First record of Protomystides hatsushimaensis (Annelida: Phyllodocidae) inhabiting vacant tubes of vestimentiferan tubeworms

Abstract

Background

Vestimentiferan tubeworms (Annelida: Siboglinidae) often play an important role as a foundation species in chemosynthetic ecosystems by providing microhabitats for other organisms. In the present study, we detected a new relationship between phyllodocid worms and tubes of a vestimentiferan Alaysia sp.

Methods

Tubes of Alaysia sp. were collected from a hydrothermal vent field at a depth of 1052 m on the North Iheya Knoll in the Okinawa Trough on January 17, 2000. The Alaysia tubes were fixed with 4.7% neutralized formaldehyde solution and preserved in 70% ethyl alcohol. Phyllodocid worms were later obtained from empty tubes of Alaysia sp.

Results

We classified the collected phyllodocid worms as Protomystides hatsushimaensis based on the morphology of specialized chaetae. They were observed in thin brownish tubes of mucous, probably secreted by P. hatsushimaensis, at approximately 30 and 50 mm from the upper openings of the tubes of Alaysia sp.

Conclusions

The phyllodocid worm P. hatsushimaensis was found inside the tubes of Alaysia sp., a vestimentiferan tubeworm, collected in a hydrothermal vent field on the North Iheya Knoll in the Okinawa Trough of the western Pacific. The present study provides a new record of P. hatsushimaensis using empty vestimentiferan tubes as a microhabitat.

Background

Biological structures, such as annelid tubes, can affect community structuring by facilitating the recruitment of other benthic organisms (Gallagher et al., 1983; Reise, 1983; Trueblood, 1991; Zühlke et al., 1998; Callaway, 2006). Vestimentiferan tubeworms (Annelida: Siboglinidae) often play an important role in chemosynthetic ecosystems by providing microhabitats for other organisms (Govenar et al., 2005). Their chitinous tubes are used as substrata for colonization of sessile organisms, such as actiniarians (Desbruyères et al., 2006), barnacles (Tunnicliffe & Southward, 2004), bivalves (Järnegren et al., 2005), foraminiferans (Sen Gupta et al., 2007), limpets (McLean, 1993), polyps of jellyfishes (Miyake et al., 2004), sponges (Maldonado & Young, 1998), and stoloniferans (Becker et al., 2013). In addition, many organisms aggregate around the vestimentiferan tubes: annelids, cephalopods, zoarcid fishes, pantopods, and shrimps (Desbruyères et al., 2006). An experimental study of habitat provision by vestimentiferans has suggested that the structures made by vestimentiferans are not interchangeable with those made by other habitat-creating invertebrates, such as mussels, for some epifaunal species (Govenar & Fisher, 2007), suggesting a key role of vestimentiferans in generating microhabitats as a foundation species.

Some annelid species endemic to chemosynthetic ecosystems have been collected from the aggregations of vestimentiferans (Govenar et al., 2005; Govenar & Fisher, 2007; Tsurumi & Tunnicliffe, 2003; Govenar et al., 2004). Species of the family Phyllodocidae have also been recorded from the aggregations of vestimentiferans in the western and eastern Pacific (Desbruyères et al., 2006; Martin & Britayev, 1998): Eulalia papillosa (Blake, 1985); Garapagomystides aristata Blake, 1985; Protomystides hatsushimaensis Miura, 1988; Protomystides verenae Blake & Hilbig, 1990; and an unidentified species of the genus Protomystides inhabiting Gulf of Mexico (Becker, 2010).

Some phyllodocids have been suggested to feed on vestimentiferans (Jenkins et al., 2002), and they were found on the outer surface of vestimentiferan tubes. In contrast, Protomystides sp. was obtained from both the outside and inside of a dead tube of a vestimentiferan species (Becker, 2010), although it remains unclear whether this behavior is common or not among phyllodocids aggregating on vestimentiferans. Protomystides hatsushimaensis was discovered on the outer surface of a tube of Lamellibrachia sagami Kobayashi et al., 2015 in a cold seep area at a depth of 1140 m off Hatsushima Island. Later, additional specimens were obtained from bottom sediments sampled within Calyptogena beds with Nicomache (Loxochona) ohtai Miura, 1991 (Annelida: Maldanidae) from a site off Hatsushima (Fujikura et al., 2002). In the present study, we show a new record of P. hatsushimaensis in a hydrothermal vent field, which was obtained from the inside of empty tubes constructed by a vestimentiferan tubeworm, Alaysia sp.

Methods

Tubes of Alaysia sp. were collected from a hydrothermal vent field at a depth of 1052 m on the North Iheya Knoll in the Okinawa Trough (27°47.23′N, 126°54.26′E) using the human-occupied vehicle Shinkai 2000 during the NT00–08 cruise of the research vessel (R/V) Natsushima of the Japan Agency for Marine-Earth Science and Technology (JAMSTEC) on January 17, 2000 (Fig. 1). The Okinawa Trough is a representative back-arc basin with hydrothermal vent fields in the western Pacific (Fujikura et al., 2008). The Alaysia tubes were fixed with 4.7% neutralized formaldehyde solution and preserved in 70% ethyl alcohol without removing the vestimentiferans from the tubes. The gross morphology of the phyllodocid specimens obtained from the Alaysia tubes was observed under a stereomicroscope. The parapodium on the 11th chaetiger was cut for observation under a biological microscope. The phyllodocid specimens are available at JAMSTEC under JAMSTEC No. 2000044404 in the Marine Biological Sample Database (samples available only in Japan).

Fig. 1

Distribution of Protomystides hatsushimaensis. The open star indicates the type locality, a cold seep area at a site off Hatsushima, Sagami Bay (Miura 1988); the closed star indicates the location of the new record, a hydrothermal vent field on the North Iheya Knoll in the Okinawa Trough

Results

Two phyllodocids were obtained from the inside of 2 of over 30 empty tubes of an Alaysia sp., by dissecting the tubes in 2014. They were observed in thin brownish tubes of mucous, probably secreted by phyllodocids, at approximately 30 and 50 mm from the upper openings of the tubes of Alaysia sp. (Fig. 2c).

Fig. 2

Protomystides hatsushimaensis. Dorsal view, scale bar = 500 μm (a); ventral view, scale bar = 500 μm (b); P. hatsushimaensis in the tube of a vestimentiferan tubeworm: the arrow indicates the prostomium, and the arrowhead indicates the pygidium of P. hatsushimaensis (c), probably a single broken individual). The asterisk indicates a mucous tube of P. hatsushimaensis

We classified the phyllodocids as P. hatsushimaensis (Fig. 2a, b) based on the morphology of the specialized chaetae. Among congeneric species, only P. hatsushimaensis and P. verenae have very short, aristate-like blades of compound spinigers (Miura, 1988; Blake & Hilbig, 1990). P. hatsushimaensis and P. verenae were distinguished by the shape of their parapodia, having a single type of spinigers in the former and two types in the latter (Blake & Hilbig, 1990). The trapezoidal shape of the prostomium slightly differed from the original description (hexagonal prostomium) probably because of a variation in the degree of modifications when they were fixed in the tubes.

Discussion

Some studies have suggested that certain species of phyllodocids feed on vestimentiferans. For example, the blood feeding of G. aristata on Riftia pachyptila Jones, 1981 has been suggested at the 9°N vent site on the East Pacific Rise (Jenkins et al., 2002). However, it was suggested that P. hatsushimaensis utilizes tubes as a habitat because the worms were collected from vacant vestimentiferan tubes. The behavior of occupying tubes constructed by other species appears to be uncommon among annelids, as well as benthic organisms. Indeed, no other organisms were obtained from the inside of more than 30 tubes of Alaysia sp., although at least five epifaunal annelid species inhabit vent fields on the North Iheya Knoll (Yamamoto et al., 1999). Protomystides sp. in the eastern Pacific has been reported from the dead tubes of the vestimentiferan Escarpia laminata Jones, 1985 (Becker, 2010); therefore, our observation suggests that this occupying behavior may be common among species of Protomystides.

Annelid tubes provide small annelids with shelters from predators, waves, and thermal or chemical extremes (Zbinden et al., 2003; Stewart et al., 2004; Vinn & Kupriyanova, 2011). Tube production, however, can be the largest energy expenditure of such organisms: tube production energy expenditure exceeds that for somatic growth and gamete production in serpulid species (Dixon, 1980). Thus, the occupying behavior of P. hatsushimaensis may be advantageous in saving the production energy cost for hard tubes. Physiological and ecological characteristics would provide further insights into the benefits of the occupying behavior of P. hatsushimaensis.

Conclusions

Tubes of vestimentiferans provide habitats for other organisms (Desbruyères et al., 2006). This new record of P. hatsushimaensis using vestimentiferan tubes as a microhabitat provides a new association between phyllodocids and vestimentiferans. This is also the first record of P. hatsushimaensis from a hydrothermal vent, providing one of relatively few examples of species inhabiting both seep and vent sites.