Balanoglossus misakiensis (Kuwano, 1902)
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publication ID |
https://doi.org/ 10.1007/s13127-015-0201-2 |
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DOI |
https://doi.org/10.5281/zenodo.13333777 |
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persistent identifier |
https://treatment.plazi.org/id/AB59ED17-564E-FFBA-FCAE-FE75FAE1FBF3 |
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treatment provided by |
Felipe |
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scientific name |
Balanoglossus misakiensis |
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Balanoglossus misakiensis View in CoL : Spengel stage
After about 13 days postfertilization (pf), the tornaria larvae start transforming into the Spengel stage accompanied by a series of morphological changes. The larvae are approximately 950 μm in length and are subdivided by a deep circular constriction into a slightly conical preoral region forming the future proboscis and a voluminous spherical posterior region bearing the distinct opisthotroch ( Fig. 2a, b View Fig ). The oral field is almost completely obliterated as the ciliary bands of the neotroch are fused together. The position of the ciliary bands is still indicated by grooves ( Fig. 2a View Fig ). A pair of dorsolateral slit-like depressions on the anterior part of the postoral body indicates the position of the prospective first gill pores ( Fig. 2a View Fig , arrowhead).
The entire larva is covered by short cilia. An apical tuft composed of longer cilia is present at the apical tip ( Fig. 2b View Fig ). Within the apical epidermis, numerous serotonin-LIR neurons are grouped together to form an anterior and a posterior cluster of cells which are interconnected by a median neuropil ( Fig. 2f View Fig ). The serotonin-LIR somata are slender, sometimes flask-shaped, cells with a nucleus that is positioned centrally or basally within the cytoplasm. Each soma is connected to the apical cell surface by a narrow elongation, the distal neurite ( Fig. 2f View Fig ). The serotonin-LIR cells are bipolar neurons that send a neurite into the median neuropil of the apical organ. Aside from the cells of the apical organ, numerous serotonin-LIR somata are scattered throughout the proboscis’ epidermis. Each bipolar neuron exhibits a distal neurite connecting to the apical surface and a proximal neurite. The proximal neurites of those bipolar neurons form a basiepidermal plexus-like arrangement throughout the proboscis epidermis. Within the voluminous postoral region, serotonin-LIR somata are only occasionally present. A conspicuous number of neurites are present at the level of the opisthotroch and form a distinct neurite bundle, namely, the opisthotroch neurite ring ( Fig. 2b, e View Fig ). Aside from that neurite bundle, the postoral body shows only individual neurites arranged in a loose, sometimes discontinuous pattern ( Fig. 2e View Fig ).
B. misakiensis : Agassiz stage
The larvae of the Agassiz stage (14 days pf) are of elongated shape measuring approximately 1 mm in length and 650 μm in width. The anterior proboscis is of conical acorn shape ( Fig. 2c, d View Fig ). It is separated from the posterior body by a deep
of the Spengel stage in lateral view. Note the anterior and posterior cluster of bipolar neurons connected by a central neuropil. g Detail showing the elaborated 5-HT+ nervous plexus in the prospective trunk region of an Agassiz stage larva. h Detail view of 5-HT+ apical bipolar neurons. A slender distal neurite connects the soma to the apical cell surface. i Detail of the neuite bundles passing the neck region, connecting the proboscis to the collar region. k Close-up of the dorsal collar region showing the 5- HT+ bipolar neurons.5-HT, serotonin; ac-α- tub, acetylated α- tubulin; ao, apical organ; at, apical tuft; ci, cilia; co, collar; ne, neurite; nn, nervous plexus; np, neuropil; onr, opisthotroch nerve ring; ot, opisthotroch; pf, perianal field; pr, proboscis; sn, serotonin-LIR neuron; tr, trunk
circular constriction ( Fig. 2c, d View Fig ). The grooves of the fused ciliary bands are no longer visible externally (compare Fig. 2a and d View Fig ). A second circular constriction indicates the posterior margin of the collar region ( Fig. 2d View Fig ). The collar region is about 150 μm long. The remaining posterior part of the body constitutes the future trunk region. It measures approximately 400 μm in total length and bears the opisthotroch at the midlevel of the trunk region ( Fig. 2c, d View Fig ).
Serotonin-LIR is present at the anterior tip of the proboscis region ( Fig. 2c View Fig ) and reveals numerous bipolar neurons with thin and long extensions to the cell surface where each neuron bears a single cilium ( Fig. 2h View Fig ). The overall morphology of the serotonin-LIR bipolar neurons of the apical organ is comparable to that of the Spengel stage. Further individual serotoninLIR neurons are interspersed throughout the proboscis with a higher density present near the base of the proboscis ( Fig. 2c View Fig , sn). All serotonin-LIR somata project into a basiepidermal plexus that is present throughout the proboscis. The plexus of the proboscis region is connected to that of the collar region by two laterally condensed neurite bundles that pass through a neck-like transition into the collar region ( Fig. 2c, i View Fig ). A pair of bilateral muscle bundles that run anteriorly into the base of the proboscis accompanies the neurite bundles ( Fig. 2i View Fig ). Several serotonin-LIR bipolar neurons are present within the anterior
neurites in the juvenile. Inset Color-coded image of the micrograph shown in d. Color code for insets: ectoderm, light blue; neurites, yellow; basal lamina (ecm), dark blue; mesoderm, red. bl, blastocoel; ecm, extra cellular matrix; epc, epidermal cell; gp, gill pore; i, intestine; ms, mesocoel; mt, metacoel; mtc, metacoelic cell; myo, myofilaments; ne, neurite; nu, nucleus; pc, protocoel; yo, yolk
collar region ( Fig. 2i, k View Fig ), whereas only scattered neurons are present within the prospective trunk region. The number of neurites within the collar and trunk region has considerably increased compared to the Spengel stage, and the neurites show a distinct plexus-like pattern, particularly in the prospective trunk region ( Fig. 2g View Fig ). The opisthotroch nerve ring is still well developed and encircles the larva’ s body in the middle of the prospective trunk region ( Fig. 2c View Fig ). Ultrastructural analyses of the metamorphosing Agassiz stage of B. misakiensis revealed the presence of numerous neurites that form a 4– 6-μm-thick basiepidermal layer within the prospective trunk region ( Fig. 3a, c View Fig , inset).
B. misakiensis : early settled juvenile
Early settled Balanoglossus (12-h postsettlement (ps)) have an elongated body of vermiform shape measuring approximately 1 mm in length ( Fig. 4a, b View Fig ). The proboscis is pointed at the anterior tip and about 450 μm long. The collar region measures 200 μm in length and is subdivided by a circular constriction into a broader anterior and narrower posterior part. The trunk region has significantly increased in length, now being 430 μm long. One pair of dorsolateral gill pores is developed at the anterior margin just behind the collar region. The opisthotroch is still present and encircles the trunk region ( Fig. 4b View Fig ).
Numerous serotonin-LIR somata are distributed throughout the epidermis of the proboscis region, and the apical organ is still visible at the anterior tip; yet, the number of serotoninLIR cells is reduced ( Fig. 4a View Fig ) compared to the Agassiz stage. The serotonin-LIR nervous system of the proboscis region differs from the Agassiz stage in having a neurite-rich plexus at the dorsomedian base of the proboscis ( Fig. 4a, e View Fig ). This socalled proboscis stem comprises one of the most condensed areas of the adult enteropneust nervous system. Posterior of the proboscis plexus, two serotonin-LIR neurite bundles project into the collar region and pass through the collar on a subepidermal level ( Fig. 4e View Fig ). Both serotonin-LIR bundles are part of the neurulated collar cord that forms at this stage. Although DAPI staining reveals numerous nuclei accompanying the collar cord, no soma stains positively for serotonin within the collar cord. At the posterior end of the collar, the two neurite bundles become basiepidermal again and project laterally ( Fig. 4e View Fig ) into the prebranchial nerve ring (see below). Within the epidermis of the collar region, numerous serotoninLIR somata are intercalated between the epidermis cells. Each serotonin-LIR bipolar neuron sends a proximal neurite into the basiepidermal plexus. The majority of serotonin-LIR neurites within the collar region runs in longitudinal direction ( Fig. 4d View Fig ) and project into one of the two circular serotoninLIR neurite bundles within the posterior half of the collar region ( Fig. 4d View Fig , mcb and 4f, pnr). The more anterior circular neurite bundle runs basiepidermally at the level of the internal margin of the collar coelom (mesocoel) ( Fig. 4d View Fig , mcb), whereas the more posterior ring, the prebranchial nerve ring, is present at the very posterior margin of the collar region. The prebranchial nerve ring forms a distinct network of serotonin-LIR neurites around the paired mesocoelic pores ( Fig. 4f, g View Fig ). These mesocoelic pores connect the coeloms of the collar region, the mesocoels, to the opening of the first gill pore, and eventually to the exterior. At this stage of development, a basiepidermal plexus is detectable by serotonin-LIR throughout the entire trunk region ( Fig. 4c View Fig ), however, with only few serotonin-LIR somata. The opisthotroch neurite ring is less condensed and comprises only a loose arrangement of circular neurites ( Fig. 4a, c View Fig ).
B. misakiensis : 1-gill-slit juvenile
After approximately 1-day postsettlement, the majority of juveniles have lost the opisthotroch ( Fig. 4h View Fig ). The proboscis shape has slightly changed into a blunt, rounded acorn, measuring between 250 and 350 μm in length. The collar region resembles that described for the previous stage and the trunk region is shorter than the previous stage ( Fig. 4h, l View Fig ).
Within the proboscis and collar region, serotonin-LIR reveals only few changes of the overall architecture of the nervous system. Along the anterior tip of the proboscis, the number of the serotonin-LIR somata within the former apical organ is further reduced ( Fig. 4i, l View Fig ). Along the anterior-posterior axis of the proboscis region, distinct neurite bundles indicate the position of the former larval ciliary bands ( Fig. 4i View Fig , cgn, l). Within the anterior two thirds of the collar region, two rings of numerous serotonin-LIR neurons are present ( Fig. 4k View Fig ). These cells are long, slender bipolar neurons with the somata placed basally, centrally, or even apically within the epidermis ( Fig. 4k View Fig ). At the posterior collar margin, a pair of prebranchial nerves runs circumferentially, passes the mesocoelic pores, and eventually connects to the ventral part of the nervous plexus ( Fig. 4l View Fig , pnr). While the arrangement and orientation of the basiepidermal neurites within the proboscis and collar region have not changed much, the situation in the trunk region is considerably different. A plexus-like arrangement of serotonin-LIR neurites is only detectable in the anterior half of the trunk ( Fig. 4l, m View Fig ), whereas in the posterior part of the trunk, individual circumferential neurites are present. These circular neurites project into a longitudinal neurite bundle that is present along the ventral midline ( Fig. 4l View Fig , vnb).
B. misakiensis : 2-gill-slit juvenile
After about 3-day postsettlement, most of the juveniles exhibit two pairs of gill slits ( Fig. 5a, b View Fig ). Both gill slits are U-shaped and heavily ciliated on the inside ( Fig. 5b View Fig ). No synapticles are developed. The juveniles measure up to 1.5 mm in total length ( Fig. 5a–c View Fig ). The proboscis shows the typical acorn shape, while the mesosome has developed into a 200-μm-long threelobed collar region ( Fig. 5a View Fig ). Scanning electron micrographs and acetylated-α- tubulin-LIR reveal that the proboscis and collar region are evenly covered with cilia, whereas on the trunk region, only scattered tufts of cilia are present ( Fig. 5a, c View Fig ).
Throughout the epidermis of the proboscis, numerous serotonin-LIR bipolar neurons are intercalated between the other epidermal cells ( Fig. 5c, i View Fig ). Each soma projects a single proximal neurite into the basiepidermal plexus of the proboscis region ( Fig. 5i View Fig ). The most condensed area of serotonin-LIR neurites is present dorsally at the base of the proboscis, comprising a part of the proboscis plexus ( Fig. 5c, d View Fig ). This dense network of neurites measures approximately 200 μm in width and 100 μm in length. From here, three distinct serotonin-LIR neurite bundles leave the proboscis plexus posteriorly to pass through the subepidermal collar cord within the collar region ( Fig. 5d View Fig ). These serotonin-LIR neurite bundles are part of the ventral layer of neurites of the collar cord ( Fig. 5h View Fig ). The dorsal area of the collar cord is composed of numerous cells, presumably neurons, which do not show serotonin-LIR in any of the somata ( Fig. 5h View Fig ). At the posterior pole of the collar region, the three serotonin-LIR neurite bundles become basiepidermal again and connect to the nervous system within the trunk region. The median neurite bundle, composed of 7–10 serotonin-LIR neurites, continues directly into the dorsal midline and is part of the dorsal nerve cord ( Fig. 5f View Fig ). SerotoninLIR is detectable until the posterior pole of the animals, with a discontinuity of about 150 μm in the middle of the trunk region ( Fig. 5f, g View Fig , double arrowheads). Several serotoninLIR bipolar neurons are located dorsolaterally close to the dorsal midline and project a short neurite into the dorsal neurite bundle ( Fig. 5f View Fig ). The lateral pair of neurite bundles that leaves the collar cord posteriorly runs circumferentially to the ventral side ( Fig. 5d View Fig ). At the level of the dorsolateral gill slits, the bilateral neurite bundles form a distinctive network around the mesocoelic pores as also described for younger stages ( Fig. 5d View Fig ). The bilateral neurite bundles are part of the prebranchial nerve ring and project into the ventral nerve cord. Numerous serotonin-LIR neurites extend along the entire midline of the trunk region thereby running within the ventral nerve cord that is about 40 μm wide ( Fig. 5c, e View Fig ). Several serotonin-LIR somata are interspersed throughout the trunk epidermis. The majority of these bipolar neurons project a proximal neurite running circumferential into the ventral nerve cord ( Fig. 5e View Fig ). The serotonin-LIR somata of the very posterior end send a proximal neurite running radially into the ventral neurite bundle ( Fig. 5e View Fig ). It should be noted that a serotonin-LIR basiepidermal plexus is only present in the epidermis of the proboscis and collar, but completely absent within the trunk region, where instead a condensed dorsal and ventral neurite bundle is present.
The analysis of serial sections for electron microscopy of the trunk epidermis in juvenile B. misakiensis shows comparatively few basiepidermal neurites in the epidermis ( Fig. 3b, d View Fig and inset). Neurite bundles composed of 4–8 neurites are scattered throughout the lateral areas of the trunk epidermis ( Fig. 3d View Fig ). The most condensed neurite bundles run along the ventral and dorsal midline of the trunk region and comprise the nerve cords.
No known copyright restrictions apply. See Agosti, D., Egloff, W., 2009. Taxonomic information exchange and copyright: the Plazi approach. BMC Research Notes 2009, 2:53 for further explanation.
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