Histochemical evidence of β‐chitin in parapodial glandular organs and tubes of Spiophanes (Annelida, Sedentaria: Spionidae), and first studies on selected Annelida

Abstract

A generic character of the genus Spiophanes (Annelida, Sedentaria: Spionidae) is the presence of parapodial glandular organs. Parapodial glandular organs in Spiophanes species include secretory cells with cup-shaped microvilli, similar to those present in deep-sea inhabiting vestimentiferans and frenulate Siboglinidae. These cells are supposed to secrete β-chitin for tube-building. In this study, transverse histological and/or ultrathin sections of parapodial glandular organs and tubes of Spiophanes spp. as well as of Glandulospio orestes (Spionidae) and Owenia fusiformis (Oweniidae) were examined. Fluorescent markers together with confocal laser scanning microscopy, and Raman spectroscopy were used to detect chitin in the parapodial glandular organs of Spiophanes and/or in the glands of Owenia and Glandulospio. Tubes of these taxa were tested for chitin to elucidate the use of it for tube-building. The examinations revealed a distinct labelling of the gland contents. Raman spectroscopy documented the presence of β-chitin in both gland types of Spiophanes. The tubes of Spiophanes were found to have a grid-like structure that seems to be built with this β-chitin. Tests of tubes of Dipolydora quadrilobata (Spionidae) for chitin were negative. However, the results of our study provide strong evidence that Spiophanes species, O. fusiformis and probably also G. orestes produce chitin and supposedly use it for tube-building. This implies that the production of chitin and its use as a constituent part of tube-building is more widespread among polychaetes as yet known. The histochemical data presented in this study support previous assumptions inferring homology of parapodial glandular organs of Spionidae and Siboglinidae based on ultrastructure. Furthermore, transmission electron microscopy-based evidence of secretory cells with nail-headed microvilli in O. fusiformis suggests homology of parapodial grandular organs across annelids including Sipuncula.

Parapodial glandular organs in Owenia borealis (Annelida: Oweniidae) and their possible relationship with nephridia

“…The first two segments of O. borealis adults possess glands associated with parapodia, and these are called PGOs. In annelids, glands that secrete the material used for forming a tube can be associated with the protruding parts of the animals, and these are usually parapodia (if present) in nereidids (Daly, 1973; Dorsett & Hyde, 1970), onuphids (Budaeva & Fauchald, 2011), Phyllodoce mucosa (Prezant, 1980), and spionids (Guggolz et al, 2015; Hedley, 1956a, 1956b; Müller & Hylleberg, & Michalik, 2015), or are anterior collar structures or ventral shield in sabellids and serpulids (Kryvi, 1972; Mastrodonato et al, 2005; Meyer, 1893; Vovelle, Rusaouen‐Innocent, Grasset, & Truchet 1994). The so‐called tube‐secreting glands are located on the ventral side, as in onuphids, sabellids, Spio species, oweniids, and alvinellids; the ventrolateral side, as in nereidids and serpulids; the dorsal side, as in clitellates; or around the entire worm, as in siboglinids (Budaeva & Fauchald, 2010; Daly, 1973; Dorsett & Hyde, 1970; Hedley, 1956a, 1956b; Kryvi, 1972; Malakhov & Galkin, 1998; Karaseva, Malakhov, & Galkin 2012; Vovelle et al, 1994).…”

“…The tube‐secreting glands are often restricted to the anterior part of the animal, which is the part that can extend from the tube, as is the case for oweniids (Guggolz et al, 2015; Smart & Von Dassow, 2009; Watson, 1901), nereids (Daly, 1973; Dorsett & Hyde, 1970), sabellids (Kryvi, 1972; Mastrodonato et al, 2005; Vovelle et al, 1994), the serpulid Pomatoceros triqueter (Hedley, 1956a, 1956b), spionids (Guggolz et al, 2015; Müller et al, 2015), and the alvinellid Alvinella pompejna (Vovelle & Gaill, 1986). Also in clitellates, the clitellum is in the anterior end of clitelliates and contains glandular cells that secrete the cocoon‐like slimy tube, which is used for the copulation (Morris, 1985; Suzutani, 1977).…”

“…The glands have a lumen storing the secreted material. There could be muscle cells around the gland which are used to extrude material outside (e.g., Spiophanes , Owenia —see Guggolz et al [2015]; Siboglinidae—see Gardiner and Jones [1993]; Southward et al [2005]). Among the secretory glands, the complex subepidermal multicellular glands may be the most efficient because of the significant increase in the number of secreting cells.…”

“…In O. fusiformis , the cells of the proximal walls of the glands produce a chitinous material, and the distal portion of the glandular epithelium produces (and exudes?) a proteinaceous material (Gardiner, 1979; Guggolz et al, 2015). Overall, these reports are inconsistent concerning the number and location of nephridia‐like structures in oweniids.…”

Identification of fossil worm tubes from Phanerozoic hydrothermal vents and cold seeps

“…The latter composition most notably occurs in the tubes of siboglinids (Brunet & Carlisle 1958;Shillito et al 1995), which constitute the most prominent tubicolous annelid family occupying modern vents and seeps. Chitin content can vary throughout the length of siboglinid tubes (Julian et al 1999), and has also recently been detected in the tubes of spionids and oweniids (Guggolz et al 2015). Annelid builders of calcareous, agglutinated and organic tubes all occur at modern hydrothermal vents and cold seeps (Olu et al 1996;Desbruy eres et al 2006;Levin & Mendoza 2007;Kupriyanova et al 2010).…”