Capitellid connections: contributions from neuromuscular development of the maldanid polychaete Axiothella rubrocincta(Annelida)
© Brinkmann and Wanninger; licensee BioMed Central Ltd. 2010
Received: 13 September 2009
Accepted: 8 June 2010
Published: 8 June 2010
Numerous phylogenetic analyses on polychaete annelids suggest a taxon Capitellida that comprises the three families Maldanidae, Arenicolidae and Capitellidae. Recent molecular studies support the position of the Echiura, traditionally ranked as a separate phylum, within the capitellids. In order to test the robustness of this molecular-based hypothesis we take a different approach using comparative analyses of nervous and muscle system development in the maldanid Axiothella rubrocincta. Employing immunocytochemistry in combination with confocal laserscanning microscopy, we broaden the database on capitellid organogenesis, thereby incorporating classical histological data in our analysis. Besides assessing possible shared features with the echiurans, we also discuss the variability of neural and muscular characters within the Capitellida.
The scaffold of the adult central nervous system, which is already established in early developmental stages of Axiothella, consists of cerebral commissures that give rise to simple circumesophageal connectives with fused ventral and dorsal roots and a single ventral neurite bundle. From the latter arise segmental neurites that innervate the peripheral bodywall. Since there is no observable regular pattern, and individual neurites are lost during ontogeny, their exact arrangement remains elusive. The pharynx is encircled by a prominent stomatogastric nerve ring, with a pair of anterior and lateral proboscis neurites directly connecting it to the central nervous system. One pair of ventral and one pair of dorsal longitudinal muscles form the earliest rudiments of the bodywall musculature in late larval stages, while a continuous layer of circular muscles is lacking throughout ontogeny.
Comparative neurodevelopmental analysis of capitellid and echiuran species reveals several common characters, including simple circumesophageal connectives, a single fused ventral nerve strand, and a stomatogastric ring nerve, that support a close relationship of both taxa, thus corroborating recent molecular phylogenetic analyses. The data on myogenesis show that four longitudinal muscle bands most likely represent an ancestral character not only for the Capitellida, but for the Annelida in general. Whether or not circular muscles are part of the annelid groundpattern remains uncertain.
The Maldanidae, also referred to as 'bamboo worms', comprise a group of deposit-feeding polychaete annelids that live in tubes composed of bottom material. They are usually considered related to the Arenicolidae and Capitellidae, and these three families are grouped together in the taxon Capitellida . Recent molecular analyses have confirmed the established hypothesis of a close relationship between the Maldanidae and the Arenicolidae (lugworms) [2–4] and have repeatedly found indications that Echiura, a hotly debated group that has been traditionally ranked as a separate phylum, nests within the capitellid polychaetes [2–7]. This novel view on the phylogenetic position of the echiurans is further supported by morphological studies on neurogenesis [8–10]. In this context, investigation of the maldanid species Axiothella rubrocincta not only offers an opportunity to assess the ingroup variability of neural characters within the Capitellida but also allows to compare neurogenesis and nervous system organization with those data that recently have become available for echiurans. This serves as an independent test of the molecular data which propose the placement of the echiurans within the Capitellida.
Apart from the relevance of maldanids for the evolution of neural characters, Axiothella may also aid in casting light on the ancestral state of muscular systems in annelids and lophotrochozoans as a whole. The musculature of the Capitellida comprises a closed outer layer of circular fibers similar to that of clitellate oligochaetes . However, in contrast to the latter group, recent studies have shown that circular muscles are only weakly developed or even absent in most polychaete taxa [11, 12], and it has been argued that absence of circular muscles represents the plesiomorphic state for the entire Annelida . Therefore, the presence of closed circular muscles in the Maldanidae represents a striking exception that deserves further investigation.
The systematics of the monophyletic Maldanidae is primarily based on external morphological features of the head, pygidium, and setae [13, 14]. The maldanid ingroup relationships, as well as the monophyly of the individual subtaxa, are still unresolved [14, 15]. Most studies of the internal morphology of maldanid polychaetes have focused on members of the subfamily Euclymeninae , to which also the investigated species, Axiothella rubrocincta, belongs. In particular, the comprehensive investigations of Pilgrim [16–21] serve thereby as a basis for comparison of our data on neuro- and myogenesis. We discuss the present data in the context of a hypothesized close annelid-echiuran relationship and contribute to the discussion on ancestral bodyplan features of the Annelida. In this respect, it has to be taken into account that A. rubrocincta represents a sibling species complex with considerable plasticity between populations concerning reproductive mode, size, and feeding, but with no obvious morphological differences . Herein, we have adopted most of Pilgrim's [19–21] designations. However, we use different terms for some neuronal structures and the anterior-most muscles in the head region due to incongruency of the macro-anatomical data described by Pilgrim, which are based on light microscopy, and our confocal microscopy data.
Neurogenesis as revealed by anti-tubulin immunoreactivity
Apart from that, the number and arrangement of segmental neurites, which branch off the ventral neurite bundle, changes considerably between the 4- and 7-setiger stage. At first, two major segmental neurites are visible in the head region (Figure 2E). In most of the following setigers, approximately four segmental neurites are present in the posterior part of the segments (Figure 2E). Most of these segmental neurites appear to be ring neurites (Figure 2J, inset). Their exact arborization patterns are elusive, since their arrangement is different in the various segments. Moreover, the segmental neurites are partly reduced during development. In particular, in the anterior segments only a few small and irregularly distributed neurite branches are visible in the 7-setiger stage (Figure 2G and 2J). In the posterior four segments, however, various segmental neurites are still present. Some of these are located at the segmental borders, whereas others appear to be positioned at intersegmental furrows in the epidermis (Figure 2J).
Serotonergic nervous system
FMRFamidergic nervous system
In pre-segmental larval stages, the first F-actin staining labels few, very delicate muscle fibers of the bodywall. The most prominent ones are oriented in a longitudinal direction and have a ventro- or a dorso-lateral position (Figure 4A). In larvae with three setigers, these longitudinal muscles form very broad muscle bands. Thus, one pair of ventral and one pair of dorsal longitudinal muscles extend from the peristomium to the posterior-most part of the body, where an anal sphincter is visible in the pygidium (Figure 4B and 4D). The labeled prostomial and peristomial muscles arise from anterior elongations of the longitudinal muscles. Laterally, setal muscles are attached to the base of the setal sheath (Figure 4B). In 5-setiger individuals, the median layer of both ventral longitudinal muscles tapers towards the prostomial tip, forming the anterior diagonal muscles, whereas the innermost layer is directed towards the mouth (Figure 4D). The latter composes the longitudinal retractor sheath muscle of the pharynx. Later on, the bucco-pharyngeal musculature exhibits a basket-like structure comprising in addition circular retractor sheath muscles. The dorsal portion of the ventral longitudinal muscles extends straight towards the anterior pole of the prostomium (Figure 4G). Interestingly, a continuous sheath of circular bodywall muscles is lacking throughout development of Axiothella, and the four longitudinal muscle bands do not form a closed muscle layer.
Development and structure of the nervous system in Capitellida
Immunocytochemical data on polychaete neurogenesis remain scarce and are mostly restricted to isolated developmental stages. At present, there are only few studies that document the neuronal differentiation for complete developmental series and they focus on polychaetes with an indirect mode of development [28–31]. The two classical TEM-based studies on species of the Capitellida likewise offer only limited insights. The first is restricted to the 3-setiger larva of Arenicola cristata (Arenicolidae), whereas the second one describes different developmental stages up to metamorphosis in Capitella capitata (Capitellidae) [32, 33]. In both studies the presented ultrastructural data are only superficially interpreted with respect to gross morphology.
One of the most prominent features of trochozoan larvae is the ciliated prototroch and its underlying serotonergic nerve ring. The latter was most likely already present in the last common ancestor of the lophotrochozoans [34, 35]. Although developmental stages of Axiothella rubrocincta possess a ciliated prototroch, a corresponding serotonergic innervation was not found in the present study, thus corroborating earlier studies on the benthic larvae of Arenicola . Accordingly, it appears likely that the larvae of Axiothella may have secondarily lost not only the serotonergic innervation of the prototroch, but maybe the entire prototroch nerve as such.
Elements of the adult central nervous system, such as the cerebral ganglion, the circumesophageal connectives, and the ventral neurite bundle, are established at a very early stage of Axiothella development. This simple and essentially adult organization of the central nervous system in larval stages corresponds to the neuronal arrangement described for the benthic larva of Arenicola and other direct developing polychaete annelids [32, 36]. One characteristic feature during the observed developmental period, however, is the apparently unpaired ventral neurite bundle that does not show a primarily dichotomous organization in Axiothella. By contrast, the larvae of Arenicola possess a broad ventral neurite bundle . In the genus Capitella, two different conditions have been documented, namely a penta-neural organization in C. capitata and two separate axonal tracts in C. teleta [36–38]. This variety in the neuronal composition of the ventral neurite bundle in developmental stages is also known from other polychaete larvae and may either indicate distant phylogenetic relationships or merely reflect the recently suggested general wide plasticity of polychaete neural patterning and nervous system anatomy . Apart from that, the general arrangement of the central nervous system is consistent with previous investigations of the adult maldanid and arenicolid neuroanatomy [21, 39–42]. For example, no indications of ganglionic segmentation have been found in Arenicola . Moreover, the description of the adult ventral nerve cord in the maldanid species Clymenella torquata  can be directly correlated with the observed threefold pattern of the ventral neurite bundle with one median and two lateral main strands in the tubulin, serotonin, and FMRF-amide stainings. It is highly probable that the lateral tubulinergic strands can be assigned to a dorsally located fibrous neuropil which is separated into two parts by giant fibers that run along the ventral midline. Such multicellular giant nerve fibers have been described for several species of the Capitellida [21, 39, 41, 43–45]. The serotonergic and FMRFamidergic median strand of the ventral neurite bundle in Axiothella represents most likely the precursor of such a giant nerve.
Despite these similarities in the central nervous system, conflicting views exist with regard to the stomatogastric and peripheral nervous system. The prominent stomatogastric nerve ring around the pharynx in Axiothella rubrocincta has not been mentioned in previous studies on the nervous system of the Maldanidae . However, the neuronal fibers that connect the ring nerve to the central nervous system have been depicted and described in a similar way for the euclymenin species Clymenella torquata [; Figure 3 present work]. The position and course of the lateral proboscis nerve in Clymenella, termed anterior ring nerve by Pilgrim , is almost identical to the one in Axiothella. The same holds true for the anterior proboscis nerves, which only differ in number, with one nerve being present in Axiothella and in several species of the genus Clymene, and three anterior proboscis nerves in Clymenella [21, 46–48]. It has to be taken into account that this comparison involves on the one hand different taxa and on the other juvenile versus adult features. Given, in addition, the above stated differences in the applied methodology, it is not possible to unequivocally decide whether or not these differences indeed reflect natural conditions. However, in Capitella, a pair of nerves, emanating from the cerebral neuropil, encircles the mouth region, and the even more closely related taxon Arenicola has an additional nerve ring that surrounds the foregut at the transition between the pharynx and the esophagus [33, 49]. Moreover, the descriptions of the nerves that supply the bucco-pharyngeal region in Arenicola agree in basic features with the documented arrangement in Axiothella and Clymenella [41, 49]. Accordingly, irrespective of the varying position of the stomatogastric nerve ring, this feature is most probably part of the groundpattern of Capitellida.
The peripheral nervous system of Axiothella consists mainly of the segmental neurites that emerge from the ventral neurite bundle. Additional longitudinal nerve fibers have not been detected in the setigers. The arborization patterns and the exact number of the segmental neurites per setiger remain elusive. However, the arrangement of the segmental neurites does not show an obvious metameric pattern and the number of these neurites is apparently reduced during development of Axiothella. Similar observations have been documented previously for the adult nervous system of other maldanid taxa [21, 39]. This has led to the conclusion that the nervous system of the Maldanidae shows only few signs of metamerism, namely by the presence of larger clusters of neurons opposite the parapodia and of larger nerves at the segment boundaries . In Arenicola, however, the organization of the nervous system is very regular. A pair of nerves originates from the ventral nerve cord at the level of the borders between annuli, while opposite each setigerous annulus there are two to four pairs of nerves . Slight differences in the life history traits and ecology of Axiothella and Arenicola might be the reason for the disparity in the organization of the peripheral nervous system.
Comparative aspects of the capitellid and the echiuran nervous system
Comparison of the capitellid and echiuran nervous system
repetitive units of nerve cells
metameric, peripheral neurites
single ventral neurite bundle
simple circumesophageal connectives
stomatogastric nerve ring
Myogenesis of the bodywall musculature in Capitellida
The number and position of longitudinal muscle bands in adult polychaete annelids varies considerably among taxa . However, there are only four to six longitudinal muscle bands present in most polychaetes . In contrast to that, the altered arrangement in larvae of Capitella with eight primary longitudinal muscles most likely constitutes an exception due to secondary multiplication .
In the case of adult individuals of Axiothella rubrocinta, the number of longitudinal strands is not known. However, the closely related maldanid species Clymenella torquata has been depicted by illustrations of cross sections with up to six longitudinal bands that form an almost closed muscle layer . In larval stages of Axiothella, only four delicate longitudinal muscles form the precursors of the later paired ventral and dorsal longitudinal muscle bands. Similarly, one pair of ventrolateral and another pair of dorsolateral longitudinal muscles are present in the 3-setiger larva of Arenicola cristata . Four longitudinal muscles have also been documented in all recently investigated polychaete larvae and in developmental stages of some oligochaetes [30, 53–55]. In sipunculan larvae, the first longitudinal muscle fibers likewise form a quartet and give rise to the retractor muscles of the adult [56, 57]. These data strongly suggest that two pairs of primary longitudinal muscles organized in separate strands represent the plesiomorphic condition for the Capitellida and the Annelida altogether, although data on muscle development of a number of annelid taxa including the echiurans are still lacking.
Circular bodywall muscles are either poorly developed or not present in most polychaete taxa studied so far . This absence of circular fibers has been interpreted as a plesiomorphic polychaete character . Accordingly, the circular fibers of the capitellid species that form a closed muscle layer, similar to that of the clitellates, could represent an apomorphic feature of this group. In the investigated individuals of Axiothella, however, circular fibers have neither been documented in the pre-segmental larvae nor in the 7-setiger juveniles. In fact, in adult specimens of Axiothella the longitudinal bodywall muscles are usually more prominently developed than the circular fibers . Accordingly, the lack of circular fibers during development implies that these muscles are not a larval character in Axiothella but that development of circular muscles is restricted to adult stages. By contrast, complete circular fibers have been interpreted as a juvenile polychaete character due to their presence in progenetic species such as Dinophilus gryociliatus and Parapodrilus psammophilus .
The gradual anterior-posterior development of circular muscles starts only after the initial differentiation of the longitudinal fibers in larvae of Capitella . In the 3-setiger larva of Arenicola, circular fibers are present in more or less regular intervals along the longitudinal body axis . Unfortunately, the dynamics involved in the formation of this circular musculature in Arenicola have not been studied. However, based on the gap in timing between the differentiation of longitudinal and circular muscles in Capitella, it has been suggested that the lack of circular fibers in polychaetes could be interpreted as a convergent reduction due to 'switching off' of the respective ontogenetic program . Hence, the last common annelid ancestor might have possessed weak circular fibers which only differentiate relatively late during ontogeny. The complete layer of circular fibers, as expressed in the clitellates and capitellids, would then have evolved only in a second step to enable peristaltic movement and burrowing in firm substrate .
The presence of circular muscles is a shared feature of the capitellid taxa, despite the heterogeneous development of this muscle group. However, the question whether circular muscles are part of the annelid groundplan is still under discussion, also because the phylogenetic tree of the Annelida remains unresolved [2–4]. Moreover, the different myogenetic pathway of circular muscle formation in sipunculans, described recently as a synchronous-fission-type, strikingly shows the divergent ontogenetic routes that lead to the establishment of the circular layer of the bodywall musculature in annelids and their closest allies .
Our immunocytochemical data on morphogenesis in the maldanid Axiothella complement previous studies and facilitate a comparison of the nervous system and musculature in capitellid polychaetes. Based on this comparative analysis, it appears that the adult nervous system of the Capitellida is secondarily reduced, comprising simple circumesophageal connectives, a characteristic stomatogastric nerve ring, and a single ventral connective as shared characters. The arrangement and number of segmental nerves and ganglion-like clusters of perikarya differ in the investigated species, possibly due to differences in the benthic life style. The data on myogenesis support the view that four longitudinal muscle bands are ancestral for Capitellida and the entire Annelida, while the presence of circular muscles is certainly a shared but not necessarily a plesiomorphic feature of the former.
The general organization of the nervous system is largely similar in capitellid and echiuran species, corroborating molecular analyses that argue for a close relationship of both taxa. However, further investigations, in particular of the neuronal connections between the stomatogastric and the central nervous system in echiuran species, are needed to substantiate this notion, since some of these common morphological traits might have been caused by convergent reduction events.
Animal collection and fixation
Tubes housing adult Axiothella rubrocincta (Johnson, 1901) were collected in the intertidal of False Bay, San Juan Island, Washington, USA, during summer 2008. The tubes contained mucous cocoons from which larvae were dissected and transferred to Petri dishes filled with Millipore-filtered seawater (MFSW). Within the cocoons, the most advanced developmental stages were found to be 7-setiger juveniles, of which some exhibit precursors of additional segments. Prior to fixation, the specimens were anesthetized with a 1:1 dilution of MFSW and MgCl2 (7%). They were then fixed at room temperature in 4% paraformaldehyde in 0.1 M phosphate buffer (PB) for 1.5 h, washed three times in PB, and stored at 4°C in PB containing 0.1% sodium azide (NaN3).
Immunolabeling and confocal laserscanning microscopy (CLSM)
The following steps were all performed at 4°C. Antibody staining was preceded by tissue permeabilization for 1 h in 0.1 M PB with 0.1% NaN3 and 0.1% Triton X-100 (PTA), followed by overnight incubation in block-PTA [6% normal goat serum (Sigma-Aldrich, St. Louis, MO, USA) in PTA]. The primary antibodies, polyclonal rabbit anti-serotonin (Zymed, San Francisco, CA, USA, dilution 1:800), polyclonal rabbit anti-FMRFamide (Chemicon, Temecula, CA, USA, dilution 1:400), and monoclonal mouse anti-acetylated α-tubulin (Sigma-Aldrich, dilution 1:1000), all in block-PTA, were either applied separately or in a mixed cocktail for 24 h. Subsequently, the specimens were rinsed in block-PTA with three changes over 6 h and incubated in a mixture of 4'6-diamidino-2-phenyl-indole [DAPI (Invitrogen, Eugene, OR, USA)], secondary fluorochrome-conjugated antibodies [goat anti-rabbit FITC (Sigma-Aldrich), dilution 1:400; goat anti-rabbit Alexa Fluor 594 (Invitrogen), dilution 1:1000; goat anti-mouse FITC (Sigma-Aldrich), dilution 1:400] and, for F-actin visualization, Alexa Fluor 488 phalloidin (Molecular Probes, Eugene, OR, USA; dilution 1:40) in block-PTA overnight. Finally, the specimens were washed three times in PB without NaN3 and were directly mounted in Fluoromount G (Southern Biotech, Birmingham, AL) on glass slides. A minimum of 10 immunolabeled specimens per developmental stage was analyzed for each antibody. Approximately 65 image stacks of optical sections were recorded as Z-wide-projections with 0.1-0.5 μm step size using a Leica DM IRE2 fluorescence microscope equipped with a Leica TCS SP 2 confocal laserscanning unit (Leica, Wetzlar, Germany). Setae are visible in the tubulin scans due to autofluorescence. Images were processed with Adobe Photoshop CS3 to adjust contrast and brightness and were arranged into figure plates using Adobe Illustrator CS3 (Adobe Systems, San Jose, CA, USA). The three-dimensional computer reconstructions were generated with the imaging software Imaris v. 5.5.3 (Bitplane, Zürich, Switzerland) using surface rendering algorhithms.
anterior proboscis neurite
accessory stomatogastric nerve ring
nerves of the buccal epithelium
circular muscle of the retractor sheath
dorsal lobe of the cerebral ganglion
dorsal longitudinal muscle bundle
dorsal serotonergic perikarya
diagonal ventral longitudinal muscle
longitudinal muscle fiber
longitudinal muscle of the retractor sheath
lateral proboscis neurite
peripheral network of neurites
neuronal stomatogastric projection
stomatogastric nerve ring
straight ventral longitudinal muscle
ventral lobe of the cerebral ganglion
ventral longitudinal muscle bundle
ventral neurite bundle
ventral serotonergic perikarya.
We are grateful to Tim Wollesen (University of Copenhagen) for collection and fixation of the material used herein. NB is the recipient of an EU fellowship within the MOLMORPH network under the 6th Framework Program 'Marie Curie Host Fellowships for Early Stage Research Training' (contract number MEST-CT-2005-020542), which is coordinated by AW.
- Fauchald K, Rouse GW: Polychaete systematics: Past and present. Zool Scr. 1997, 26: 71-138. 10.1111/j.1463-6409.1997.tb00411.x.View ArticleGoogle Scholar
- Rousset V, Pleijel F, Rouse GW, Erséus C, Siddall ME: A molecular phylogeny of annelids. Cladistics. 2007, 23: 1-23. 10.1111/j.1096-0031.2006.00128.x.View ArticleGoogle Scholar
- Struck TH, Schult N, Kusen T, Hickman E, Bleidorn C, McHugh D, Halanych KM: Annelid phylogeny and the status of Sipuncula and Echiura. BMC Evol Biol. 2007, 7: 57-10.1186/1471-2148-7-57.PubMed CentralView ArticlePubMedGoogle Scholar
- Zrzavý J, Říha P, Piálek L, Janouškovec J: Phylogeny of Annelida (Lophotrochozoa): total-evidence analysis of morphology and six genes. BMC Evol Biol. 2009, 9: 189-10.1186/1471-2148-9-189.PubMed CentralView ArticlePubMedGoogle Scholar
- Bleidorn C, Vogt L, Bartolomaeus T: A contribution to sedentary polychaete phylogeny using 18S rRNA sequence data. J Zool Syst Evol Res. 2003, 41: 186-195. 10.1046/j.1439-0469.2003.00212.x.View ArticleGoogle Scholar
- Bleidorn C, Vogt L, Bartolomaeus T: New insights into polychaete phylogeny (Annelida) inferred from 18S rDNA sequences. Mol Phyl Evol. 2003, 29: 279-288. 10.1016/S1055-7903(03)00107-6.View ArticleGoogle Scholar
- Hall KA, Hutchings P, Colgan D: Further phylogenetic studies of the Polychaeta using 18S rDNA sequence data. J Mar Biol Assoc UK. 2004, 84: 949-960. 10.1017/S0025315404010240h.View ArticleGoogle Scholar
- Hessling R: Metameric organisation of the nervous system in developmental stages of Urechis caupo (Echiura) and its phylogenetic implications. Zoomorphology. 2002, 121: 221-234. 10.1007/s00435-002-0059-7.View ArticleGoogle Scholar
- Hessling R, Westheide W: Are Echiura derived from a segmented ancestor? Immunohistochemical analysis of the nervous system in developmental stages of Bonellia viridis. J Morphol. 2002, 252: 100-113. 10.1002/jmor.1093.View ArticlePubMedGoogle Scholar
- Hessling R: Novel aspects of the nervous system of Bonellia viridis (Echiura) revealed by the combination of immunohistochemistry, confocal laser-scanning microscopy and three-dimensional reconstruction. Hydrobiologia. 2003, 496: 225-239. 10.1023/A:1026153016913.View ArticleGoogle Scholar
- Tzetlin AB, Filippova AV: Muscular system in polychaetes (Annelida). Hydrobiologia. 2005, 113-126. 10.1007/s10750-004-1409-x. 535/536
- Purschke G, Müller MCM: Evolution of body wall musculature. Integr Comp Biol. 2006, 46: 497-507. 10.1093/icb/icj053.View ArticlePubMedGoogle Scholar
- Green KD: Septa and nephridia of maldanid polychaetes of the subfamily Maldanidae. Bull Mar Sci. 2000, 67: 373-389.Google Scholar
- Rouse GW, Pleijel F: Polychaetes. 2001, Oxford: University PressGoogle Scholar
- Hausen H, Bleidorn C: Significance of chaetal arrangement for maldanid systematics (Annelida: Maldanidae). Sci Mar. 2006, 70S3: 75-79.Google Scholar
- Pilgrim M: The functional anatomy of the reproductive systems of the polychaetes Clymenella torquata and Caesicirrus neglectus. Proc Zool Soc London. 1964, 143: 443-464.View ArticleGoogle Scholar
- Pilgrim M: The coelomocytes of the maldanid polychaetes Clymenella torquata and Euclymene oerstedi. J Zool. 1965, 147: 30-37. 10.1111/j.1469-7998.1965.tb01875.x.View ArticleGoogle Scholar
- Pilgrim M: The functional anatomy and histology of the alimentary canal of the maldanid polychaetes Clymenella torquata and Euclymene oerstedi. J Zool. 1965, 147: 387-405. 10.1111/j.1469-7998.1966.tb02907.x.View ArticleGoogle Scholar
- Pilgrim M: The morphology of the head, thorax, proboscis apparatus and pygidium of the maldanid polychaetes Clymenella torquata and Euclymene oerstedi. J Zool. 1966, 148: 453-475. 10.1111/j.1469-7998.1966.tb02963.x.View ArticleGoogle Scholar
- Pilgrim M: The anatomy and histology of the blood system of the maldanid polychaetes Clymenella torquata and Euclymene oerstedi. J Zool. 1966, 149: 242-261. 10.1111/j.1469-7998.1966.tb03896.x.View ArticleGoogle Scholar
- Pilgrim M: The anatomy and histology of the nervous system and excretory system of the maldanid polychaetes Clymenella torquata and Euclymene oerstedi. J Morphol. 1978, 155: 311-326. 10.1002/jmor.1051550305.View ArticlePubMedGoogle Scholar
- Wilson WH: Life-history evidence for sibling species in Axiothella rubrocincta (Polychaeta: Maldanidae). Mar Biol. 1983, 76: 297-300. 10.1007/BF00393032.View ArticleGoogle Scholar
- Bookhout CG, Horn EC: The development of Axiothella mucosa (Andrews). J Morphol. 1949, 84: 145-183. 10.1002/jmor.1050840107.View ArticlePubMedGoogle Scholar
- Dales RP: The polychaete stomodeum and the inter-relationships of the families of Polychaeta. Proc Zool Soc London. 1962, 139: 389-428.View ArticleGoogle Scholar
- Purschke G: Pharynx. The ultrastructure of Polychaeta. Edited by: Westheide W, Hermans CO. 1988, Microfauna Marina, 4: 177-197.Google Scholar
- Green KD: The head of Maldanidae polychaetes of the subfamily Maldaninae. Mém Mus natn Hist nat. 1994, 162: 101-109.Google Scholar
- Tzetlin A, Purschke G: Pharynx and intestine. Hydrobiologia. 2005, 535/536: 199-225. 10.1007/s10750-004-1431-z.View ArticleGoogle Scholar
- Hay-Schmidt A: The larval nervous system of Polygordius lacteus Schneider, 1896 (Polygordiidae, Polychaeta): Immunocytochemical data. Acta Zool. 1995, 76: 121-140. 10.1111/j.1463-6395.1995.tb00987.x.View ArticleGoogle Scholar
- Voronezhskaya EE, Tsitrin EB, Nezlin LP: Neuronal development in larval polychaete Phyllodoce maculata (Phyllodocidae). J Comp Neurol. 2003, 455: 299-309. 10.1002/cne.10488.View ArticlePubMedGoogle Scholar
- McDougall C, Chen W-C, Shimeld SM, Ferrier DE: The development of the larval nervous system, musculature and ciliary bands of Pomatocerus lamarckii (Annelida): heterochrony in polychaetes. Front Zool. 2006, 3: 16-10.1186/1742-9994-3-16.PubMed CentralView ArticlePubMedGoogle Scholar
- Brinkmann N, Wanninger A: Larval neurogenesis in Sabellaria alveolata reveals plasticity in polychaete neural patterning. Evol Dev. 2008, 10: 606-618. 10.1111/j.1525-142X.2008.00275.x.View ArticlePubMedGoogle Scholar
- Marsden JR, Lacalli T: Morphology and behaviour of the benthic larva of Arenicola cristata (Polychaeta). Can J Zool. 1978, 56: 224-237. 10.1139/z78-032.View ArticleGoogle Scholar
- Bhup R, Marsden JR: The development of the central nervous system in Capitella capitata (Polychaeta, Annelida). Can J Zool. 1982, 60: 2284-2295. 10.1139/z82-295.View ArticleGoogle Scholar
- Wanninger A: Comparative lophotrochozoan neurogenesis and larval neuroanatomy: recent advances from previously neglected taxa. Acta Biol Hung. 2008, 59 (Suppl): 127-136. 10.1556/ABiol.59.2008.Suppl.21.View ArticlePubMedGoogle Scholar
- Wanninger A: Shaping the things to come: ontogeny of lophotrochozoan neuromuscular systems and the Tetraneuralia concept. Biol Bull. 2009, 216: 293-306. 10.2307/25548161.PubMedGoogle Scholar
- Orrhage L, Müller MCM: Morphology of the nervous system of Polychaeta (Annelida). Hydrobiologia. 2005, 535/536: 79-111. 10.1007/s10750-004-4375-4.View ArticleGoogle Scholar
- Meyer NP, Seaver EC: Neurogenesis in an annelid: characterization of brain neural precursors in the polychaete Capitella sp. I. Dev Biol. 2009, 335: 237-252. 10.1016/j.ydbio.2009.06.017.View ArticlePubMedGoogle Scholar
- Blake JA, Grassle JP, Eckelbarger KJ: Capitella teleta, a new species designation for the opportunistic and experimental Capitella sp. I, with a review of the literature for confirmed records. Zoosymposia. 2009, 2: 25-53.Google Scholar
- Lewis M: Studies on the central and peripheral nervous system of two polychaete annelids. Proc Amer Acad Arts Sci. 1898, 33: 225-268.View ArticleGoogle Scholar
- Gamble FW, Ashworth JH: The habits and structure of Arenicola marina. Q J Microsc Sci. 1898, 41: 1-42.Google Scholar
- Gamble FW, Ashworth JH: The anatomy and classification of the Arenicolidae, with some observations on their postlarval stages. Q J Microsc Sci. 1900, 43: 419-569.Google Scholar
- Ashworth JH: The anatomy of Arenicola assimilis, Ehlers, and of a new variety of the species, with some observations on the post-larval stages. Q J Microsc Sci. 1903, 46: 737-781.Google Scholar
- Wells GP: Giant nerve cells and fibres in Arenicola claparedii. Nature. 1958, 182: 1609-1610. 10.1038/1821609a0.View ArticlePubMedGoogle Scholar
- Mangum CP, Passano LM: The giant nerve fibres in maldanid polychaetes. Nature. 1964, 201: 210-211. 10.1038/201210a0.View ArticlePubMedGoogle Scholar
- Bullock TH, Horridge GA: Structure and function in the nervous system of invertebrates. 1965, London: WH Freeman and Company, 1:Google Scholar
- de Quatrefages A: Mémoire sur le système nerveux des Annélides. Ann Sci Nat Zool. 1850, 14: 329-398.Google Scholar
- Racovitza ÉG: Le lobe céphalique et l'encéphale des Annelides polychètes (Anatomie, Morphologie, Histologie). Arch Zool exp gen. 1896, 4: 133-343.Google Scholar
- Orlandi S: Maldanidi del Golfo di Napoli con osservazioni sopra alcuni punti della loro anatomia ed istologia. Atti Soc Ligust Sci Nat Geogr. 1898, 9: 257-311.Google Scholar
- Whitear M: The stomatogastric nervous system of Arenicola. Q J Microsc Sci. 1953, 94: 293-302.Google Scholar
- Eisig HD: Die Capitelliden des Golfes von Neapel. Fauna und Flora des Golfes von Neapel. 1887, 16: 1-908.Google Scholar
- Purschke G: On the groundpattern of Annelida. Org Divers Evol. 2002, 2: 181-196. 10.1078/1439-6092-00042.View ArticleGoogle Scholar
- Hill SD, Boyer BC: Phalloidin labeling of developing muscle in embryos of the polychaete Capitella sp. I. Biol Bull. 2001, 201: 257-258. 10.2307/1543353.View ArticlePubMedGoogle Scholar
- Bergter A, Hunnekuhl VS, Schniederjans M, Paululat A: Evolutionary aspects of patterning formation during clitellate muscle development. Evol Dev. 2007, 9: 602-617.View ArticlePubMedGoogle Scholar
- Bergter A, Brubacher J, Paululat A: Muscle formation during embryogenesis of the polychaete Ophryotrocha diadema (Dorvilleidae) - new insights into annelid muscle patterns. Front Zool. 2008, 5: 1-10.1186/1742-9994-5-1.PubMed CentralView ArticlePubMedGoogle Scholar
- Brinkmann N, Wanninger A: Integrative analysis of polychaete ontogeny: cell proliferation patterns and myogenesis in trochophore larvae of Sabellaria alveolata. Evol Dev. 2010, 12: 5-15. 10.1111/j.1525-142X.2009.00386.x.View ArticlePubMedGoogle Scholar
- Wanninger A, Koop D, Bromham L, Noonan E, Degnan BM: Nervous and muscle system development in Phascolion strombus (Sipuncula). Dev Genes Evol. 2005, 215: 509-518. 10.1007/s00427-005-0012-0.View ArticlePubMedGoogle Scholar
- Schulze A: Musculature in sipunculan worms: ontogeny and ancestral states. Evol Dev. 2009, 11: 97-108. 10.1111/j.1525-142X.2008.00306.x.View ArticlePubMedGoogle Scholar
- Kudenov JD: The functional morphology of feeding in three species of maldanid polychaetes. Zool J Linn Soc. 1977, 60: 95-109. 10.1111/j.1096-3642.1977.tb00835.x.View ArticleGoogle Scholar
- Rüchel J, Müller MCM: F-actin framework in Spirorbis cf. spirorbis (Annelida: Serpulidae): phalloidin staining investigated and reconstructed by cLSM. Invertebr Biol. 2007, 126: 173-182. 10.1111/j.1744-7410.2007.00087.x.View ArticleGoogle Scholar
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