New data on echiuran anatomy and histology: the case of Lissomyema mellita (Annelida: Thalassematidae)
Graphical abstract
Introduction
Echiurans are unsegmented marine worms, which are now considered as annelids and as the sister group to the Capitellidae (Struck et al., 2015; Goto et al., 2020). The body of echiurans, which are commonly called spoon worms, is divided into a sausage-like trunk and a long, moveable proboscis; the proboscis rests on the surface of the substrate and is used to collect food particles. Echiurans are abundant in some habitat or locality; for example, thousands of specimens of Urechis unicinctus (Drasche, 1880) are offer become washed ashore after a storms in some shallow bays of the Sea of Japan, some species (e.g. Alomasoma nordpacificum Zenkevitch, 1958, Pseudoikedella achaeta (Zenkevitch, 1958)) are abundant in the deep sea (Zenkevitch, 1966; DattaGupta, 1981; Abe et al., 2014; Maiorova and Adrianov, 2018, 2020). All adult echiurans are benthic animals: some live in deep burrows in soft sediments, and others burrow into hard substrates (Ikeda, 1901, 1907; Ditadi, 1982). A specific faunal community usually develops in echiuran burrows (Fisher and MacGinitie, 1928; Ditadi, 1982; Stull et al., 1986; Nickell et al., 1986; Anker et al., 2005; Goto and Kato, 2012; Marin, 2014; Anker et al., 2015; Komai, 2015; Biseswar and Glynn, 2016; Goto, 2017; Goto et al., 2017; George and Schwabe, 2019; Marin and Antokhina, 2020).
There were two superfamilies of echiurans: Echiurioidea (with Echiuridae, Urechidae, and Thalassematidae) and Bonellioidea (with Bonelliidae and Ikedidae) (Goto, 2016). In the most recent classification in Goto et al. (2020), Thalassematidae is now the name for Echiura, a family-ranked clade within Annelida. Within the family there are two subfamilies: Thalassematinae, including two tribes Thalasematini and Echiurini, and Bonellinae.
Although echiurans are nearly globally distributed, from polar to equatorial seas, their anatomy and ultrastructure have been rarely studied by modern methods of electron microscopy, immunocytochemistry, and confocal laser scanning microscopy. It may be caused because echiurans live deep in the sediment and are therefore difficult to capture. Most researches concerning echiurans have been focused on commonly found species that thereby are well-studied within the group: Bonellia viridis Rolando, 1822, Thalassema thalassema (Palas, 1774), and Urechis caupo Fisher & MacGinitie, 1928 (Baltzer, 1917, 1931; Bock, 1942; Bartolomaeus, 1994; Lehrke and Bartolomaeus, 2011; Seitz, 1907; Harris and Jaccarini, 1981; Menon and Arp, 1992, 1993; Hessling, 2002, 2003; Hessling and Westheide, 2002). Information on the detailed anatomy, histology, and ultrastructure of echiuran organ systems is largely based on observations of B. viridis (Pilger, 1993). A recent study, however, indicated that the organization of organ systems may differ among echiurans, i.e., the organization of the digestive tract and blood system of at least one echiuran did not always correspond to that of B. viridis (Temereva et al., 2017).
Because 3D reconstruction allows researchers to reconstruct all organ systems in detail, its use should clarify the degree to which the organization of organ systems in Bonellia viridis is representative of organ system organization in other echiurans. The main aim of this paper was to use histology and 3D reconstruction to describe the morphology and anatomy of organ systems in Lissomyema mellita (Thalasematini).
Section snippets
Materials and methods
Seven specimens of Lissomyema mellita (Conn, 1886) were collected by A.S. Maiorova from dead coral in shallow water near Fort Pierce, Florida (USA). Whole animals were fixed with 4% formalin in seawater. After they were washed in 0.2 M phosphate buffer, the animals were kept in 70% ethanol.
The morphology of all individuals and the anatomy of two dissected individuals of Lyssomyema mellita were studied with a Leica MZ6 stereomicroscope (Leica Microsystems, Wetzlar, Germany). A series of
Morphology
The body of L. mellita consists of an oval or spherical sac-shaped trunk and a spatula-shaped proboscis; the proboscis arises at dorsal side of the anterior end of the trunk (Figs. 1A, B; 2 A). The lateral margins of the proboscis are curled, and the lips are not united at the base of the mouth (Figs. 1A, B; 2 B). The trunk surface is densely covered with papillae (Fig. 1A, B). The posterior end of the trunk is cylindrical and has a terminal anus (Figs. 1A, B; 2 A). A pair of golden hooked
Discussion
The morphology of Lissomyema mellita is typical for echiurans, i.e., the body is divided into a proboscis and trunk. Most echiurans are deposit-feeders, and the proboscis is used to collect food particles from the substrate (e.g., Ikeda, 1904; Baltzer, 1931; Hughes and Crisp, 1976; Biseswar, 1991; Hughes et al., 1993; Jumars et al., 2015; Kharlamenko et al., 2018). During burrowing, the initial penetration involves a repeated expansion and retraction of the proboscis (Biseswar, 1991). During
Conclusion
For the first time for echiurans, 3D reconstruction was used to visualize in detail the morphology and co-localization of all organs in L. mellita (Fig. 13D, E). The method revealed some anatomical features that have not been previously described for this species or for echiurans in general, including presence large glands in the posterior trunk that might aid in burrowing, the shortness of the foregut, and complex organization of blood vascular system. The combined use of 3D reconstruction,
Author contributions
PK performed the histology, prepared the serial sections, and made all 3D reconstructions, schemes, and photographs of sections. AM collected the animals, helped interpret the results, and helped write the manuscript. ET prepared all figures, wrote the manuscript, and interpreted the results.
Declaration of Competing Interest
The authors declare that they do not have any conflict of interest. All authors have read the text and approved the final version of the manuscript.
Acknowledgements
This study was conducted with financial support from the Russian Foundation for Basic Research (#20-04-00096). 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. The study was also supported by a Moscow State University Grant for Leading Scientific Schools "Depository of the Living Systems" within the MSU Development Program.
References (66)
- et al.
Swimming behavior of the spoon worm Urechis unicinctus (Annelida: Echiura)
Zoology
(2014) - et al.
A new species of Ectinosomatidae Sars (Copepoda, Harpacticoida) associated with Pseudoikedella achaeta (Zenkevitch, 1958) (Echiura, Bonelliida)
Prog. Oceanogr.
(2019) A comprehensive molecular phylogeny of spoon worms (Echiura, Annelida): Implications for morphological evolution, the origin of dwarf males, and habitat shifts
Mol. Phylogenet. Evol.
(2016)- et al.
Feeding and particle selection in the echiuran worm Bonellia viridis Rolando (Echiura: Bonelliidae)
J. Exp. Mar. Bio. Ecol.
(1977) - et al.
The evolution of annelids reveals two adaptive routes to the interstitial realm
Curr. Biol.
(2015) - et al.
Effects of Listriolobus pelodes (Echiura) on coastal shelf benthic communities and sediments modified by a major California wastewater discharge
Estuar. Coast. Shelf Sci.
(1986) - et al.
Structure and oxygen equilibrium of three coelomic cell hemoglobins of the genus Thalassema mellita
Comp. Biochem. Physiol.
(1987) Modelos de sistema vascular en Echiura
Asoc. Argentina Ciencias Nat. Physis, Buenos Aires
(1973)- et al.
A new echiuran-associated snapping shrimp (Crustacea: Decapoda: Alpheidae) from the Indo-West Pacific
Zootaxa
(2015) - et al.
Macrofauna associated with Echiuran burrows: A review with new observations of the innkeeper worm, Ochetostoma erythrogrammon Leuckart and Rüppel, in Venezuela
Zool. Stud.
(2005)
Echiuriden 1. Teil: Echiurus abyssalis Skor.
Fauna Und Flora Des Golfes von Neapel Und Der Angrenzenden Meeres-Abschnitte
Echiurida
On the ultrastructure of the coelomic lining in the Annelida
Microfauna Mar.
Burrowing, locomotion and other movements of the Echiuran Ochetostoma caudex
Acta Zool.
A new coral reef associated species of Echiura, Anelassorhynchus panamensis from the eastern Pacific Ocean
Proc. Biol. Soc. Washingt.
On the structure and affinities of “Thalassema” lankesteri Herdman and the classification of the group
Echiuroidea. Goteborgs. Vent. o. Vitterh. Samh. Handl. ser. B
Les cavidades de la trompa de Bonellia viridis (Rolando, 1821): revision anatomica y ultraestructural
Publicaciones del Dep. Zool. Univ. Barcelona
Sur un noveau type de symbiose chez la Bonellie (Bonellia viridis, Echiuridae). Compte Rendu Hebd. des Séances l’Académie des
Sci. Paris Ser. D
Atlantic Echiurans Part I. Report on twenty-two species of deep sea echiurans of the North and the South Atlantic Ocean
Bull. du Muséum Natl. d’histoire Nat. Sect. A, Zool. Biol. écologie Anim.
Classe des Echiuriens (Echiurida de Blainville, Gephyrea armata de Quatrefages, 1847)
On the burrows of echiuran worms (Echiura): a survey
Bol. Zool.
On the coelomic fluid of Lissomyema exilii (F. Muller, 1883) (Echiura)
Echiuroid worms of the north Pacific Ocean
Proc. United States Natl. Museum
A new echiuroid worm from California
Ann. Mag. Nat. Hist. (Series 10)
On the natural history and anatomy of Thalassema and Echiurus
Edinburgh New Philos. J.
The echiura of Japan: diversity, classification, phylogeny, and their associated fauna
The enigmatic bivalve genus Paramya (Myoidea: Myidae): Symbiotic association of an East Asian species with spoon worms (Echiura) and its transfer to the family Basterotiidae (Galeommatoidea)
J. Mar. Biol. Assoc. United Kingdom
Geographic mosaic of mutually exclusive dominance of obligate commensals in symbiotic communities associated with a burrowing echiuran worm
Mar. Biol.
Phylogeny of Echiura updated, with a revised taxonomy to reflect their placement in Annelida as sister group to Capitellidae
Invertebr. Syst.
Underwater observations of the giant spoon worm Ikeda taenioides (Annelida: Echiura: Ikedidae) in a subtidal soft-bottom environment in northeastern Japan, which survived tsunamis of the 2011 off the Pacific Coast of Tohoku Earthquake
J. Oceanogr.
Structure and function of the anal sacs of Bonellia virirdis (Echiura: Bonelliidae)
J. Mar. Biol. Assoc. United Kingdom
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
Metameric organisation of the nervous system in developmental stages of Urechis caupo (Echiura) and its phylogenetic implications
Zoomorphology
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