The organization and development of the nervous system are traditionally used for phylogenetic analysis and may be useful for clarification of evolution and phylogeny of some poor studied groups. One of these groups is brachiopods: most data on their nervous system organization were obtained in 19th century. In this research, antibody staining and confocal laser scanning microscopy were used to study the nervous system of early ontogenetic stages of the brachiopod Novocrania anomala. Although N. anomala adults are thought to lack a supraenteric ganglion, a large supraenteric ganglion exists in N. anomala juveniles with either a trocholophe or a schizolophe. During ontogenesis, the supraenteric ganglion in the juvenile changes its shape: the commissure between the two lobes of the ganglion extends. This commissure possibly gives rise to the main brachial nerve in adults. The supraenteric ganglion gives rise to the cross (transversal) nerves that extend to the accessory brachial nerve, which gives rise to the tentacular nerves. In juveniles with a trocholophe, the accessory brachial nerve gives rise to the frontal and intertentacular nerves of tentacles that form a single row. When the trocholophe transforms into the schizolophe, the second row of tentacles appears and the innervation of the tentacles changes. The intertentacular nerves disappear and the second accessory nerve forms and gives rise to the laterofrontal tentacular nerves of the inner and outer tentacles and to the abfrontal nerves of the inner tentacles. The so-called subenteric ganglion, which was described as a ganglion in N. anomala adults, is represented by a large circumvisceral nerve in N. anomala juveniles.The results suggest that ‘phoronid-like’ non-specialized tentacles may be regarded as the ancestral type of tentacles for brachiopods and probably for all lophophorates. The presence of intertentacular nerves is the ancestral feature of all lophophorates. The transformation of the juvenile supraenteric ganglion into the main brachial nerve of N. anomala adults suggests that research is needed on the development and organization of the supraenteric ganglion and the main brachial nerve in other brachiopods, whose adults have a prominent supraenteric ganglion.
Brachiopods are marine benthic animals with sessile life styles. They are filter feeders, i.e., they use a specialized tentacular structure called the lophophore to capture food particles. Today about 400 extant species species are described, however more than 30,000 extinct species are known to science1,2,3. An understanding of the biology of the many extinct brachiopods requires research on the development and organization of all organ systems of extant species from different groups.
Although the organization of the nervous system is traditionally regarded as important for comparative anatomy and phylogeny, the anatomy of the nervous system of extant brachiopods has not been adequately studied by transmission electron microscopy, antibody staining, and confocal laser scanning microscopy. Most of the detailed morphological information we have today is gained by histological methods from the 18th century4,5,6,7. In recent studies, the phylum Brachiopoda is subdivided into three subphyla, whose relationships are still vague: Cranoiiformea, Linguliformea, and Rhinchonelliformea8,9,10. Transmission electron microscopy, antibody staining, and confocal laser scanning microscopy have been used, however, to obtain data concerning the lophophore, the nervous system of species in the subphyla Linguliformea11 and Rhinchonelliformea12. The nervous system of Craniiformea is still not studied by modern immunohistological methods.
According to some researchers, the metamorphosis of craniiform larvae may reflect some steps of brachiopod evolution13,14,15. The development of the nervous system was described in advanced larvae and juveniles of the craniiform species, Novocrania anomala16. According to the latter study, 17-day-old juveniles lack a large nerve center, and their nervous system is represented by several main nerve cords. This result is supported by previous study, according to which adults of N. anomala lack a supraenteric ganglion and possess only a subenteric ganglion6. At the same time, Altenburger and Wanninger16 neither described any nerve tracts related to the tentacular innervation nor any tentacular neurites in juveniles. The latter findings seem odd, because they indicate that juveniles lack tentacles (or innervation of tentacles) and do not feed for a prolonged period.
In all brachiopods, the body is surrounded by a shell consisting of a ventral and a dorsal valve17,18. Many brachiopods have a pedicle, which is attached to the substratum and which facilitates the movement of the whole body in response to local water currents. N. anomala lacks a pedicle; the ventral valve tightly adheres to the substratum19. The dorsal valve is mitriform. The organization of the N. anomala shell and body causes the tentacles to be near the substratum, which presents a potential challenge for the filtration of particles from the water column. This potential challenge suggests that the organization of tentacles and the lophophore in N. anomala might be different in other brachiopods.
The study of the nervous system and innervation of the tentacular apparatus is useful for the comparative analysis of the organization of different types of lophophores in brachiopods in particular and in lophophorates in general20,21. It is also important for the reconstruction of the ancestral type of lophophore and tentacles in the lophophorates. The first goal of this report is a detailed description of the nervous system in general and the innervation of the lophophore in particular in juveniles of Novocrania anomala. In this report, I also consider how these new data provide insight into the evolution of the tentacles and the lophophore in brachiopods and lophophorates in general.
General morphology of the body and lophophore in juveniles
Juveniles of N. anomala examined in this study had a dorsal valve that ranged from 0.5 to 1.0 mm in diameter; an increase in diameter presumably indicates a shift to the next ontogenetic stage (Fig. 1A,B). Most of the body occupies the posterior portion of the dorsal valve, but the tentacles extend anteriorly and occupy the mantle cavity. At early ontogenetic stages, juveniles have a trocholophe (i.e., a simple type of lophophore), which bears one row of tentacles that surround the mouth from the posterior side (Fig. 1C). In these early juveniles, a short brachial fold covers the mouth from the anterior side. At late ontogenetic stages, juveniles develop a schizolophe, a type of lophophore with two rows of tentacles (inner and outer) and a large brachial fold (Fig. 1D).
Morphology of tentacles of a single row in the trocholophe of N. anomala, is similar. Each tentacle has a highly ciliated frontal surface that faces the mouth, heavily ciliated lateral zones, and a sparsely ciliated abfrontal surface that is opposite to the frontal surface (Fig. 2A). The two rows of tentacles in the schizolophe are formed by alternating inner and outer tentacles that differ in morphology. The inner tentacles are located near the brachial fold, and their morphology is similar to that of the tentacles in the trocholophe. The outer tentacles are located between the inner tentacles in a staggered order. The frontal surface of the outer tentacles forms a deeply ciliated groove (Fig. 2B).
Anatomy of the nervous system
In juveniles with a trocholophe or with a schizolophe, the most prominent part of the nervous system is a large supraenteric ganglion (Figs. 3A,B and 4A–E). This ganglion is bilobed and consists of many cells that give rise to numerous neurites. These form a large neuropil and the commissure-like nerve cord between the two lobes (Fig. 5A). In juveniles with a trocholophe, the commissure-like nerve cord is very short and contains numerous perikarya, whereas in juveniles with a schizolophe, the commissure-like nerve cord is longer and contains fewer perikarya (Fig. 3A,B). In both cases, the commissure contains perikarya and should be regarded as part of the ganglion.
The supraenteric ganglion gives rise to several nerve tracts: cross (transversal) nerves and circumenteric dorsal connectives.(Fig. 4A–E). In juveniles with a trocholophe or with a schizolophe, cross (transversal) nerves originate from the two lobes of the supraenteric ganglion and extend to the accessory brachial nerve (Fig. 6A,B). The most posterior cross nerves are the largest and form the circumoral connectives (Fig. 6A).
The circumenteric dorsal connectives extend via three short roots from the lobes of the supraenteric ganglion to the subenteric ganglion (Figs. 4E and 7A). The accessory brachial nerve looks like a thick net of numerous thin neurites at the base of the tentacles (Fig. 7B). In juveniles with a trocholophe, the accessory brachial nerve seems to be composed of two halves (left and right), which are connected mid-ventrally to the mouth (Fig. 6A). The accessory brachial nerve follows the shape of the lophophore and gives rise to the tentacle nerves.
A large aggregation of perikarya that does not resemble a ganglion is located below the mouth: it is the thick circumvisceral nerve (Fig. 4A,B). It extends around the middle part of the dorsal side of the body to the posterior end and consists of many neurites and perikarya (Fig. 5C). The presence of perikarya indicates that the circumvisceral nerve should be regarded as the subenteric ganglion. It gives rise to numerous bundles of dorsal–radial mantle neurites. These neurite bundles usually originate from two dorsolateral regions of the subenteric ganglion (Fig. 4A,D). Most of the mantle neurite bundles are radial: they extend from the subenteric neurites to the edge of the mantle, where the dorsal–marginal mantle nerve runs (Figs. 4A,B,D, 5D). There are thick and thin types of the mantle neurite bundles, both of which are associated with perikarya (Fig. 5D). Some of the mantle neurite bundles branch and give rise to very thin neurites, which form a dense net in the mantle. Most of the thin neurites are associated with caeca, which extend into the shell (Fig. 5E).
Juveniles with schizolophes have a lower brachial nerve (Fig. 4C,E). It extends between two circumenteric dorsal connectives and is located below the mouth.
Innervation of tentacles
During ontogenesis of juveniles the innervation of the tentacles changes and occurs in different ways. This difference is correlated with the reorganization of the tentacle apparatus. In juveniles with a trocholophe, the innervation of tentacles is completely supplied by an accessory brachial nerve (Fig. 7C). Two groups of neurite bundles, frontal and intertentacular, extend from the accessory brachial nerve (Fig. 7C, 8A). Frontal neurite bundles penetrate into each tentacle and extend along the frontal zone of the tentacle; i.e. these are the frontal tentacular nerves (Fig. 7C). The intertentacular nerves extend from the accessory brachial nerve to the base between adjacent tentacles, where they branch and form two neurite bundles that penetrate into adjacent tentacles and give rise to the laterofrontal tentacular nerves (Fig. 8A).
In juveniles with a schizolophe, the innervation described in the previous paragraph applies only to the oral tentacles (Fig. 9). Along the lateral sides of the lophophore, where the tentacles of the outer row appear, the innervation of tentacles is more complicated than described for earlier juvenile stages that have only one row of tentacles (Figs. 4F, 8B and 9). In juveniles with two rows of tentacles, frontal neurite bundles penetrate into the outer and inner tentacles. The frontal neurite bundles of the outer tentacles branch at their base. They give rise to short, oblique neurites, which are directed to the left and right and which extend to the base of the abfrontal side of adjacent inner tentacles (Fig. 5B). At the abfrontal base of the inner tentacles, oblique neurites with different orientations fuse and form a kind of additional accessory nerve (Figs. 8B, 9). The additional accessory nerve gives rise to the laterofrontal nerves of the inner and outer tentacles and to the abfrontal nerves of the inner tentacles (Fig. 4F). Thus, each outer tentacle is innervated by one frontal and two laterofrontal neurite bundles, whereas each inner tentacle is innervated by one frontal, two laterofrontal, and two abfrontal neurite bundles (Fig. 4G).
Morphology of the lophophore and tentacles in brachiopods
In extant and extinct brachiopods, there are at least nine different types of lophophores10. Two types, the taxolophe and the trocholophe, may be distinguished in the postembryonic development of all species studied to date22. At the same time, some brachiopods have a trocholophe throughout all ontogenetic stages23,24. The taxolophe and trocholophe types of lophophore only have one row of tentacles and only one small coelomic canal. The schizolophe type of lophophore has two rows of tentacles and a large and a small coelomic canal. The morphology of the schizolophe is similar to that of the horseshoe-shaped lophophore of phoronids and phylactolaemate bryozoans. In schizolophes, one row of tentacles is retained below the mouth. The nomenclature used for these tentacles is inconsistent: they are described as inner tentacles in N. anomala25 but as outer tentacles in “articulated brachiopods”26.
According to the data obtained in the present study, the oral tentacles (which are located below the mouth) may be described as ‘phoronid-like’ tentacles, which lack the specific characteristics that are typical for the inner and outer tentacles of brachiopods (Fig. 10). These specific characteristics are ridges in the inner tentacles and a groove in the outer tentacles22,27. ‘Phoronid-like’ tentacles may be regarded as tentacles of the primitive type, which might be ancestral for all lophophorates (Fig. 10). Although this type of tentacles may be considered to be ‘unspecialized’ in comparison with brachiopod and bryozoans tentacles, they are undoubtedly specialized in comparison with tentacles of some oweniids28. The specialization of phoronid-like tentacles is expressed in the co-localization of ciliated zones, nerve tracts, and muscles21.
Anatomy of the nervous system
Anatomy of the nervous system of juveniles of N. anomala is similar to that in adults6, but exhibits several main differences. First, adults of N. anomala lack a supraenteric ganglion6. At the same time, juveniles with trocholophes or schizolophes have a well-developed ganglion dorsally to the mouth. This ganglion is bilobed, and the two lobes are connected by a commissure-like nerve cord. Because this commissure extends with development, the two lobes of the supraenteric ganglion move away from each other. In late juvenile stages and in adults, this commissure probably becomes the main brachial nerve, whereas the two lobes of the ganglion are probably located at terminal end of each brachial arm. These possibilities should be tested by the examination of juvenile development and organization of the lophophore nervous system in adults of other brachiopods. The transformation of the supraenteric ganglion into the main brachial nerve indicates that research is needed on the development and morphology of the main brachial nerve in brachiopods that are known to have a prominent supreaenteric ganglion.
The second difference is the presence of additional accessory nerve in juveniles (this study) and its absence in adults6. This nerve is discovered in late juveniles, which have two rows of tentacles. Moreover, the additional accessory nerve appears as a result of the split of intertentacular nerves, which retain only between oral tentacles.
The second accessory brachial nerve was first described as a neurite bundle that extends between the bases of two rows of tentacles in Hemithiris psittacea12. In H. psittacea, the second accessory nerve surrounds the frontal sides of both the inner and outer rows of tentacles12. In juveniles of N. anomala, in contrast, the additional accessory nerve surrounds the abfrontal sides of only the inner tentacles. Because of its location, the second accessory nerve of H. psittacea cannot be regarded as the homologue of the additional accessory nerve of N. anomala. This inference, however, should be supported by data from N. anomala adults. Based on the available data, the presence of additional nerves in N. anomala juveniles with a schizolophe and in H. psittacea adults may be regarded as an increase in complexity of the innervation of tentacles. In late juveniles of N. anomala, this modification is expressed in the appearance of paired abfrontal nerves in the inner tentacles. At the same time, the outer tentacles of late juveniles of N. anomala lack abfrontal nerves. It would be useful to examine the innervation of tentacles in N. anomala adults to determine whether the outer tentacles have abfrontal nerves and, if they do, their roots.
Innervation of tentacles
Innervation of brachiopod tentacles is described for several species11,12,29,30. The current findings indicate that the innervation of N. anomala tentacles differs substantially in juveniles with a trocholophe and juveniles with the schizolophe (Fig. 8). This difference is related to the presence of one row of tentacles with trocholophes vs. two rows of tentacles for schizolophes. In the trocholophe, the innervation pattern is simple: there are only frontal and intertentacular nerves, which extend from the accessory brachial nerve. The same pattern may be distinguished in different groups of bryozoans31,32,33,34,35,36 and in Phoronis ovalis21, in which the circumoral nerve ring gives rise to the frontal and intertentacular nerves (Figs. 10, 11). This pattern leads to the presence of only three neurite bundles in each tentacle: one frontal and two laterofrontal. The pattern becomes more complicated when additional tentacular nerves appear. These nerves may originate from frontal and laterofrontal bundles as in bryozoans, or from an outer nerve ring as in phoronids.
In adult brachiopods studied to date by transmission electron microscopy, antibody staining, and confocal laser scanning microscopy, the accessory brachial nerve (in Lingula anatina) or the main brachial nerve (in Hemithiris psittacea) gives rise only to frontal neurite bundles, which then branch to form the nerves that extend into the outer and inner tentacles11,12. Thus, in adult brachiopods, the brachial nerves give rise to the frontal neurite bundles but not to the intertentacular neurite bundles that are present in those juveniles of N. anomala that have a single row of tentacles. The current results suggest that the “adult” pattern of tentacle innervation might result from the formation of the second row of tentacles, which originate exactly in the location of the intertentacular nerves. The appearance of a second row of tentacles leads to the disappearance of the integral intertentacular nerves, which split into several neurite bundles that form the additional accessory brachial nerve.
Evolution of the lophophore and tentacles in the lophophorates
The monophyly of the lophophorates recently gained support from transcriptomic, phylogenomic, and morphological studies11,20,21,34,35,37,38,39,40. Determining how the ancestral lophophore was organized will increase our understanding of the evolution of recent lophophorates and the evolution of many extinct “tentaculates” including the enigmatic hyoliths and other groups41,42,43. The lophophore is a specialized organ, with a structure that is adapted to collect food particles from the water column. As previously suggested44, the ancestral lophophore had a simple morphology and was probably ovoid or crescent-shaped, bore one row of tentacles, and contained a single coelomic cavity. According to the data concerning the organization of the lophophoral nervous system of N. anomala (this study) and of other lophophorates, the nervous system of the ancestral lophophore may have consisted of only a few nerve elements: the cerebral ganglion, the circumoral nerve ring, and tentacular nerves (Fig. 11). In extant lophophorates, the cerebral ganglion corresponds to a dorsal ganglion in phoronids, a supraenteric ganglion in brachiopods, and a cerebral ganglion in bryozoans. The circumoral nerve ring corresponds to an inner nerve ring in phoronids, an accessory brachial nerve in brachiopods, and a circumoral nerve ring in bryozoans. In each tentacle of the last common lophophorate ancestor, there were at least three groups of nerves: one frontal and two laterofrontal. Such an arrangement is correlated with the zones with the highest density of cilia, i.e., the frontal and laterofrontal zones. The presence of intertentacular nerves and the innervation of adjacent tentacles from the one intertentaculate nerve are important. This innervation allows the coordination of the ciliary activity of laterofrontal zones of adjacent tentacles, whose cilia function as a mesh to capture food particles22,45,46. The appearance of the second nerve center and the second nerve ring21, which extends at the base of tentacles, may be regarded as a way to innervate different zones of tentacles to improve their function.
Among lophophorates, phoronids have the least specialized tentacles. In brachiopods, the specialization is expressed in the formation of two types of tentacles with different morphologies: inner and outer tentacles22,27. In bryozoans, the specialization of tentacles is related to their miniaturization: in transversal sections of bryozoan tentacles, each zone is represented by a few cells or even a single cell47. The presence of ‘phoronid-like’ tentacles in brachiopod ontogeny, in all adult brachiopods (as oral tentacles), and in phoronids suggests that this type of tentacle is ancestral for all lophophorates.
Larval and juvenile nervous systems
Novocrania anomala has lecitotrophic larvae that undergo a metamorphosis resulting in the formation of the shell and the lophophore13. The larval nervous system changes into the juvenile nervous system with the disappearance of the apical organ and the formation of new nerve cords16. Two lateral neurite bundles are well-developed in the ventral side of the apical lobe in 5-day-old juveniles16. Based on their position (along the lateral sides of the body), these “ventral neurite bundles”16 may be compared with the circumenteric dorsal connectives, which were found in juveniles in the current study. The ventral or dorsal position is impossible to be determined without a whole-3D reconstruction of the nervous system and the body. According to Altenburger and Wanninger16, supraenteric and subenteric ganglioa originate as commissures between two “ventral neurite bundles”. Previous data and the current findings suggests that the anterior commissure gives rise to the supraenteric ganglion, the median commissure, the posterior commissure, and the “ventral neurite bundles”; the latter elongates in a posterior direction and forms the subenteric ganglion, which is the large circumvisceral nerve.
According to the current findings, the radial mantle nerves in N. anomala extend from two dorsolateral points of the subenteric ganglion to the dorsal mantle nerve, which runs along the mantle margin. In adults, the mantle nerves also originate from the two dorsolateral points of the subenteric ganglion6. According to Altenburger and Wanninger16, “serially arranged mantle neurites” extend from anterior portions of the “ventral neurite bundles” and also from the anterior commissure. It seems possible that Altenburger and Wanninger16 may have regarded some of the lophophoral nerves as mantle nerves.
Planktotrophic larvae of linguliform brachiopods have lophophores with tentacles which are innervated from ventral and dorsal lophophoral nerve rings55,56. The ventral nerve ring gives rise to the frontal tentacular nerves; the dorsal nerve ring gives rise to the abfrontal tentacular nerves54. Researchers have generally concluded that linguliform brachiopods do not undergo any catastrophic changes in morphology during metamorphosis57,58. Thus, the larval trocholophe is inherited by the juvenile and develops into the schizolophe. Although the transformation of the nervous system has not been studied, we can infer that the larval nervous system is retained by the juvenile. An exception concerns the median tentacle, which has serotonin-like immunoreactive perikarya that disappear during metamorphosis. Based on their contribution to the innervation of tentacles, the ventral and dorsal lophophoral nerve rings of the larva may develop into the accessory and lower brachial nerves of the juvenile. The main brachial nerve and the subenteric ganglion, which have been described in adult Lingula anatina7,11, probably develop de novo in juveniles. This suggestion raises the question how the supraenteric ganglion and the main brachial nerve develop and are organized in other adult brachiopods, which are documented to have a prominent supraenteric ganglion.
Materials and methods
Sampling of animals and light microscopy
In the North Sea (Storingavika Bay) in May 2019, a drag net was used to collect stones and adhering juveniles of N. anomala. The juveniles were carefully separated from the stones, except that the ventral valves remained attached to the stones. Live animals were photographed from the ventral side using a Leica M165C (Leica, Germany) stereomicroscope equipped with a Leica DFC420 digital camera.
In general, for this part of work I have used the protocol, which was previously efficient in the study of the lophophore nervous system in phoronids21 and brachiopods11,12. Whole juveniles were fixed in a 4% paraformaldehyde solution in filtered sea water and washed in phosphate buffer (pH 7.4) (Fisher Scientific, Pittsburgh, PA, USA) with Triton X-100 (1%) (Fisher Scientific) (PBT) for a total of 24 h. Nonspecific binding sites were blocked with 12% normal donkey serum (Jackson ImmunoResearch, Newmarket, Suffolk, UK) in PBT overnight at 4 °C. The specimens were then transferred into primary antibody anti-α-Tubulin-mouse (1:600) (ImmunoStar, Hudson, WI, USA) in PBT, and incubated for 24 h at 4 °C with rotation. Specimens were washed in PBT and were then exposed to the secondary antibody, 635-Alexa-Mouse (1:1000) (Invitrogen, Grand Island, NY, USA) in PBT, for 24 h at 4 °C. Before washing, DAPI and phalloidin (Alexa-488) were added to the vials with animals at concentration ratios of 1:300 and 1:250, respectively. After they were washed in phosphate buffer, the specimens were embedded in Murray Clear (50:50, benzyl benzoate:benzyl alcohol). Specimens were examined with a Nikon Eclipse Ti confocal microscope (Nikon, ThermoFisher Scientific, Waltham, MA). Z-projections were obtained using Image J version 1.43. Three-dimensional reconstructions and volume renderings were produced with Amira version 5.2.2 (Thermo Fisher Scientific, USA).
Scanning electron microscopy (SEM)
For SEM the standard protocol was used: specimens were fixed in 2.5% glutaraldehyde in 0.2 M cacodylate buffer overnight. The specimens were then washed in 0.2 M cacodylate buffer and postfixed in 1% osmium tetroxide in the same buffer for 3 h at room temperature. The specimens were dehydrated in ethanol and acetone, critical point dried, and then sputter coated with platinum-palladium. Specimens were examined with a Jeol JSM scanning electron microscope (JEOL Ltd., Tokyo, Japan).
The terminology, which is used in this report, is in line with the traditional terminology that was suggested in first papers devoted to the brachiopod nervous system4,5,6,7,58. This traditional terminology is often inconsistent with the recent knowledge on organization of the nervous system59. Thus, so-called brachiopod ganglia are not true ganglia; they are formed by neurioepithelia60. In order to escape the misunderstanding in description of the brachiopod nervous system, I have used the traditional terminology.
The field sampling did not involve endangered or protected species. The use of brachiopods in the laboratory does not raise any ethical issues.
The data sets analyzed during this study are available from the author upon request
Williams, A., Carlson, S. J., Branton, C. H. C., Holmer, L. E. & Popov, L. E. A supra-ordinal classification of the Brachiopoda. Philos. Trans. R. Soc B 35, 1171–93 (1996).
Emig, C. C., Bitner, M. A. & Ávarez, F.: Phylum Brachiopoda. In: Zhang, Z.-Q. (Ed.) Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness (Addenda 2013). Zootaxa. 3703(1), 75–78 (2013).
Carlson, S. The evolution of brachiopods. Annu. Rev. Earth Planet. Sci. 44, 409–38 (2016).
Hancock, A. On the organization of the Brachiopoda. Philos. Trans. R. Soc 148, 791–869 (1859).
Van Bemmelen, J. F. V. Untersuchungen uber den anatomichen und histologichen Bau der Brachiopoda Testicardina. Jena Z. Naturwiss(Leipzig) 16, 88–161 (1883).
Blochmann, F. D A von Crania anomala (Müller). In: Blochmann F (ed) Untersuchungen über den Bau der Brachiopoden I. Gustav Fischer, Germany, Jena, 1–65 (1892).
Blochmann, F. D A von Discinisca lamellose (Broderip) und Lingula anatina (Bruguiére). In: Blochmann F. (ed) Untersuchungen uber den Bau der Brachiopoden II. Gustav Fischer, Germany, Jena, 1–124 (1900).
Cohen, B. L. Rerooting the rDNA tree reveals phoronids to be ‘brachiopods without shells’; dangers of wide taxon samples in metazoan phylogenetics (Phoronida; Brachiopoda). Zool. J. Linn. Soc. 167, 82–92 (2013).
Harper, D. A., Popov, L. E. & Holmer, L. E. Brachiopods: origin and early history. Paléo 60, 1–24 (2017).
Temereva, E. N. & Kuzmina, T. V. Spermatogenesis in the deep-sea brachiopod Pelagodiscus atlanticus and the phylogenetic significance of spermatozoon structure. J. Morphol. 279(11), 1579–1589 (2018).
Temereva, E. N. & Tsitrin, E. B. Modern data on the Innervation of the Lophophore in Lingula anatina (Brachiopoda) support the Monophyly of the Lophophorates. PLoS One. 10(4), e0123040 (2015).
Temereva, E. N. & Kuzmina, T. V. The first data on the innervation of the lophophore in the rhynchonelliform brachiopod Hemithiris psittacea: what is the ground pattern of the lophophore in lophophorates? BMC Evol. Biol. 17, 172 (2017).
Nielsen, C. The development of the brachiopod Crania (Neocrania) anomala (O.F. Müller) and its phylogenetic significance. Acta Zool 72(1), 7–28 (1991).
Temereva, E. N. & Malakhov, V. V. The evidence of metamery in adult brachiopods and phoronids. Invert. Zool 8(2), 91–112 (2011).
Kuzmina, T. V., Malakhov, V. V. & Temereva, E. N. Larval development of the brachiopod Coptothyris grayi (Davidson, 1852) (Terebratulida: Rhynchonelliformea) and the evolution of brachiopod life cycles. Invert. Zool 16(1), 27–40 (2019).
Altenburger, A. & Wanninger, A. Neuromuscular development in Novocrania anomala: evidence for the presence of serotonin and a spiralian-like apical organ in lecithotrophic brachiopod larvae. Evol. Dev 12, 16–24 (2010).
James, M. A. et al. Biology of living brachiopods. Adv Mar Biol 28, 175–387 (1992).
Williams, A., James, M. A., Emig, C. C., Mackay, S. & Rhodes, M. C. Brachiopod anatomy. (ed. Kaesler R.L). 7–189 (The Geological Society of America Inc. and the University of Kansas Boulder Colorado and Lawrence, 1997).
Robinson, J. The muscles, body wall and valve-opening mechanism of extant craniid (inarticulated) brachiopods. J. Nat. Hist 48(2), 1231–1252 (2014).
Temereva, E. N. Morphology evidences the lophophorates monophyly: brief review of studies on the lophophore innervation. Invert. Zool 14(1), 85–91 (2017).
Temereva, E. N. Innervation of the lophophore suggests that the phoronid Phoronis ovalis is a link between phoronids and bryozoans. Sci. Rep 7, 1440 (2017).
Kuzmina, T. V. & Malakhov, V. V. The organization of the lophophore in brachiopods. J. Paleontol. 5, 1–18 (2007).
Swedmark, B. Gwynia capsula (Jeffreys), an articulate brachiopod with brood protection. Nature. 213, 1151–1152 (1967).
Emig, C. C. Functional disposition of the lophophore in living Brachiopoda. Lethaia. 25, 291–302 (1992).
Atkins, D. & Rudwick, M. J. S. The lophophore and ciliary feeding mechanisms in the brachiopod Crania anomala (Müller). J. Mar. Biol. Assoc 42, 469–480 (1962).
Williams, A. & Carlson, S. J. Affinities of brachiopods and trends in their evolution. (ed. Selden, P.A.) 2823–2877 (Supplement. Geological Society of America & University of Kansas Press, Boulder; Lawrence, 2007).
James M. Brachiopoda: internal anatomy, embryology, and development. (ed. Harrison, F. W. & Woollacott, R. M.) 297–407 (NY: Willey-Liss, 1997).
Gardiner, S. L. Fine structure of the ciliated epidermis on the tentacles of Owenia fusiformis (Polychaeta, Oweniidae). Zoomorphologie 91, 37–48 (1978).
Reed, C. G. & Cloney, R. A. Brachiopod tentacles: ultrastructure and functional significance of the connective tissue and myoepithelial cells in Terebratalia. Cell Tissue Res 185, 17–42 (1977).
Storch, V. & Welsch, U. Elektronenmikroskopische und enzymhistochemische Untersuchungen fiber Lophophor und Tentakeln von Lingula unguis (L.) (Brachiopoda). Zool. Jb. Anat 96, 225–237 (1976).
Gerwerzhagen, A. Untersuchungen an Bryozoen. Sitz Heidelb Akad Wiss, Math-nat Kl B 9, 1–16 (1913).
Weber, A. V., Wanninger, A. & Schwaha, T. F. The nervous system of Paludicella articulata - first evidence of a neuroepithelium in a ctenostome bryozoan. Front. Zool. 11(1), 89 (2014).
Schwaha, T. F. & Wanninger, A. The serotonin-lir nervous system of the Bryozoa (Lophotrochozoa): a general pattern in the Gymnolaemata and implications for lophophore evolution of the phylum. BMC Evol. Biol. 15, 223 (2015).
Temereva, E. N. & Kosevich, I. A. The nervous system of the lophophore in the ctenostome Amathia gracilis provides insight into the morphology of ancestral bryozoans and the monophyly of the lophophorates. BMC Evol. Biol. 16, 181 (2016).
Temereva, E. N. & Kosevich, I. A. The nervous system in the cyclostome bryozoan Crisia eburnea as revealed by transmission electron and confocal laser scanning microscopy. Front. Zool. 15, 48 (2018).
Worsaae, K., Frykman, T. & Nielsen, C. The neuromuscular system of cyclostome bryozoan Crisia eburnea. Acta Zool. 100(3), 268–281 (2018).
Laumer, C. E. et al. Spiralian phylogeny informs the evolution of microscopic lineages. Curr Biol. 25(15), 2000–6 (2015).
Laumer, C. E. et al. Revisiting metazoan phylogeny with genomic sampling of all phyla. Proc Biol Sci 286(1906), 20190831 (2019).
Marlétaz, F., Peijnenburg, K., Goto, T., Satoh, N. & Rokhsar, D. S. A New Spiralian Phylogeny Places the Enigmatic Arrow Worms among Gnathiferans. Curr. Biol. 29(2), 312–8 e3 (2019).
Zverkov, O. A. et al. Dicyemida and Orthonectida: Two Stories of Body Plan Simplification. Front. Genet 10, 443 (2019).
Zhang, Z. et al. An early Cambrian agglutinated tubular lophophorate with brachiopod characters. Sci. Rep 4, 4682, https://doi.org/10.1038/srep04682 (2015).
Moysiuk, J., Smith, M. & Caron, J. Hyoliths are Palaeozoic lophophorates. Nature. 541, 394–397, https://doi.org/10.1038/nature20804 (2017).
Liu, F., Skovsted, C., Topper, T., Zhang, Z. & Shu, D. Are hyoliths Palaeozoic lophophorates? Nat. Sci. Revi 7, 453–469 (2020).
Kuzmina, T. V. & Temereva, E. N. Organization of the lophophore in the deep-sea brachiopod Pelagodiscus atlanticus and evolution of the lophophore in the Brachiozoa. Org. Divers. Evol. 19, 31–39 (2019).
Nielsen, C. & Riisgard, H. U. Tentacle structure and filter-feeding in Crisia eburnea and other cyclostomatous bryozoans, with a review of upstreamcollecting mechanisms. Mar. Ecol. Progr. Ser. 168, 163–186 (1998).
Temereva, E. N. & Malakhov, V. V. Filter feeding mechanism in the phoronid Phoronopsis harmeri (Phoronida, Lophophorata). Russ. J. Mar. Biol. 36(2), 109–116 (2010).
Tamberg, Y. & Shunatova, N. Tentacle structure in freshwater bryozoans. J. Morphol. 278, 718–733 (2017).
Pardos, F., Roldán, C., Benito, J. & Emig, C. C. Fine structure of the tentacles of Phoronis australis (Phoronida, Lophophorata). Acta Zool 72(2), 81–90 (1991).
Pardos, F., Roldán, C., Benito, J., Aguirre, A. & Fernández, I. Ulstrastructure of the lophophoral tentacles in the genus Phoronis (Phoronida, Lophophorata). Can. J. Zool. 71, 1861–1868 (1993).
Temereva, E. N. & Malakhov, V. V. On the organization of the lophophore in phoronids (Lophophorata: Phoronida). Russ. J. Mar. Biol. 35(6), 425–435 (2009).
Temereva, E. N. Myoanatomy of the phoronid Phoronis ovalis: functional and phylogenetic implications. Zoology. 133, 27–39 (2019).
Temereva, E. N. Myoanatomy of the lophophore in adult phoronids and the evolution of the phoronid lophophore. Biol. Bull. 237(6), 270–282 (2019).
Temereva, E. N. Novel data on the innervation of the lophophore in adult phoronids (Lophophorata, Phoronida). Zoology. In press (2020).
Shunatova, N. & Borisenko, I. Proliferating activity in a bryozoan lophophore: a case study of gymnolaemates. PeerJ. 8, e9179, https://doi.org/10.7717/peerj.9179 (2020).
Santagata, S. Evaluating neurophylogenetic patterns in the larval nervous systems of brachiopods and their evolutionary significance to other bilaterian phyla. J. Morphol. 272, 1153–1169 (2011).
Hay-Schmidt, A. Ultrastructure and immunocytochemistry of the nervous system of the larvae of Lingula anatina and Glottidia sp. (Brachiopoda). Zoomorphol 112, 189–205 (1992).
Chuang, S. H. Brachiopoda. In K. G. Adiyodi & R. G. Adiyodi, eds., Reproductive Biology of Invertebrates. Fertilisation, Development and Parental Care, Vol. VI. John Wiley and Sons Ltd. p. 211–254 (1990).
Williams, A., James, M. A., Emig, C. C., Mackay, S. & Rhodes, M. C. Brachiopodanatomy. In: Kaesler, R.L. (Ed.), Treatise on Invertebrate Paleontology, Part H,Brachiopoda V. 1 Introduction. The Geological Society of America Inc. and theUniversity of Kansas Boulder Colorado and Lawrence, Kansas, pp. 7–189 (1997).
Richter, S. et al. Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary. Front Zool 7(1), 29 (2010).
Temereva, E. N. & Kuzmina, T. V. First description of ultrastructure of brachiopod ganglia and its phylogenetic significance. J. Zool. Syst. Evol. Res. In press. (2020).
This study is done with support from Russian Science Foundation (#18-14-00082). The author is very grateful to Nataliya Budaeva (Bergen, Norway), who invited me to the Espegrend and organized the expedition for gathering animals. I also thank my colleague and friend Tatiana Kuzmina (Moscow, Russia), who is a specialist in brachiopods, for valuable discussions. The research was performed at the User Facilities Center of M.V. Lomonosov Moscow State University with financial support from the Ministry of Education and Science of the Russian Federation. This work was supported by Moscow State University Grant for Leading Scientific Schools “Depository of the Living Systems” in the frame of the MSU Development Program.
The author declares no competing interests.
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Temereva, E.N. First data on the organization of the nervous system in juveniles of Novocrania anomala (Brachiopoda, Craniiformea). Sci Rep 10, 9295 (2020). https://doi.org/10.1038/s41598-020-66014-9