Myoanatomy and anterior muscle regeneration of the fireworm Eurythoe cf. complanata (Annelida: Amphinomidae)

Abstract

Amphinomidae or so-called "fireworms" are known for their inflammatory substances and their regeneration ability. Recent transcriptome-based molecular analyses revealed that these remarkable annelids are a basal branching taxon outside the annelid main radiation (Pleistoannelida). Although several studies dealing with analyses of the morphology of these annelids have been published, detailed investigations of the anterior muscle regeneration and the musculature in general are largely lacking for amphinomids. Using histology, phalloidin labeling together with subsequent confocal laser scanning microscopy (cLSM), and further light microscopic image acquisition of different regeneration stages, we here present the first morphological study describing the myoanatomy and muscular regeneration. During anterior muscular regeneration, longitudinal muscle bundles develop prior to transverse muscle fibers and segment boundaries. Additionally, Eurythoe cf. complanata develops an independent muscular ring surrounding the mouth opening in an early stage of regeneration. Detailed investigation of adult body wall musculature and the parapodial muscle complex in amphinomids show that E. cf. complanata bears well-developed dorsal and ventral longitudinal muscle bundles as well as outer transverse muscles comparable to the pattern described for several Pleistoannelida. Furthermore, the biramous parapodia possess a complex meshwork of distinct muscle fibers allowing detailed comparisons with other annelid families.

Pygospio elegans (Annelida: Spionidae) — an annelid model for regeneration studies

“…First signs of muscular regeneration become visible only at 3-4 dpa. At the anterior end the first elements that become distinguishable, are longitudinal muscles as well as the musculature, surrounding the mouth opening that is in great accordance with data available on amphinomids and cirratulids (Weidhase et al, 2014(Weidhase et al, , 2015(Weidhase et al, , 2016. It is interesting to note that during larval development in annelids, the longitudinal muscles appear far prior to transversal or oblique ones (McDougall et al, 2006;Fisher et al, 2010), so we can assume some similarities in muscle formation programs between larval development and regeneration.…”

“…Despite the first CA elements were detected at 2 dpa, the process begins slowly and has apparently saltatory character. Comparison with the data available on the annelid central nervous system regeneration (Müller et al, 2003;Müller, 2004;Lindsay et al, 2008;Weidhase et al, 2014Weidhase et al, , 2015Weidhase et al, , 2016Kozin et al, 2017) together with our preliminary unpublished data clearly suggests that CA-positive structures appear later than many other nerve elements. We can suppose that CA-positive neurons in the central nervous system may play higher associative functions.…”

Regeneration mechanisms in Syllidae (Annelida)

“…Some of the most recent studies were those published by Franke (, ), Heacox and Schroeder (), and Franke and Pfannenstiel (). After three decades, this topic re‐emerged with a study about the role of the proventricle during the stolonization of T. antoni (Weidhase, Bleidorn et al., ). This species was also used for investigating muscular and nervous system regeneration (Weidhase, Beckers et al., ; Weidhase et al., ).…”

“…Annelids, commonly referred to as “segmented worms,” have remarkable abilities of whole‐body regeneration, even from few segments (Bely, , ; Seaver, ). Hence some species have been considered as excellent models to investigate regeneration, such as Alitta virens (Bakalenko, Novikova, Nesterenko, & Kulakova, ; Kozin, Filippova, & Kostyuchenko, ) , Capitella teleta (Hill, Ferkowicz, & Grassle, ; Jong & Seaver, ), Cirratulus cirratus (Weidhase, Bleidorn, & Helm, ), Enchytraeus japonensis (Myohara, Yoshida‐Nora, Kobari, & Tochinai, ; Ogawa et al., ), Eurythoe complanata (Müller, Berenzen, & Westheide, ; Weidhase, Bleidorn, Beckers, & Helm, ), Lamellibrachia satsuma (Miyamoto, Shinozaki, & Fujiwara, ), Platynereis dumerilii (Prud'homme et al., ; Starunov, Voronezhskaya, & Nezlin, ), Pristina leidyi (Bely & Wray, ; Nyberg, Conte, Kostyun, Forde, & Bely, ; Özpolat, Sloane, Zattara, & Bely, ) , Timarete punctata (Weidhase, Helm, & Bleidorn, ), and Typosyllis antoni (Aguado, Helm, Weidhase, & Bleidorn, ; Weidhase, Beckers, Bleidorn, & Aguado, ; Weidhase, Beckers, Bleidorn, & Aguado, ).…”

Musculature and innervation of the pygidium in Eunicida (Annelida: Errantia)

“…the other hand, in Magelona cf. mirabilis and Eurythoe complanata, belonging to the basally branching annelids, circular muscles in the pygidium were not found (Filippova, Purschke, Tzetlin and Müller, 2005;Weidhase, Bleidorn, Beckers and Helm, 2016). This may suggest that the circular pygidial muscle may either be a synapomorphy of Pleistoannelida, or it may be lost in studied basal branching species.…”