Serpula and Spiraserpula (Polychaeta, Serpulidae) from the Tropical Western Atlantic and Gulf of Guinea

Abstract Six species of Serpula and Spiraserpula were identified, mainly, from the material of the expeditions of the Rosenstiel School of Marine and Atmospheric Science, University of Miami, including two new species of Serpula. Serpula madrigalae sp. n. from the Turks and Caicos has a tube with five longitudinal ridges, four rows of alveoli and a medium-sized shallow symmetrical opercular funnel with 17 radii, and an inner surface with opercular tubercles. Serpula vossae sp. n. from the Western Caribbean and Bahamas has a tube with 6–8 longitudinal ridges, and a large, deep symmetrical opercular funnel, with 21–33 radii, and a smooth inner surface. Serpula cf. vermicularis, recorded from the Gulf of Guinea (tropical eastern Atlantic), is distinguished from the nominal species in possessing fewer opercular radii (33–39) and the lack of a proximal rasp in the bayonet chaetae; tubes are missing. The distribution range is extended for the three known Spiraserpula species found in the collections, Spiraserpula caribensis, Spiraserpula karpatensis and Spiraserpula ypsilon.

introduction Serpula Linnaeus, 1758 the type genus of the polychaete family Serpulidae Rafinesque, 1815, has 31 species (ten Hove and Kupriyanova 2009, Pillai 2009). Six species have been described in the Eastern Atlantic and Mediterranean, including the type species, S. vermicularis Linnaeus, 1767, S. concharum Langerhans, 1880, S. lobiancoi Rioja, 1917, S. planorbis Southward, 1963, S. israelitica Amoureux, 1976and S. cavernicola Fassari & Mòllica, 1991. However, there are taxonomic problems in some species because they were poorly described and/or recorded from widely separated localities. For example, S. vermicularis has been recorded from several tropical, subtropical, temperate and cold water localities of the world (Kupriyanova 1999). There is a consensus now that S. vermicularis, previously considered to be a cosmopolitan species, is ill-defined and its distribution is possibly restricted to temperate and cold waters of the North Atlantic Ocean and Mediterranean (ten Hove and Jansen-Jacobs 1984, Imajima and ten Hove 1984, Kupriyanova and Jirkov 1997, Kupriyanova 1999, ten Hove and Kupriyanova 2009).
In the Western Atlantic, the genus Serpula is very poorly known, as only two species have been recorded: S. vermicularis granulosa by Day (1973) from Beaufort, North Carolina, and Serpula sp. A by ten Hove and Wolf (1984) from the northeastern Gulf of Mexico. Another taxon, S. sombreriana McIntosh, 1885, from Sombrero and St. Thomas Islands, lacks an operculum and was therefore transferred to Hyalopomatus (Ben-Eliahu and Fiege 1996).
The current state of our knowledge on Serpula species, compared to that of almost 100 species of Hydroides (ten Hove and Kupriyanova 2009, Pillai 2009), is probably explained by the fact that most tropical Serpula species are sublittoral and many extend their distribution into deeper waters. In cold and temperate waters, Serpula species can be present in shallow waters, attain larger sizes (Kupriyanova 1999), and form large aggregations, even reefs (Ramos and San Martin 1999).
Spiraserpula Regenhardt, 1961 was established initially for fossil serpulids. Pillai and ten Hove (1994) revised the Recent species belonging to the genus. They described 16 species out of 19 currently included in the genus, and eight of them were from the Caribbean. The main distinguishing feature of this genus is their complex internal tube structures (ITS), described by Pillai and ten Hove (1994). Unfortunately, the species remain mostly unknown to non-specialists, mainly because they are tiny, most are sublittoral, and often overlooked or confused with other taxa.
This work is part of a larger study examining subtidal and deep sea serpulids from the Grand Caribbean region and from the Gulf of Guinea, tropical eastern Atlantic.

Materials and methods
Between 1963 and 1975, the Rosenstiel School of Marine and Atmospheric Science (RSMAS) conducted the University of Miami Deep Sea Expeditions aboard of R/V Gerda, John Elliot Pillsbury, James M. Gillis and Columbus Iselin, and sampled more than 3,350 stations from the Gulf of Panama, throughout the Caribbean to the Gulf of Guinea, the Straits of Florida, the Bahamas, the area northward to the Bermudas and the deep basins and the deep waters, from the intertidal to 8,650 m in the Puerto Rico Trench (Voss et al. 1977, Bastida-Zavala et al. 2001. The revision of the serpulid material from these expeditions resulted in finding of 11 Serpula and 10 Spiraserpula specimens from the western Caribbean, Bahamas, Turks and Caicos, Los Roques Islands, Trinidad and Tobago, and in the Gulf of Guinea. Additionally, two specimens of Serpula (recorded by Bastida-Zavala and Salazar-Vallejo 2000) and 14 specimens of Spiraserpula of the collections of El Colegio de la Frontera Sur and the Instituto de Oceanología of Cuba were available for study. Type specimens were deposited in the National Museum of Natural History, Smithsonian Institution, Washington, D.C. Other specimens were deposited in the collections of the respective lending institutions.
The specimens of Serpula and Spiraserpula were fixed with 10% formalin and preserved with 70% alcohol. They were studied in a standardized way (ten Hove and Jansen-Jacobs 1984, Bastida-Zavala and ten Hove 2002). Line drawings were made using a camera lucida, and the photographs were taken with a digital camera Canon G11 fitted to a microscope adapter.
The main standard measurements and observations on Serpula were: total length (measured from most distal part of the operculum to the pygidium), thoracic width (measured from the collar region level), number of thoracic chaetigers, number of radioles in each lobe of the branchial crown, number of longitudinal ridges on the tube (not counting basal ridges attached to the substratum), presence or absence of peristomes, transverse ridges or alveoli on the tube, opercular length (measured from the base of funnel, or constriction, if present, to the tips of the radii), opercular diameter (measured across the distal part of the funnel), number of funnel radii, number of teeth on bayonet chaetae and the presence or absence of a proximal rasp in these chaetae. An exploratory analysis of the number of opercular radii and body length ratio of the Serpula species is included. Scales of figures and photographs are in millimeters. Serpula madrigalae sp. n. resembles S. vermicularis granulosa, in having tubercles on the internal surface of the operculum; however, the diagnosis of the latter species  was brief (Day 1973). At least S. madrigalae sp. n. differs by the tube with five longitudinal ridges and four rows of alveoli (Figs 1C-D, 2A-B), while S. vermicularis granulosa is "faintly ridged" (Day 1973:131); also, Day (1973) mentioned more opercular radii (20-40) than present in Serpula madrigalae sp. n. (17,Figs 1B,5).
Serpula madrigalae sp. n. also resembles Serpula sp. A, from the northeastern part of the Gulf of Mexico, with regard to the shape of the operculum, the number of radii and the depths from which they were collected. However, they differ with regards to other features: S. madrigalae sp. n. has irregular tubercles on the internal surface of the operculum (Figs 1B, 2D) and lacks a proximal rasp in the bayonet chaetae ( Fig.  2F), while Serpula sp. A lacks tubercles (ten Hove and Wolf 1984, Fig. 55-8a) and has bayonet chaetae with a proximal rasp. Additionally, ten Hove and Wolf (1984) mentioned that all the specimens lacked their tubes. Hence is not possible to assign the specimens recorded as Serpula sp. A. to S. madrigalae sp. n. Description. Tube color brownish, or light brown to white; with 6-8 longitudinal ridges, all similar in size; some tubes with shallow transverse ridges, forming a rugged surface, other tubes lacking transverse ridges; most tubes lacking peristomes, two have only one peristome with appearance of a groove with shallow growth lines. Tubes lacking alveoli ( Fig. 4A, C-D).
Collar thick, with short ventral and dorsal lobes. Thorax consists of seven chaetigers. Collar fascicles in three specimens asymmetrical with regard to sizes and number of chaetae; right fascicle with larger and more chaetae than left fascicle (Fig. 4E). Bayonet chaetae with two blunt-elongate teeth, distal blade smooth, lacking proximal rasp (Fig. 4G); hooded (capillary) chaetae present.
Anterior part of abdomen lacks a distinct achaetous region. Anterior and middle abdominal chaetigers with flat-trumpet chaetae. Posterior chaetigers with 'capillary' chaetae. Anterior and posterior uncini saw-shaped.
Etymology. Named after Professor Nancy Voss, a distinguished cephalopod specialist and Director of the Marine Invertebrate Museum, who generously loaned the serpulid samples from the oceanographic expeditions of the University of Miami.
Reproductive characters. The specimen from Cayo Diego Pérez, Cuba, has eggs adhering to the pinnules of the radioles. The eggs, circular to slightly oval, are 55-68 µm (Fig. 4F).

Serpula cf. vermicularis
Peduncle smooth, with insertion on left (n=2) or right (n=2); lacking constriction between it and operculum, its position represented only by a slight change in color (Figs 1E, 2I). Club-shaped pseudoperculum present in all specimens.
Collar thick, with ventral and dorsal lobes short. Thorax consists of seven chaetigers. Collar chaetal fascicles symmetrical with regard to size and composition unlike in S. vossae sp. n. Bayonet chaetae with two blunt-elongate teeth, distal blade smooth, lacking proximal rasp (Fig. 2J); hooded (capillary) chaetae present.
Distribution. Nigeria, Gulf of Guinea (Fig. 6). Ecology. Sublittoral, 33 m. Remarks. Serpula cf. vermicularis resembles the nominal species; unfortunately, the tubes of all the specimens are missing. There are some differences with the nominal species, particularly with regard to the number of radii: Serpula cf. vermicularis has 33-39 opercular radii (Fig. 1F, 2I, 5), while Zibrowius (1968) recorded specimens from Marseille with more than 40 opercular radii, and Kupriyanova and Jirkov (1997) recorded specimens from Norway and Iceland with a mean of 50.8 opercular radii; and the proximal rasp of the bayonet chaetae: Serpula cf. vermicularis lacks a proximal rasp (Fig. 2J), while Rioja (1931) and Kupriyanova (1999, Table 1) mentioned that their specimens have a proximal rasp. Zibrowius (1973) recorded several specimens as S. vermicularis, from Western Africa (from Angola to Morocco); unfortunately the description was too brief and did not included figures; however, Zibrowius (1973) mentioned that the specimens that he reviewed showed considerable variation. Description. Some specimens forming tube aggregations; others were found isolated. Tubes sinuous or spiraled (Fig. 7A), with two internal ridges: mid-dorsal one smooth, mid-ventral one serrated (Fig. 7B-C), occasionally with two internal lateral ridges (Fig. 7D). Some tubes externally pinkish, others with two dorsal pink bands ( Fig. 7A-B). Body brown to dark brown (preserved material only). The worms are damaged. Branchial crowns lost. Thorax with eight chaetigers, including collar fascicles. Abdomen damaged.

Genus
Distribution. Caribbean, Florida and Pacific of Panama. Ecology. Intertidal to sublittoral, 10 m. On coral debris. Pillai and ten Hove (1994) recorded the species from 0-18 m deep.
Remarks. Spiraserpula caribensis is easily distinguishable from the other Caribbean species by their pink tubes (Fig. 7A).  Description. Empty tube larger (Fig. 7E) than occupied one attached to empty tubes of S. ypsilon. Tubes sinuous or spiraled, with two internal ridges: mid-dorsal one smooth, mid-ventral one serrated (Fig. 7E). Both tubes white, internal and externally (Fig. 7E). The branchial crown and thorax of incomplete specimen is missing. Abdomen partially transparent, with double packets of gametes in each segment (Fig. 7F).

Spiraserpula karpatensis
Distribution. Eastern Caribbean. Bonaire, Curaçao and Los Roques Islands. Ecology. Sublittoral, 65 m. On coral debris. Pillai and ten Hove (1994) recorded the species from depths of 10-30 m. The sample also contained two Spiraserpula species: S. ypsilon and Spiraserpula sp., a chaetopterid tube, a lumbrinerid and several empty tubes of serpulids resembling Protula and Vermiliopsis.

Spiraserpula ypsilon
Distribution. Caribbean, Florida and Pacific of Panama.
Remarks. Spiraserpula ypsilon is very similar to S. paraypsilon Pillai & ten Hove, 1994, described from the Netherlands Antilles, mainly with regard to the internal ridges of the tube. However, some differences separate both species, mainly the absence of lateral tubercles in the thoracic uncini in S. ypsilon, characteristic of S. paraypsilon; additionally, S. ypsilon has fewer radioles (6-7) than S. paraypsilon (11). Description. Tube attached to a chaetopterid tube, is white and lacks any internal ridges characteristic of Spiraserpula. External surface with granular appearance, internally smooth. Body white, fragmented and damaged but complete. Branchial crown with nine radioles per lobe; lacking inter-radiolar membrane.
Remarks. Most of the tube belonging to this specimen is missing and the remaining fragments lacked the internal ridges characteristic of Spiraserpula. The operculum of this Spiraserpula sp. resembles that of S. karpatensis, S. plaiae Pillai &ten Hove, 1994 andS. sumbensis Pillai &ten Hove, 1994; the former two are from Caribbean and the latter is from Indonesia. Due to the loss of the rest of the tube the present specimen cannot be assigned to species. It may be a juvenile stage of another genus, such as Crucigera or Serpula.

Discussion
Despite having reviewed 158 lots of serpulids from the same number of stations collected during past deep sea expeditions, specimens of Serpula were found only at six stations (3.8%), which combined with the fact that there were only two previous records of Serpula (Day 1973, ten Hove andWolf 1984) from the U.S. Atlantic, indicates that the genus is very rare in the Western Atlantic.
However, the original descriptions of the species mentioned in the remarks, indicate that many are incomplete, unclear or contradictory with respect to the figures provided. Descriptions need to be standardized and include as many characters as possible, as argued extensively by ten Hove and Jansen-Jacobs (1984), Kupriyanova (1999), and ten Hove and Kupriyanova (2009).
As regards Spiraserpula, another little-known serpulid genus in the Caribbean closely similar to Serpula, complete descriptions of species were made in an important and recent revision of the genus, including most species from the Caribbean (Pillai and ten Hove 1994). Unfortunately, due to the characteristics of the internal tube structures and small size of the specimens, their manipulation and study of Spiraserpula is more difficult as compared to other serpulids.