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Unity in diversity: a survey of muscular systems of ctenostome Gymnolaemata (Lophotrochozoa, Bryozoa)
© The Author(s). 2018
Received: 23 January 2018
Accepted: 17 May 2018
Published: 7 June 2018
Myoanatomical studies of adult bryozoans employing fluorescent staining and confocal laser scanning microscopy (CLSM) have been chiefly conducted on freshwater bryozoans. The diversity of muscular systems in the marine bryozoans is currently not well known with only two species being studied in more detail. The aim of this study is to unravel the diversity of muscle systems of 15 ctenostome bryozoans by phalloidin-coupled fluorescence stainings combined with CLSM.
In general, the myoanatomy of the selected ctenostomes shows significant similarities and consists of 1) muscles associated with the body wall, 2) apertural muscles, 3) lophophoral muscles, 4) tentacle sheath muscles, 5) digestive tract muscles and 6) the prominent retractor muscles. Differences are present in the arrangement of the apertural muscles from generally three muscles sets of four bundles, which in some species can be partially reduced or modified into a bilateral arrangement. The cardiac region of the digestive tract shows a distinct sphincter in four of the six studied clades. In some cases the cardiac region forms a prominent proventriculus or gizzard. Tentacle sheath muscles in victorelloideans and walkerioideans are arranged diagonally and differ from the simple longitudinal muscle arrangements common to all other taxa. Lophophoral base muscles consist of four sets that vary in the size of the sets and in the shape of the inner lophophoral ring, which either forms a complete ring or separate, intertentacular muscle bundles. The stolon-forming walkeridiodean ctenostomes show prominent transverse muscles in their stolons. These are always present in the shorter side stolons, but their occurrence in the main stolon seems to depend on the colony form, being present in creeping but absent in erect colony forms.
This study represents the first broad survey of muscular systems in adult ctenostome bryozoans and shows a certain degree of conservation in a series of diverse colony forms belonging to five major clades. However, several myoanatomical features such as the cardiac sphincter, basal (possibly transitory) cystid muscles, tentacle sheath muscles or apertural muscle arrangement vary across taxa and thus show a high potential for the assessment of character evolution within ctenostomes. As such, this study represents an essential contribution towards determining and reconstructing the character states of the bryozoan ground pattern once a reliable phylogenetic tree of the whole phylum becomes available.
Bryozoa is a phylum of colonial invertebrate animals with 6000 recent and 15.000 fossil species described . Most bryozoans are colonial and consist of repetitive modules of individuals, so-called zooids, which constitute the colony. Each zooid consists of a protective body wall called the cystid and a polypide, consisting of the soft body parts. Within the polypide are the ciliated tentacle crown (the lophophore), u-shaped digestive tract as well as associated muscles, associated neuronal elements and gonads where present. Typical for all bryozoans is the retraction process; a defensive response where the polypide is retracted into the cystid for protection [2, 3]. Eversion of the tentacle crown is achieved by an increase in coelomic pressure [3, 4].
Three different taxa of bryozoans are currently recognized: Phylactolaemata, Stenolaemata and Gymnolaemata . Among other features, each of these groups is characterized by its cystid structure and thus a respective protrusion mechanism . The phylactolaemate cystid is unmineralized and flexible which allows contraction of the regular body wall musculature to increase coelomic pressure upon contraction thereby everting the polypide [5, 6]. Stenolaemates have calcified and rigid cystids which are incompressible. Consequently, the coelomic epithelium is detached from the body to form a so-called membranous sac around the polypide which allows contraction by annular ring muscles in its epithelial lining for polypide eversion (see [3, 4, 7]).Gymnolaemata is the most species-rich and diverse taxon of bryozoans, comprising over 5000 species. The gymnolaemate cystid can be either uncalcified and flexible such as those of the paraphyletic “Ctenostomata”  or partially or fully calcified such as those of the Cheilostomata . Both these groups possess parietal muscles derived from putative ancestral body-wall musculature, which they use for polypide eversion [3, 9]. Most of these protrusion mechanisms were already described in the 19th century by light-microscopy combined with histological sectioning (e. g. [10–12]). Information on the other muscular systems (e.g., the digestive tract or lophophore) are scarce and mainly consists of a few whole-mount staining analyses [13–15] or ultrastructural studies that focused on specific organ systems (e.g. [16–20]).
The application of confocal laser scanning microscopy in the past decade has yielded new insights into the neuro-muscular system of larval and adult bryozoans (e.g. [6, 21–36]). Adult muscular systems have only been studied in a few phylactolaemate and ctenostome species [6, 28, 30, 35]. These studies demonstrated distinct differences in the digestive tract and lophophore muscle systems between phylactolaemates and ctenostomes. However, knowledge of the broader diversity of bryozoan muscular systems is lacking as only two of the six major clades have been studied [8, 37]. The aim of the current work was to investigate the diversity of ctenostome muscular systems by analyzing five of the six major ctenostome clades. The results presented here will be of substantial importance for the reconstruction of the muscular ground pattern of ctenostome bryozoans.
List of ctenostome bryozoans here studied
Ascorhiza cf. mawatarii
Amathia (Zoobotryon) verticillata
Mimosella sp. erect
Results and discussion
Description and comparison of different ctenostome muscle systems
Body-wall muscles and their derivatives
In the cheilostome Gymnolaemata and a few ctenostomes, the pore complex is associated with funicular strands that connect the polypide with the communication pores [3, 42, 43]. Distinct connecting cords were rarely encountered in this study. Some cord-like structures were encountered in the f-actin stainings of Victorella pavida and Nolella dilatata (two genera with reported funicular interconnectivity, [11, 44]; Figs. 3d, 8b). In Triticella flava, which has thin proximal stalks, a thin tissue cord is present in some specimens. However, since no nuclei were encountered adjacent to the cystid cuticle (Fig. 8c), it appears that the encountered tissue cord is composed of the epidermis and possibly an underlying peritoneum. Consequently, previous reports of funicular cords in ctenostomes could in fact be parts of the body wall rather than distinct funicular strands.
Distinct funicular strands are present in some species in the form of peritoneal cords supplied with longitudinal musculature (Fig. 3). In Paludicella articulata, two funicular cords are present. Both extend from the caecum towards the body wall, one on the proximal side close to the tip of the caecum and a second more distally at the border of the pylorus (Fig. 3a). Most other encountered muscular funiculi were mostly singular and also extended from the caecum to the body wall (Fig. 3). This corresponds to the situation previously found in the ctenostome Triticella minini  and is also the general condition of Phylactolaemata and Stenolaemata . Many cheilostomes possess a muscular caecal ligament in a similar area .
The Walkerioidea and Vesicularioidea produce polymorphic heterozooids in form of stolonal kenozooids . Stolons consist of interconnecting cystids that possess the above mentioned pore complexes and linings of the cuticle. In contrast to the Vesicularioidea, stolons in walkerioideans possess distinct muscle bundles in their distal end close to the pore complexes (Fig. 5a and c). These bundles traverse the stolon from the basal to the frontal side and were sometimes referred to as ‘dorso-ventral muscles’ , but here will be referred to as stolonal transverse muscle. Walkerioideans possess large and elongated main stolons and shorter side stolons where the feeding autozooids are situated . The stolonal transverse muscle is always present in the side stolon and fills almost the entire volume of the stolon (Fig. 5a). In the main stolon, it seems that the presence of this muscle depends on the colony form. In the creeping species Mimosella verticillata, the muscle is present in the main stolon (Fig. 5a) whereas in an erect species of the same genus, it is absent (Fig. 5c). Interestingly, the primary form of vesicularioidean ctenostomes is erect whereas walkerioideans are primarly creeping forms . Vesicularioidean ctenostomes never show any stolonal muscles ([37, 42], this study), which, along with the lack of this muscle in the main stolon of the erect Mimosella, indicates that such a muscle is only functional and present in creeping forms. In the genus Triticella that only possess extremely small heterozooids as attachment sites only show very small bundles in these polymorphs (Fig. 7b and d).
Recently, ctenostome apertural muscles were reviewed in detail . The present study confirms three principal sets of muscles: distal muscular fibers that are present as parieto-vestibular and as parieto-diaphragmatic muscles, second, peritoneal (parietovaginal) bands supplied with muscles, and the muscles associated with the vestibular wall (Fig. 2a).
The parieto-vaginal bands are homologous to the duplicature bands of the Phylactolaemata [28, 30]. As concluded from all the data available, parieto-vaginal bands are present in the ctenostome clades Alcyonidioidea, Arachnidioidea, and Paludicelloidea (cf. , this study), whereas all Hislopioidea and most Walkerioidea, Vesicularioidea and Victorelloidea have reduced these muscular bands (see  for a recent comparison). With the exception of the Hislopioidea, representatives of the other major clades commonly form colonies with very elongated peristomes or even heteromorphic colonies with interconnecting stolons between feeding autozooids [37, 48]. Consequently, it was suggested that the loss of parieto-vaginal bands might be correlated with distinct stolonization of colonies or highly enlarged peristomes (cf. ). However, the lack of parieto-vaginal bands in hislopioideans and also the discovery of the parieto-vaginal bands in the arachnidioidean genus Nolella (Fig. 6a), the vesicularioidean genus Cryptopolyzoon (Fig. 4b) and the walkerioidean Triticella minini  shows that there is no distinct correlation. Noteworthy, parieto-vaginal bands were not encountered in T. flava in contrast to T. minini.
As indicated above, some variation exists in the general arrangement of these muscle groups. Most species have an arrangement of four parieto-diaphragmatic muscles, parieto-vestibular muscles and parieto-vaginal bands. This original arrangement is modified in some encrusting sheet-like runners such as Hislopia malayensis  or Flustrellidra , which show a bilateral arrangement of the apertural muscles with two large lateral portions. The alcyonidioid genera Alcyonidium and Ascorhiza do not have a distinct arrangement of clearly defined bundles such as other ctenostomes but possess a series of diffuse apertural muscle that extend from the body wall towards the vestibular wall (Fig. 6e, f). In addition, the stolon-bearing Triticella flava also has a bilateral arrangement of its apertural muscles. This species only has a single pair of parieto-vestibular muscles.
Some other genera also show slight modifications from the four parieto-diaphragmatic and vestibular muscles: one species of Mimosella has only two parieto-diaphragmatic muscles (but four parieto-vaginal ones, Fig. 6d). In Paludicella articulata, an additional bundle of a few muscle fibers is present that originates from the disto-lateral body wall and inserts proximally into the tentacle sheath (Fig. 6b and c). These muscle are arranged in parallel to the parieto-vaginal bands. These bundles appear to be unique for this species.
Tentacle sheath muscles
The ctenostome grade tentacle sheath generally shows longitudinal smooth muscle bands that are equally distributed over the entire range of the tentacle sheath, as found in the ctenostome Hislopia malayensis  and other gymnolaemates (Fig. 4b; ). In the analyzed walkerioidean and victorelloidean species investigated so far, the tentacle sheath muscles are comprised of diagonally orientated muscles instead of longitudinal fibers (Fig. 10). Given the wide distribution of only longitudinal muscles in other groups such as cheilostomes (e.g. ), cyclostomes  and some phylactolaemates [6, 30], it is clear that the diagonal basket of these two ctenostome families is derived. Depending on the phylogenetic interpretation and interrelations of the major ctenostome clades, this character might be an apomorphy for each of these clades or a synapomorphy (see also below).
Digestive tract musculature
The caecum is supplied with a sparse net of mostly circular smooth muscles (Figs. 3b, d, 4a and e). A few longitudinal fibers are mainly found in the proximal end of the caecum. Some species show a more regular grid of circular and longitudinal muscles, but this seems to be the exception. As previously noted , this condition is strikingly different from the anatomy of Phylactolaemata where a dense cross-striated muscle basket is present [6, 30]. This is involved in peristaltic movements of food contents being pumped forwards and down within the caecum . These movements are absent among Gymnolaemata and food particles are generally rotated in the gut lumen via ciliary action of the pylorus .
In non-phylactolaemates the remaining hindgut is separated by a pyloric region towards the intestine or rectum. This region is densely ciliated causing the active movement within the stomach . As previously described for H. malayensis, the intestine terminating via the anus is supplied only with longitudinal smooth musculature in all species (Figs. 3d, 4a and 8b). This is again different from phylactolaemate species where only circular musculature is present (see ).
The lophophore is circular in all species, as is the case in all other non-phylactolaemates . Several sets of muscles can be distinguished:
Lophophoral base muscles
Lophophoral base musculature varies in its appearance, but the basic setup of 3–4 sets of muscles as previously described for Hislopia malayensis is present in all species . Proximally, several muscle bundles, the buccal dilatators, originate from the pharynx and traverse like spokes towards the lophophoral base (Fig. 2a; 13). These dilatators run at the base of each tentacle and thus correspond in number to that of the tentacles. In several instances, distinct striation is apparent in these fibers (Fig. 13d). Buccal dilatators have been found in all other studied gymnolaemate species (e.g. [3, 17]) and Cyclostomata [12, 36]. Approximately at the site where the dilatators insert; longitudinal muscle fibers extend on the lateral distal lophophoral side. These appear mostly paired and vary in the length from long (Paludicella, Nolella, ~ 25 μm, Fig. 13a and b) to rather short (e.g. Victorella, Mimosella, ~ 10-15 μm, Fig. 13c and f), which correlates with the general size of the autozooids. Sometimes these muscles appear only faintly in CLSM preparations. The muscles have so far only been described for the ctenostome Hislopia malayensis  and Triticella minini . On its distal side or in some species even slightly above it, a set of previously described ‘v-shaped’ muscles (cf. ) represents the third set of lophophoral base muscles. In most species these do not appear as continuous ‘v’ such as found in H. malayensis , but are formed by three separate actin-rich elements: a median proximal element and two laterally and distally located ‘horns’ (Fig. 13b, d and f). In some species only the lateral parts are distinguishable with the median one being absent (Fig. 13a, c and e). The last and fourth muscle at the lophophoral base is located internally on the frontal side, approximately at the level where the buccal dilatators insert on their outer rim. This muscle constitutes a continuous ring of smooth muscles as previously reported for the hislopioidean H. malayensis, in arachnidioideans (Nolella, Fig. 13a) and paludicelloideans (Paludicella, Fig. 13b) . Other major clades do not show a continuous ring musculature but similarly oriented, separate bundles of muscles (Fig. 13c-f). These are located between the tentacles and were first described in the cheilostome Cryptosula pallasiana as basal transversal muscle . The distribution of these muscles in ctenostomes, however, is never as dense and thick such as found in the cheilostome C. pallasiana and often appears as an incomplete ring with bundles between the tentacles (Fig. 13c-f). This indicates that a continuous ring muscle is the possible ancestral state of this character. In the ancestral condition of cheilostomes and some ctenostomes it was subsequently reduced to several intertentacular muscle bundles. These intertentacular muscle bundles are much more pronounced in cheilostomes as basal transversal muscle.
Tentacles in all species are always supplied with two longitudinal muscle bands – one on the frontal and another on the abfrontal side of each tentacle (Figs. 4b; 12b; 13b-d). This corresponds to the situation described for other bryozoans (Phylactolaemata: [3, 6, 20, 30, 36]; Cyclostomata: [36, 54]; Gymnolaemata: [16, 17, 28, 55]). Longitudinal tentacle muscles are commonly used for tentacle flicking , but also to contract the tentacles to make them more compact during the retraction process when contained within the tentacle sheath. Retracted tentacles are commonly contorted and their coelomic cavity often not directly visible due to the contracted state. The tentacle muscle bands are striated in all species. Only Cryptopolyzoon wilsoni has a different arrangement with striated abfrontal muscles and smooth frontal muscles. In Triticella flava, the frontal tentacle muscles start more distally than the abfrontal ones. However, samples of Triticella flava were preserved in a relaxed state with tentacles protruding from the orifice. Preservational differences may affect image interpretations when comparing well anesthetized samples to those where the lophophores are retracted.
In Victorella pavida, circular muscles were found on the distal tip of each tentacle (Fig. 12). Tentacles in bryozoans are generally the main organs for the dispersal of sperm [57, 58] and it appears likely that this species can actively open or at the very least close terminal tentacle pores for controlled release of sperm. A high-density of actin was also found in the tentacle tips of H. malayensis . The actin concentrations in the tentacles of the latter, however, differ from those in V. pavida in not being sphincter-like muscles, but rather appear as pore-like structures on each tentacle. It is not clear why this muscle has not been found in any other species so far.
The retractor muscles are prominent muscle bands extending from the proximal or lateral body wall towards the lophophoral base and parts of the anterior digestive tract. Whether these muscles are smooth or striated has been discussed in previous works  whereas the current study supports both observations (Fig. 1; 3e; 4e; 7c; 9d; 13). Most species have smooth retractor muscle fibers similar to the situation of phylactolaemates [6, 30] and cyclostomes . Previous data corroborate this finding [6, 28, 30, 35]. As mentioned, in some species retractor muscle fibers appear striated (Figs. 7c; 13d). The arrangement of the stripes appears too regular to reflect true arrangement of striated sarcomeres. In addition, the striation pattern is similar in retracted and protruded zooids. There appears to be a correlation between the number of retractor muscle fibres and these striation patterns: species with fewer and thicker fibres appear smooth whereas the striated appearance is common to species with fewer and thinner fibres. Other bryozoans have also been reported to contain striated compartments among retractor fibres (Phylactolaemata: Fredericella sultana, ; Ctenostomata: Hislopia malayensis, ). The significance and true nature of these striation patterns remains ambiguous and cannot be unambiguously answered by the methods employed to date. Nonetheless, it should inspire future work to analyze these patterns with transmission electron microscopy, particularly since it is now obvious that there exist differences among species.
Myoanatomical characters in ctenostome phylogeny
Most previous phylogenetic analyses regarded flat uni- to multiserial encrusters (e.g. Hislopioidea, Alcyonidioidea) as early branching lineages mainly due to the similarity of fossil colony morphologies (see e.g. [8, 9]). The orifical area of these species is frontally located and in these forms is rather simple either being inconspicuously elevated from the remaining cystid wall or in form of an apertural/orificial papilla. These frontal elongations are generally called peristomes. Upright colonies such as those seen in the Paludicelloidea were considered to be a derived state given that the basic colony still retains an encrusting uni-serial colony type [37, 48]. Subsequent colony branches growing upright from the substratum to form erect, bushy colony types. The basic budding mode of one distal and two lateral buds is, however, retained in these colonies.
A second type of colony morphology is characterized by an elongation of the peristome that forms longs tubes. In most cases such as found in the Victorelloidea, the peristomes contain all the contents of the polypide and only the interconnecting proximal, cystidal parts of the zooids are on the basal side. In the Arachnidioidea, the various families and species show a high variation in peristomial length with e.g. some species of Arachnidium with short peristomes, or the family Nolellidae with extremely long peristomes (similar to victorelloideans) [37, 48].
A third group consisting of two ctenostome clades, the Vesicularioidea and Walkerioidea, have independtly formed kenzooids, polymorphs devoid of any polypides, that form interconnecting modules between feeding autozooids (‘trophons’ according to ). The mode of stolon formation, however, differs among these two major clades. The Walkerioidea form stolons by separating the peristomial tube from the proximal part whereas the peristome itself becomes the stolon in the Vesicularioidea. The latter invokes peristomial budding, i.e. buds being produced on the peristome area, a feature restricted to Victorelloidea and Vesicularioidea – hence their frequently assumed close relationship [37, 48].
We plotted our current results on proposed morphological phylogenies from Jebram  and Todd . The latest tree of Waeschenbach et al.  was not considered, because of lack of representatives of any Victorelloidea, inclusions of derived forms of Walkeroidea (genus Triticella, see ), and the sole inclusion of a presumable arachnidioidean, Anguinella palmata (see also [37, 48]).
The second set, the apertural muscles, shows some variation among the different major clades, the most common being the reduction of the parieto-vaginal bands in some representatives of the major clades. As previously pointed out , stolonate forms appear to have reduced these bands. Comparison among all bryozoans show that these are present in the ground pattern and are plesiomorphic , hence calling for independent reduction of these structures in some ctenostomes.
The third set, tentacle sheath musculature is almost ubiquitously longitudinal with the exception of Victorelloidea and Walkerioidea. Depending on the phylogenetic reconstruction, these constitute independent, apomorphic characters according to Jebram’s tree (Fig. 14a) or possible synapomorphs according to Todd’s reconstruction (Fig. 14b).
List of specific muscular characters showing distinct variation among ctenostome bryozoans
Inner lophophoral base muscle
separate, basal transverse muscle
smooth or striated
smooth (few striated parts recognized)
separate, basal transverse muscle
separate, basal transverse muscle
cardiac sphincter or proventriculus
smooth or striated
The lophophoral muscles show high similarity among all ctenostomes. As indicated above, the inner lophophoral base muscles are arranged either as a single continuous ring or as distinct single basal transverse muscles. However, their distribution in the two phylogenetic trees does not seem to show any significant phylogenetic signal. Likewise, the distribution of the encountered retractor muscle fibre type (smooth vs. striated) does not seem to support certain nodes in the trees (Fig. 14).
The present analysis demonstrates both the diversity and the similarities of the muscular systems of ctenostome bryozoans. It enlarges the dataset from two major clades to six. Differences in the main muscle systems are mainly present in the apertural muscle, arrangement of tentacle sheath muscles, presence of special cardiac musculature, the lophophoral base muscle or retractor muscles (Table 2). We have provided new numerous morphological data that will aid in unraveling character evolution of both ctenostome and gymnolaemate bryozoans. Our characters will be especially important for resolving character states among ctenostome bryozoans as this systematic classification represent a paraphyletic group . Consequently, forthcoming analyses of additional morphological character evolution will not only yield insight in the ground pattern of ctenostomes, but also for gymnolaemates in general once a new robust phylogeny is available for ctenostomes.
Special thanks to all colleagues who aided in specimen collections of the past many years. Thanks to two anonymous reviewers for comments that improved the manuscript and Andrew Calcino (University of Vienna) for checking the text.
Availability of data and materials
The datasets during and/or analysed during the current study available from the corresponding author on reasonable request.
TS carried out the experiments and wrote the manuscript. AW supervised the study and contributed to data interpretation and writing of the manuscript. All authors read and approved the final version of the manuscript.
Ethics approval and consent to participate
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The authors declare that they have no competing interests.
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