Notaulax yamasui sp. n. (Annelida, Sabellidae) from Okinawa and Ogasawara, Japan, with notes on its ecology

Abstract The polychaete Notaulax yamasui sp. n. (Sabellidae) is described from Okinawa and Ogasawara, south Japan, where it was found living embedded in a dead skeleton of the coral Porites sp. The new species is characterized by the presence of a pigmented sub-distal swelling on the tips of the crown radioles, a unique feature among species of the genus. Besides, its collar chaetae have an L-shape orientation, and the dorsal basal flanges of the branchial lobes are long and have a dorsal joint.


Introduction
A revision of the Japanese sabellid polychaetes belonging to the genera Megalomma Johansson, 1925, Notaulax Tauber, 1879, Parasabella Bush, 1905and Sabella Linnaeus, 1767, is in progress. In the course of this revision, several Japanese collections are being revised for specimens belonging to these genera. As a result, two specimens belonging to the same species showed radioles with sub-distal swellings, like those found in Sabella discifera Grube, 1874 andin Bispira brunnea (Treadwell, 1917), as reported by Tovar-Hernández and Pineda-Vera (2008). These swellings can be pigmented, in which case they superficially resemble the compound eyes of Megalomma and Stylomma Knight- Jones, 1997. Other main features of the specimens include the long flanged radiolar lobes (similar to those in Notaulax, Stylomma, and Anamobaea Krøyer, 1856), and simple radiolar eyes (like those in Notaulax, Anamobaea, and Hypsicomus Grube, 1870). All these genera were revised or described by Rullier and Amoureux (1970), Perkins (1984), Knight-Jones (1997), Knight-Jones and Perkins (1998), Fitzhugh (2002) and Capa (2007). Further information on these genera can also be found in Fitzhugh (1989Fitzhugh ( , 2003 and Capa et al. (2014).
The specimens collected at Okinawa and Ogasawara (south-western Japan) were studied using both light and scanning electron microscopy (SEM) for their external morphology, and through histological cross sections at different levels of the radioles for the internal anatomy of the radioles and their sub-distal swellings. As a result, the specimens were determined to belong to an unknown species of Notaulax, which is described below as a new taxon.

Material and methods
The specimens were collected together with the surrounding coral at shallow water by hand, using chisels to break pieces of the coral, and fixed in the laboratory with a 10% seawater-buffered formalin solution. Some parapodia were removed from the body and prepared for microscopy observations. For light microscopy observations the parapodia were placed on a microscope slide, covered with a cover slip, and gentle pressure was applied in order to observe the chaetae and uncini. Histological sections were made from radioles embedded in paraffin, cut on a microtome, and stained with Sudan Black B. For SEM observations, the parapodia were run through a series of increasing concentrations of ethanol (80, 90, 95, 99 and 100%), air-dried, coated with palladium and platinum, and viewed in a Hitachi S-800 SEM. The holotype and paratype were deposited in the Coastal Branch of Natural History Museum and Institute, Chiba at Katsuura, Chiba, Japan (catalogue code, CMNH-ZW). The terminology for the anatomical structures of Notaulax follows Fitzhugh (1989Fitzhugh ( , 2002.
Diagnosis. Pigmented sub-distal swelling on tips of crown radioles; collar chaetal row in L-shape orientation; dorsal basal flanges of radiolar lobes long and with a dorsal joint.
Description. Tube dark brown, thin and membranous. Body and radiolar crown pale in preserved specimens, except for light brown collar and for two (upper and lower) brown bands on distal free region of radioles (Fig. 1A, E).
Habitat. Notaulax yamasui sp. n. is known to live in the subtidal zone, embedded in dead coral masses of Porites sp.
Etymology. The new species is named after Dr. Terufumi Yamasu, Emeritus Professor of the University of the Ryukyus, Japan, for his great contribution to the development of the Okinawan marine biology.

Systematics
Under the stereo-microscope the radiolar sub-distal swellings of Notaulax yamasui sp. n., pigmented in the holotype, superficially resemble the typical radiolar compound eyes of the genera Megalomma and Stylomma, while other characters are typical of other sabellid genera lacking such eyes: the linear collar chaetae fascicles of Notaulax, Panousea Rullier andAmoureux, 1970, or Panoumethus Fitzhugh, 2002; the loosely aligned simple radiolar eyes of Hypsicomus, Notaulax, and Anamobaea; the long radiolar lobes of Stylomma, Notaulax, and Anamobaea. From these, Panousea and Panoumethus were ruled out from the beginning due to the presence of thoracic acicular uncini.
The fan-worm eyes and other photoreceptors are summarized in  and . The compound eyes of Stylomma are stalked, which occurs neither in Megalomma, nor in the swellings of N. yamasui sp. n. The radiolar sub-distal swellings of the specimens of N. yamasui sp. n. were compared with the compound eyes of an unidentified Megalomma specimen collected at Katsuura, Chiba (Honshu, Japan). Scanning electron micrographs of Megalomma sp. eyes showed a surface structure analogous to the insect compound eyes, with many individual lenses arranged in a geometrical array (Fig. 4C, D). This does not occur in the sub-distal radiolar swellings of N. yamasui sp. n., where the surface of the swellings does not show any kind of special array (Fig. 4A). Moreover, while the former eyes have clearly defined edges, the latter have diffused edges around the swelling.
The internal morphology of both structures in Megalomma sp. and N. yamasui sp. n. compared through histological cross-sections showed ultrastructural differences: Megalomma sp. presents lenticular photoreceptor units (Fig. 5G), while the swellings of N. yamasui sp. n. are structurally similar to other regions of the radioles (Fig. 5B-E). These differences show that the new species lacks the compound eyes typical of Megalomma or Stylomma.
The remaining three genera (Notaulax, Anamobaea, and Hypsicomus) belong to a well-defined group inside the Sabellidae (Fitzhugh 1989: Clade IV in fig. 28; Nogueira et al. 2010: clade in figs 18-20, 22). These three genera share a number of features, including the presence of scattered simple radiolar eyes along the lateral margins of the radioles (Fig. 1E, F). However, Hypsicomus and Anamobaea can be easily separated from Notaulax and the new species by having the collar chaetae arranged in a bundle, instead of a long row. Besides, the spine-like shape of the superior thoracic notochaetae of the new species is typical of Notaulax, while in both Hypsicomus and Anamobaea thoracic notochaetae are elongated and narrowly hooded.
Finally, other characters typical for the genus Notaulax and also present in the new species, such as long flanged radiolar lobes, gave further support to its identification as a member of the genus. The genera Hypsicomus and Notaulax were partially revised by Perkins (1984) who, after examining the type species of Hypsicomus, the Adriatic H. stichophthalmos (Grube, 1863), redefined the genus and transferred to Notaulax all but the type species previously included in Hypsicomus. This means that the literature records of coral-boring Hypsicomus phaeotaenia sensu lato or Hypsicomus ssp. would be referable to Notaulax species (see below).
Among the members of the genus Notaulax (see Perkins 1984, Capa andMurray 2015), N. yamasui sp. n. is unique in having radiolar sub-distal swellings and L-shaped distributed collar chaetae. Another remarkable character of Notaulax yamasui sp. n. is the structure of the dorsal basal flange, which is rounded and long (Fig. 1A, D), with bases closed dorsally by a dorsal joint (Fig. 1P). A similar structure was reported in Stylomma palmatum (Quatrefages, 1866) by Capa (2008). In Japanese waters, the only recorded Notaulax species is N. lyra (Moore and Bush, 1904). Notaulax yamasui sp. n. is differentiated from N. lyra by the presence of radiolar subdistal swellings, a much longer inter-radiolar membrane which is about half the length of the radioles (Fig. 1A), and the color pattern of radioles (two or three brown bands in the former species, and reddish brown eyes pots occupying the basal three-tenth of radiole in the latter species) (Imajima and Hartman 1964).
The entire posterior peristomial ring collar is also an uncommon feature among Notaulax species, being described only in two other species: Notaulax pyrrhogaster (Grube, 1878) from Philippine Islands, and N. alticollis (Grube, 1868) from the Red Sea. Like in these two species, N. yamasui sp. n. also shows the ventral margin of the collar more or less extended forward, forming a triangular lobe. However, neither of those two species has radiolar distal swellings, nor the collar chaetae in an L-shaped arrangement. Besides, N. pyrrhogaster does not show simple radiolar eyes (likely not faded by alcohol, as according to Wiktor (1980), the syntype has been preserved in formalin), and N. alticollis has the group of radiolar eyes positioned along two rows with less than 15 eyes in each, corresponding to about 7 pinnules in length. Notaulax yamasui sp. n. has the radiolar eyes in a group corresponding to about 11-12 pinnules in length, with 8-12 eyes in a single row. Capa and Murray (2015) recorded Notaulax sp., having radiolar eyes (noted as radiolar ocelli) arranged in a single row or in teardrop-shaped groups. Other types of radiolar eyes and further details about their structure can be found in .

Ecology of Notaulax
The two types of Notaulax yamasui sp. n. were found living embedded in dead masses of coral Porites sp. Boring by worms in coral reefs is a common and very well-known phenomenon described as early as in 1902 by Gardiner (1902), and recently revised by Hutchings (2008). With the prevalent predation pressures at shallow coral reefs being high, the advantage of burrowing for protection into hard surfaces such as corals seems obvious, with positions submitted to currents and vertical surfaces being particularly favored by filter feeders to maximize feeding benefits and avoid sedimentation (Elias 1986, Hutchings 1986. Normally worms only bore into dead corals, or in the dead edges of living corals, avoiding contact with the soft parts. The recruitment by the worms is believed to be entirely via larvae or juveniles settling on the surface; as coral polyps are carnivores, the successful recruitment and subsequent boring is restricted mainly to the coral areas where polyps are damaged or very scarce Murray 1982, Hutchings 2008).
Boring by worms plays an important role in the bio-erosion of coral reefs, but much less so than grazing by echinoids and fish, with boring polychaete species belonging to several families (the most important being Eunicidae, Lumbrineridae, Dorvilleidae, Oenonidae, Spionidae, Cirratulidae, and Sabellidae) and also Sipuncula (Warme 1975, Hutchings 1986, Hutchings and Peyrot-Clausade 2002, Hutchings 2008. Boring mechanisms in polychaetes can include mechanical (Eunicida) or chemical methods (Spionidae, Sabellidae, and probably Cirratulidae) (Hutchings 2008), and normally tubes or holes made by boring organisms can be recognized by their nearly constant diameter, as they are bored continuously to accommodate the growth of the host corals (Nishi and Nishihira 1999).
Similarly, larvae of Notaulax species settle on dead corals, probably benefiting from the rugose surface for protection, while burrowing holes into the dead coral mass. A transverse section of a Notaulax sp. burrow in a Porites sp. coral is represented in Nishi and Nishihira (1999).
The latitudinal distribution of Notaulax fits almost perfectly the global carbonate production, especially as aragonite (Buddemeier 1997: fig. 1;Wood 2001: fig. 1), and by extension, the location of the scleractinian coral reefs (composed mainly by aragonite), also up to about 30°N and S, beyond which coral reefs are usually absent. Notaulax species seem to be typically borers, mainly in corals, but also in other carbonate (apparently mainly in aragonite) substrates. Besides the above cited species, references to Notaulax specimens as coral borers are frequent in the literature on coral reef polychaetes, especially as unidentified Hypsicomus species (e.g., Hartman 1954, Marsden 1960, Peyrot-Clausade et al. 1992, Nishi 1997, Hutchings and Peyrot-Clausade 2002, as H. elegans (see Gibbs 1969), H. phaeotaenia (see Hutchings et al. 1992), or as Notaulax sp. Nishihira 1999, Capa andMurray 2015).
Dr. María Ana Tovar-Hernández and an anonymous reviewer for their criticism and suggestions of useful references that significantly improved the contents and the format of our paper.