First record of the polychaete Ficopomatus uschakovi (Pillai, 1960) (Annelida, Serpulidae) in the Colombian Caribbean, South America

Abstract The genus Ficopomatus (Serpulidae) consists of sessile, tubicolous polychaete annelid worms that may colonize a diversity of substrata, and tolerate considerable variations in salinity. Thus, members of this genus, including Ficopomatus uschakovi, in some cases are exotic and maybe invasive. The purpose of our research was to collect and identify marine organisms associated with the submerged roots of mangrove trees in the Gulf of Urabá, Colombian Caribbean, South America. Within the Gulf, there is a well-developed forest of the Red Mangrove, Rhizophora mangle, along the margins of El Uno Bay. We sampled the roots of R. mangle from five stations of the bay, and we identified specimens of F. uschakovi from each of those stations. Ficopomatus uschakovi was found to be more abundant in regions of the bay that exhibit the lowest salinity. Based on a morphological comparison of the present specimens with the original species description, revised descriptions, and other records from the Indo-West Pacific, Mexican Pacific, and Venezuelan and Brazilian Caribbean, we suggest that F. uschakovi has a broader geographical distribution. Furthermore, because of this broad distribution, and the observed tolerance for low salinity in our study, we also suggest that F. uschakovi is a euryhaline species. It is also likely that F. uschakovi will be found in other localities in the Gulf of Urabá, and in other regions of the Colombian Caribbean. Thus, this record extends the distribution of the species to the Colombian Caribbean, giving the species a continuous distribution across the northern coast of South America.


Introduction
The family Serpulidae Rafinesque, 1815, includes a group of sedentary polychaetes that are easily recognizable by their calcareous tubes, with irregularly twisted or spiral growth, and by the complexity of their radiolar crown (Rouse and Pleijel 2001).However, other features, such as the shape of the operculum, the branchial crown, the form, type and position of chaetae along the collar, the thoracic membranes, as well as the thorax and abdomen, represent important taxonomic characters (Hove and Kupriyanova 2009).Some serpulids are solitary, but others such as Hydroides (Bastida-Zavala and Hove 2003), are gregarious, living in large groups or colonies that may cover the hard substrates of coral reefs, coastal lagoons, and the estuarine or brackish environments of tidal canals within mangrove forests (Bastida-Zavala and Salazar-Vallejo 2000).They are benthic, sessile organisms, and their tubes have been found attached to rocks, roots, wood, mollusc shells, dock structures, and boat hulls that facilitates their dispersal (Salgado-Barragán et al. 2004); few species have free tubes, unattached to any substratum, but living on a sandy bottom.
Ficopomatus uschakovi was described from Sri Lanka (Pillai 1960), and is widely distributed across the Indo-West Pacific (Hove and Weerdenburg 1978).It has been recorded in other regions, including the Mexican Pacific (Bastida-Zavala and García-Madrigal 2012), the Western Atlantic, in Paraiba, Brazil (de Assis et al. 2008), in Venezuela (Liñero-Arana and Díaz-Díaz 2012), and in the Eastern Atlantic, in the Gulf of Guinea (Hartmann-Schröder 1971).Therefore, F. uschakovi is thought to be an exotic, and possibly, an invasive species.
According to the World Wildlife Fund for Nature (2012), exotic and invasive species are those foreign species that have been naturally or artificially (accidentally or intentionally) introduced to a region where they did not exist before, and once there, are adapted to their new environment.Liñero-Arana and Díaz-Díaz (2012) mentioned that the presence of invasive species in a location outside their current distribution might result from five recognized causes: First, transfer by fouling communities (fouling) attached to the outside of boat hulls; second, introduction of species for culturing, or as bait for fishing; third, exchange of species through waterways; fourth, release of species related to the pet industry; and fifth, expulsion of organisms from the ballast waters of ships.In order to better understand the mechanisms by which a particular species may be found outside of its natural range, it is necessary to examine each of these five causes and their potential influence where such species are positively identified.Further, it is critically important to determine the presence of invasive species that may threaten or even lead to the extinction of native species by competition or loss of habitat (Castro-Diez et al. 2004).
This study provides the first record of F. uschakovi in the Gulf of Urabá, in a region that has been recently studied in the context of marine biodiversity.Additionally, our research provides a morphological comparison of F. uschakovi with a sympatric species, F. miamiensis, which may be competing for resources with the former, likely exotic, species within the Gulf.

Study area.
The Gulf of Urabá is located on the northern coast of Colombia adjacent to the Isthmus of Panama, and is part of the Nica-Colombian continental shelf (Salazar-Vallejo 2000).The Gulf is part of the territory of Colombia's Department of Antioquia, and it is considered the second largest estuary of the Colombian Caribbean, representing 4291 km 2 of costal area, of which 650 km 2 are estuaries, dominated by mangrove forests (CORPOURABA 2003).According to Bernal et al. (2005), the Gulf of Urabá is a semi-enclosed body of water, approximately 80 km long and 25 km wide, with an average depth of 25 m, and maximum depth of 60 m.The Gulf receives fresh water from the Atrato River in the west, and other smaller rivers that empty into its southern end.The northern end of the Gulf is open to the Caribbean Sea, which interacts with river inflows to generate estuarine circulation patterns, including substantial freshwater surface layering.Within the Gulf, a relatively large number of bays and inlets have been formed as a result of the high levels of suspended sediments carried in from surrounding rivers, which in turn supports the establishment and growth of Rhizophora mangle (Red Mangrove), Laguncularia racemosa (White Mangrove), Avicennia germinans (Black Mangrove) and fern forests.
El Uno Bay is located near the southeastern end of the Gulf, to the north of the municipality of Turbo (Fig. 1A-C).The bay is approximately 1.8 km long, 0.89 km wide, with an average depth of 1.0 m, and extends in a north-south direction.According to the mangrove system by García-Padilla and Palacio ( 2008), and our observations during this research, El Uno Bay is subdivided into the following zones: Northern zone with A. germinans dominant in the inner region, and R. mangle in the outer region; northwestern fringe zone with well-developed L. racemosa trees and low numbers of R. mangle due to harvesting; eastern zone with A. germinans dominant in the inner region, and young and mature trees of R. mangle in the outer region; southwestern fringe zone with sparse overall development dominated by R. mangle and some A. germinans trees; and the southern zone with a semi-enclosed circulation system, receiving high and low tidal water exchange, and without mangrove trees.
Sampling.El Uno Bay was sampled at five stations during August 2009 (Fig. 1C).Sampling was conducted according to the following collection process: (i) selection of the submerged roots of R. mangle trees not reaching the substrate, when possible; (ii) cutting and removal of 1-5 roots from different trees at each station, (iii) fixation of roots in a solution of 10% formalin in sea water.
In the laboratory, sampled roots of R. mangle were processed as follows: (i) formalin was removed by multiple freshwater exchanges through a 250 µm sieve to retain organisms; (ii) invertebrate and algal specimens (macroalgae, cyanobacteria) were selected and removed from roots; (iii) invertebrate specimens were preserved in 70% ethanol; macroalgae were preserved in 4% formaldehyde; (iv) invertebrates were separated into higher-level taxa (e.g.phylum, class, family), and (v) polychaetes were identified to levels of family, genus and species.The polychaete specimens were deposited in the Colección de Invertebrados Marinos, Universidad de Antioquia (CIMUA).
Taxonomic analysis.Four polychaete families were identified (Nereididae, Sabellidae, Serpulidae, Spionidae); however, only serpulids were considered for this research.For polychaete identification, we followed the dichotomous, taxonomic keys for genera prepared by Fauchald (1977), Bastida-Zavala and Salazar-Vallejo (2000) and Bastida-Zavala (2009).For identification of the serpulid polychaete species, F. uschakovi and F. miamiensis, we followed taxonomic keys and/or descriptions from Hove and Weerdenburg (1978), Bastida-Zavala (2009) and Bastida-Zavala and García-Madrigal (2012).Description.Complete specimen: Irregularly curved calcareous tubes, forming agregations.Thorax colour, brown; tori colour dark brown; abdomen colour beige; dark brown medial line along the dorsum.Length, 5.0 mm; width, 0.6 mm, with 7 thoracic chaetigers and 33 abdominal chaetigers.Branchial crown colour beige, divided into two groups of radioles: six radioles on right side, and seven radioles on left side; each radiole with six transverse bands in a ring-like arrangement with wide dark brown color pattern; most basal ring wider and darker than the rest; ventral base of branchial crown black.Inter-radiolar membrane absent.Operculum spherical with radial symmetry (Fig. 2B, C, E, F), and with a sub-convex distal plate; four rows of transparent spines directed outward, with spines of the interior row approximately one-half the length of spines in the other rows; peduncle colour, beige with dark brown groove.Eyes absent.Collar with entire margin; thoracic membranes fused along the dorsum; six thoracic neuropodial tori.Chaetae from collar serrated, with one longitudinal line of teeth from the base to the apex (Fig. 2I, J), thorax with capillary chaetae (Fig. 2H), and abdomen with geniculate chaetae, proximal half serrated (Fig. 2G), and distal half smooth.Thoracic uncini saw-shaped with 6-7 teeth (Fig. 2K).Rounded pygidium with a midline incision.

Systematics
Variations.The specimens vary in length from 3 mm to 7.5 mm, in width from 0.5 mm to 0.8 mm.The number of chaetigers varies from 36 to 45.The number of transparent rows of spines from the operculum varies from 1 to 4. The number of transversal rings in the crown varies from 4 to 6.
Remarks.Ficopomatus uschakovi was present in samples from the opening of El Uno Bay, in sympatry with F. miamiensis, although F. uschakovi was more abundant inside of El Uno Bay.Of these two serpulid species, only F. uschakovi was found within the inner bay, which may indicate that this species has replaced F. miamiensis in that region.Morphologically, F. uschakovi differs from F. miamiensis by the presence of a spherical operculum with 1-4 transparent spines in a radial arrangement, and dorsal fusion of the thoracic membranes.These characters represent important diagnostic features for recognizing F. uschakovi, according to Hove and Weerdenburg (1978).Of the remaining taxonomic characters, the presence of seven thoracic chaetigers, and toothed collar chaetae, are generic characters.Distinctively, F. uschakovi builds calcareous tubes with longitudinal keels, and well-formed rings, whereas F. miamiensis builds smoother calcareous tubes that exhibit only very diffuse growth rings (Hove and Weerdenburg 1978).
Hove and Weerdenburg (1978) comment that F. uschakovi has been commonly misidentified as F. enigmaticus, because both species are able to live in brackish water.However, Hartmann-Schröder (1971) and Pillai (1971) clarified this confusion, emphasizing on the geographical separation of these species; Ficopomatus enigmaticus occurs in subtropical regions of Europe, while F. uschakovi, originally recorded in the Indo-West Pacific region, was recently found in the Caribbean Sea and the Tropical Eastern Pacific.Nevertheless, according to Hove and Weerdenburg (1978), the most important features for splitting these two species are in terms of the morphology.While F. uschakovi has an operculum with a sub-convex distal plate, F. enigmaticus has a concave distal plate.Also, F. enigmaticus sometimes has, dorsally, incomplete and irregular rows of spines, and may have one to three short radial accessories spines, while F. uschakovi lack accessory spines and has complete and regular rows of spines in the operculum.
According to Hove and Weerdenburg (1978), F. uschakovi has a distribution in the southern hemisphere, from India, through the Indian Ocean, to the Philippines and northern Australia.However, it has been recorded also from the Caribbean region, in Venezuela (Liñero-Arana and Díaz-Díaz 2012) and north-eastern Brazil (de Assis et al. 2008); and from the tropical Eastern Pacific, in Mexico (Bastida-Zavala and García-Madrigal 2012).
We consider F. uschakovi as an exotic species in the Colombian Caribbean.It is likely that this species may have been transported to the Gulf of Urabá from the Indo-Pacific attached to hulls of ships crossing from the Pacific Ocean to Caribbean Sea through Panama Canal, or from the Eastern coast of Africa to the Caribbean.Once in the Gulf, the species migrated to El Uno Bay, which is very close to the place where the ships are charged, aided by the tidal currents.Also, in support that F. uschakovi is an exotic species: during 2009 the species was found only in El Uno Bay, southern Gulf of Urabá; but, during 2012, this species was found also to the north of El Uno Bay, where it was not found before.This means that the distribution of the species has spread along the eastern coast of the Gulf in a South-North direction.This study provides the first record of F. uschakovi in Colombia.However, many localities of the northern Colombian Caribbean lack information on the distribution of F. uschakovi, which limits our understanding of its distribution in the southern Caribbean.Further distributional data will be presented in a forthcoming paper on the biogeography of the species.
Finally, specimens of F. uschakovi were found on mangrove roots in association with specimens of other species belonging to the families Nereididae (Neanthes succinea, Stenoninereis tecolutlensis and Namalycastis sp.1), Sabellidae (Demonax lacunosus), and Spionidae (Boccardiella sp.).Future research should include formal descriptions of these other species, and an assessment of their respective distribution patterns.Physical-chemical conditions found within the Bay during the sampling period are provided in Table 1.
Distribution.Indian Ocean from the Eastern coast of Africa to Australia; Eastern Pacific in Southern Mexico; Western Atlantic, in the Colombian, Venezuelan and Brazilian Caribbean coasts.Eastern Atlantic, in the Gulf of Guinea.

Figure 1 .
Figure 1.Study Area: A Colombia B Gulf of Urabá C El Uno Bay (Red points correspond to sampling sites).

Figure 2 .
Figure 2. Ficopomatus uschakovi(Pillai, 1960).Specimen SERP 0031B: A Antero-dorsal view B Operculum in anterior view C Operculum in lateral view G Geniculate chaetae from the abdomen H Limbate chaetae from chaetiger 3 I Toothed and limbate chaetae from collar J Toothed chaetae, detail K Uncini from chaetiger 3. Specimen SERP 0033 in methyl green: D Complete specimen in dorsal view E Operculum in lateral view.Specimen 1 SERP 0034: F Operculum in lateral view.

Table 1 .
Physical-chemical conditions found in El Uno Bay, during the sampling period.Abbreviations: O 2 oxygen; T Temperature; TDS dissolved solids; Sal Salinity; Cond Conductivity.