013). These liberated buds can swim slowly with their tentacle cilia (Atkins 1932, Nielsen 1989), but their dispersal distance remains unknown (Sugiyama et al., 2010).

Development

Entoproct embryonic development is indirect with more or less typical trochophore larvae and follows the holoblastic, spiral cleavage pattern of protostomes, with the mesoderm originating from the 4d mesentoblast (Nielsen, 2013). At about the 56-cell stage, nonsynchronous divisions produce five quartets of micromeres, leading to the formation of a coeloblastula and gastrulation by invagination. When the embryos have fully developed, they are usually released as free-swimming, feeding larvae, with long pelagic planktotrophic phase. Like other trochophore larvae, entoproct larvae have equatorial ciliary bands used for feeding on suspending particles, apical and ventral sensory tufts, pigment-cup ocelli serving as light-sensing organs, digestive organs and a pair of protonephridia for waste excretion. When released into the water column, these larvae have the ability to orient themselves and sense specific settlement cues. When prompted to settle, they attach by the coronal ciliary band and undergo metamorphosis where the body mass experiences unequal growth to direct the ventral, vestibular surface away from the substrate (Brusca and Brusca, 2003). Moreover, some entoprocts also produce lecithotrophic or benthic crawling larvae with a large well-developed, ciliated, ventral foot, which have a free period of only a few hours.


Specifically, the trochophores of Barentsiidae retract the ventral side and attach to the substratum by secretions from the glandular cells above the contracted prototroch. The internal organs rotate 180 degrees along the dorsoventral axis, with the mouth, anus and gut turning to face the vestibular surface in front and the atrium opens with a series of surrounding small tentacles (Nielsen, 2013). This is followed by the differentiation of the stalk into a muscular basal section and a non-muscular distal section as well as the formation of the circulatory organ at the top. The cuticle above the atrium is shedded and small tentacles develope (Nielsen, 1971). On the other hand, the larvae of some Loxosomatidae species do not rotate when adhering to the substratum. For example, in some Loxosomella species, the larvae settle with glandular cells around the frontal organ, followed by metamorphosis through a retraction of the foot, a constriction of the prototroph and a reopening of the atrium surrounded with new tentacles (Nielsen 2013). Some, such as Loxosomella polita and Loxosomella vivipara, even produce an correctly oriented asexual buds that later becomes the adult upon settling (Nielsen, 1971). Other species with free-swimming larvae produce adult buds precociously that are formed earlier while the larvae are still in the brood chamber. They are held inside the larvae and are released by rupture of the body wall of larvae prior to settling (Shank, 2001). A reconstruction of the larva of a species each from the Barentsiidae and Loxosomatidae families are shown in Figure 4.



4
Figure 4

Behaviour

Though small and sessile, entoprocts exhibit various interesting behaviour, including locomotion and regeneration. While most movement in entoprocts happens in larval dispersal since they get attached to a substate with their foot after settlement, some adult individuals in the Loxosomatidae family can capable of movement, including gliding over, crawling on, detaching from and reattaching to the substratum with their foot, even after adulthood (Iseto 2002, Iseto & Hirose 2010). This has been observed in some Loxosomella species dwelling inside the tubes of marine annelids (Ramel, 2012). 


Moreover, entoprocts possess powers of regeneration. Under adverse environmental conditions, entoprocts may shed their calyces while the stalks and stolons remain alive. They will only regenerate new calyces when favourable conditions return. In Barentsiidae, zooids can change their sex after degeneration and regeneration of a calyx (Mukai & Makioka, 1980). While the sexual differentiation of a given calyx is irreversible, sex determination is not genetically fixed and occurs at the level of gonad-forming tissues instead of the whole zooid or calyx (Emschermann, 1985). Therefore, after calyx regeneration, the sex of a zooid can change according to the external conditions. To date, only one Loxosomatidae species, Loxosomella antarctica, is noted to be able to regenerate the entire calyx at the distalmost tip of the stalk epithelium, an adaption to the conditions of Antarctic life (Emschermann, 1993).

Anatomy and Physiology

Body Wall

The structure of the body wall in entoprocts is pseudocoelomate throughout the stalk, stolon, calyx and tentacles, consisting of one-layered epithelium with microvilli that penetrate the layer of crossing collagenous filaments (Nielsen, 2013). The calyx and stalk are clothed with a thin cuticle that does not extend over the ciliated portion of the tentacles and the vestibule. In Barentsiidae, the stalks and stolons have a thickened cuticle with chitin (Nielsen, 2013). Beneath the cuticle lies the epidermis of mostly cuboidal cells that scatter over the body surface. The epidermis is taller on the inner surface of the tentacles and heavily ciliated along the vestibular groove. The inner side of the epidermis contains musculature in the form of longitudinal bands. Though sparsely present in the calyx, they serve to retract or extend the tentacles, forming a sphincter that contracts the crown and curling the tentacles into the vestibule. Other muscles located within the stalk provide the ability to bend. As entoprocts do not have persistent body cavity, their pseudocoel is filled with mesenchyme cells and occupies the space between the body wall and digestive tract in the calyx as well as the interior of tentacles, stalks and stolon. The pseudocoel of tentacles contains free amoeboid cells while the pseudocoel of the stalk and stolon contains long tube cells. The pseudocoel of the calyx is separated from that of the stalk by the septum and cells blocking the central hole in the septum. Body support is provided by the mesenchyme and cuticle (Brusca and Brusca, 2003). 


Nervous System

Entoprocts have a greatly reduced central nervous system located in the cavity of the digestive tract. It has one main subenteric ganglion located ventral to the stomach, between the stomach and vestibular surface. The ganglion is bilaterally symmetrically and contains a pair of lateral lobes connected by a transverse commissure whose morphological integration varies within entroprocts (Borisanova et al., 2019). The paired lobes are in close proximity, forming a bilobate or oval ganglion in Barentsiidae (Hyman, 1951) whereas they are widely separated as two ganglia in Loxosomatidae (Harmer, 1885). The ganglion is said to contain a central neuropil and peripheral perikarya (Nielsem, 1997). However, some species of Barentsiidae, for instance Barentsia discreta, contain a second kind of accessory cells that are hypothesized to function as glial cells protecting the nerve cells (Borisanova et al., 2019). The ganglion also has three pairs of nerves extending to the internal organ. Each of them terminates in large ganglion cells in the tentacular membrane between the tentacle bases into adjacent tentacles. From the dorsal side of the subenteric ganglion, the three pairs of nerves lead to the calyx wall, stalk and adjacent gonads respectively. Though both Barentsiidae and Loxosomatidae have lateral and aboral paired nerves of the calyx, the aboral nerves terminate at the base in the former but extend into the stalk in the latter. Interestingly, nervous connections between zooids in the colonial species of the Barentsiidae has not been observed (Nielsen, 2013). Specific differences in the organization of the nervous system between Barentsiidae and Loxosomatidae are outlined in Figure 5.

Furthermore, entoprocts contain sense organs that include sensory tactile nerve cells. They consist of one or more bristles that proceed from a nerve cell to the epidermis. These unicellular tactile receptors are concentrated on the outer surface of the tentacles and along the calyx margin. In Loxosomatidae, ciliated papillae form the lateral sense organs that are located on the sides of the calyx near the oral end. Each consists of bristles lined by a ganglion connected to the subenteric ganglion through a nerve (Brusca and Brusca, 2003).



5
Figure 5

Digestive System

Entoprocts are sessile filter feeders. Using the ‘catch-up principle’, they extract small food particles from currents created by the compound cilia of the tentacles that form downstream-collecting ciliary bands (Riisgaard et al., 2000). Larger food particles are captured by a sticky substance secreted by the glandular cells in the tentacles. As entoprocts are oriented with the dorsal side attached to the stalk and ventral side away from the substratum, water currents pass from dorsal to ventral. The lateral cilia trap the food, cover it with mucus and move it to the frontal cilia. It is then transported to the ciliated vestibular food groves at the base of the tentacular ring where additional ciliary tracts carry the food to the mouth. The food is further moved into the gut by the cilia lining the buccal tube and muscular contractions of the esophagus, which lead to a spacious stomach from which a short intestine extends to the r ectum located within the anal cone. Food is then mixed with digestive enzymes inside the stomach by a tumbling action through the ciliary currents and is held by an intestinal-rectal sphincter muscle in the intestine where absorption takes place (Brusca and Brusca, 2003). Barentsiidae species are said to not share the ingested nutrients like ectoprocts and hydroids (Dipper, 2016). A comparative diagram between Barentsiidae and Loxosomatidae of the feeding apparatus inside the calyx is shown in Figure 6.


6
Figure 6

Excretory System

The gut functions as an excretory passage. Precipitations of uric acid and guanine are accumulated in the ventral stomach, released into the stomach lumen and discharged through the anus (Verma, 2001). A pair of flame bulb protonephridia is situated between the vestibule epithelium and the stomach. It connects to the nephridioduct lined with athrocytes that leads to pores on the vestibular surface. The athrocytes phagocytize wastes produced from the mesenchyme and deliver them to the excretory duct. Internal transport is carried out in the expansive gut. As the distance through the mesenchyme is small between the lumen and body wall, gas exchange occurs with diffusion across the body surface at the cuticle-free tentacles and vestibule (Brusca and Brusca, 2003). In Barentsiidae, the additional star-cell organ serves as a heart by pumping fluid from the calyx to the stalk.

Reproductive System

Zooids have one or two pairs of gonads beneath the vestibular surface (Brusca and Brusca, 2003). The gonads are sacciform bodies situated ventral to the liver region of the stomach and close to the ganglion and they have short gonoducts that lead to the pore opening to a brood chamber (Verma, 2001). In hermaphroditic species of Barentsiidae and Loxosomatidae, the pair of testes are located posterior to the pair of ovaries. From each gonad, a short duct protrude medially and meets its partner to connect to the ventral side of the calyx through a common gonopore. The sperm duct unites with the oviduct of that side before the formation of the common gonopore, which is located behind the nephridiopore. The gonoducts are covered with eosinophils unicellular glands or glandular epithelium. Ripe sperms with flagella are stored in the seminal vesicle in the common sperm duct while developing eggs stay in the brood chamber (Verma, 2001). The brood chamber is a depression formed from the calyx surface between the elevation of the nephridiopore and the anal cone.



Biogeographic Distribution

Entoprocts are generally widely distributed in coastal marine waters, ranging from tropical, temperate and polar regions and from the shallow intertidal seashore to the deep sea below 500m throughout the world (Iseto 2004). Barentsiidae are predominantly marine with the exception of the freshwater genus Urnatella occurring in the United States, India and central Europe (Visser and Veldhuijzen van Zanten 2003). The specific ranges in which Barentsiidae and Loxosomatidae have been recorded in scientific journals are shown in Figure 7 and 8, reflecting their specialists’ adaptations to a range of biotic and abiotic factors in the respective environments.



7
Figure 7
8
Figure 8

Evolution and Systematics

Despite numerous morphological and molecular studies, the phylogenetic relationships of entoprocts still remain unclear (Borisanova et al., 2019). They were first described as Ectoprocta (van Beneden, 1845) as they share share similar features in the larval morphologies and life cycles (Fuchs et al., 2010). However, they were later discovered to differ in the anus being located inside vs outside the tentacle crown, spiral vs radial cleavage pattern and acoelomate vs coelomate body cavities. Given these anatomical and developmental differences, entroprocts were hence proposed as a separate phylum (Hatschek, 1888). The recent discovery of the new animal phylum Cycliophora bridges the shared features between the two phyla, supporting the entoproct-ectoproct relationship. Based on both morphological and molecular data, it is generally accepted that Entoprocta are most closely related to Cycliophora. However, its sister relationship to Ectoprocta is still disputed with some studies proposing that they are more closely related to Annelida (Emschermann and Kamptozoaires, 1982) or Mollusca (Haszprunar and Wanninger, 2008; Merkel et al., 2015).


Regarding the internal relationships within Entroprocta, the monophyly of the phylum is generally supported (Fuchs et a., 2010). It splits into two lineages: Coloniales, representing all colonial taxa across three families and six genera, and Solitaria, representing solitary entoprocts in one family with five genera (Table 2), where Coloniales is basal to the phylum (Emschermann, 1972). Within Coloniales, Barentsiidae species are paraphyletic in most analyses in relation to Pedicellinidae species, rendering them a polytomy. Within Solitaria, Loxosomella genus of Loxosomatidae is a paraphyletic group with respect to other genera within the family (Figure 9a).


Order

Family

Genus

Solitaria

Loxosomatidae

Loxosoma

Loxosomella

Loxomitra

Loxocorone

Loxomespilon

Coloniales

Pedicellinidae

Pedicellina

Loxosomatoides

Myosoma

Barentsiidae

Barentisia

Urnatella

Loxokalypodidae

Loxokalypus

Table 2. Systematics of Entoprocta based on morphological characters (from Fuchs et al., 2010)

Based on the phylogenetic reconstruction of character evolution (Figure 9b), the ancestral entoproct life cycle is likely represented by the solitary Loxosomella species that settles with the frontal organ before metamorphosis (Nielsen, 1971). The solitary species with larval budding and all colonial species appear to be derived (Nielsen, 2013). It is therefore suggested that the ancestral entoproct is probably a solitary marine organism with an epizoic lifestyle where the adult stage consisted of a bilobed central nervous system, and the planktonic larvae a gut and a ciliated creeping foot with no larval eyes and budding (Fuchs et al., 2010). 



9
Figure 9

Conservation and Threats

Entoprocts are common in worldwide seas and no species are listed by the IUCN (from Global Biodiversity Information Facility). While Barentsiidae are mostly native in many regions, some Barentsiddae species have been reported having cosmopolitan distributions (Wasson et al., 2000), such as Barentsia discreta occurring in fouling communities at commercial harbours of Puerto de Santa Cruz de Tenerife and Cape Verde and Azores in the Macaronesian region (Riera et al., 2017). However, their distribution and abundance are poorly documented. Further research efforts can be targeted at recording their biogeographic distribution and monitoring their ecological responses to anthropogenic activities.


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