Elsevier

Zoology

Volume 144, February 2021, 125865
Zoology

New data on echiuran anatomy and histology: the case of Lissomyema mellita (Annelida: Thalassematidae)

https://doi.org/10.1016/j.zool.2020.125865Get rights and content

Highlights

  • 3D reconstructions of all organ systems are obtained for an echiuran for the first time.

  • Unusual gland cells are found in the proboscis and the trunk of Lissomyema mellita.

  • Circulatory system of Lissomyema mellita exhibits incomparable anatomical complexity.

  • Morpho-functional analysis of new data provides insights into echiuran biology.

  • 3D reconstructions revealed the great plasticity of echiuran anatomy.

Abstract

Echiura is small group of unsegmented marine worms that are sometimes abundant in the benthos of all areas of the World Ocean. The study of echiuran morphology and anatomy is important for understanding echiuran biology and the function of benthic communities where echiurans dominate. The current study used paraffin histology, scanning electron microscopy, and 3D reconstruction to describe the anatomy of organ systems in Lissomyema mellita, which is within the tribe Thalassematini of the subfamily Thalassematinae. The body of L. mellita consists of a trunk and a proboscis. The trunk terminates at the anal lobe, which contains many large glands, the secretions of which may be used for processing of the hard substratum where studied animals were found. The proboscis has lateral ciliated grooves that are < 7 μm wide and are probably used for collecting and separating food particles. The coelom is divided into the coelom of the proboscis and the coelom of trunk. The location of proboscis coelom may suggest that the proboscis is derived from the oral segment of the body of a hypothetical segmented echiuran ancestor. The shortness and histological uniformity of the foregut indicates that L. mellita feeds on soft food particles that do not require mechanical processing. The circulatory system has a complex organization and contains several vascular elements that have not been previously described in echiurans: voluminous plexus around the foregut, voluminous dorsal and ventral lacunes, and additional vessels between neurointestinal and circular blood vessels. The dorsal blood vessel is very short; the circumchaetael vessel is absent. Most of the anatomical peculiarities of L. mellita appear to be related to its biology. The newness of the data on the organization of the circulatory system reflects the general scarcity of knowledge on echiuran anatomy. The newly discovered features should be incorporated into general schemes of echiuran organization.

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.

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