Eunicida and Amphinomida polychaetes (Annelida) inhabiting dead coral fragments in the Chinchorro Bank Biosphere Reserve, Mexican Caribbean Poliquetos de Eunicida y Amphinomida (Annelida) que habitan fragmentos de coral muertos en la Reserva de Biosfera del Banco Chinchorro, Caribe Mexicano

Introduction: The polychaete fauna inhabiting Chinchorro Bank has been poorly studied and only 35 species have been previously reported. Objective: To examine the taxonomic composition of the Eunicida and Amphinomida associated to dead coral substrates from this coral reef atoll, a Biosphere Reserve located in the southern Mexican Caribbean. Methods: In April 2008, dead coral fragments of the genus Porites were manually collected by SCUBA diving at eight stations between 4-16.2 m depth. Results: A total of 714 individuals belonging to 17 genera and 48 species of the families Amphinomidae, Dorvilleidae, Eunicidae, Lumbrineridae, Oenonidae and Onuphidae were identified. Eunicidae was clearly the more diverse (29 species; 60.4 %) and abundant family (479 individuals; 67.1 %), while the Oenonidae and Onuphidae were represented by only one individual-species each. Thirty-eight species (79.2 %) were new records for Chinchorro Bank, of which 23 species (47.9 %) were newly reported for the Western Caribbean ecoregion. Conclusions: The polychaete fauna recorded showed that the Chinchorro Bank reef is a species-rich habitat that deserves further study; the 48 species from six families identified were similar or even greater than the number of species reported from dead coral environments of other Caribbean Sea regions.


Introduction
The Mesoamerican Barrier Reef System is the second largest barrier reef in the world, after the Great Barrier Reef in Australia (Carrillo, Johns, Smith, Lamkin, & Largier, 2015). Stretching over 1 000 km, it goes from the tip of the Yucatan Peninsula, Mexico, down to Belize, Guatemala and Honduras. The Chinchorro Bank Biosphere Reserve is part of this reef system (Instituto Nacional de Ecología [INE], 2000). It is located at the southeastern end of Mexico, approximately 39 km offshore from Mahahual, Quintana Roo (Fig. 1), and is one of the most important platform reefs of the Caribbean Sea (46 km long and 19 km in its widest part); it includes reef structures, a reef lagoon with an area of 550 km 2 , three cays and oceanic waters (De Jesús-Navarrete, 2003). Coral reefs are among the most ecologically important marine ecosystems of the planet, due to their high biodiversity and productivity, complex biological relationships and intricate trophic structures, as well as high spatial heterogeneity associated with different habitats (Glynn, 1997;Fernández, Bone, & Rodríguez, 2012;Bertness, Bruno, Silliman, & Stachowicz, 2014). Corals are abundantly distributed in Chinchorro Bank, but extensive seagrass meadows and mangrove forests, which provide additional breeding habitats for many species, can also be found there (Ruiz-Abierno & Armenteros, 2017). The Caribbean Sea has been catalogued as one of the five worldwide "biodiversity hotspots" in marine environments (Roberts et al., 2002;Dean, 2012). More than 12 000 species have been reported in this region, of which about 60 % correspond to fishes, crustaceans and mollusks . This implies that the other faunal groups are poorly known. Undoubtedly, this is the case for the annelid polychaetes, since only about 5 % of the known marine species of the Caribbean Sea correspond to annelids (Costello et al., 2010;Dean, 2012), even though they are one of the main benthic groups worldwide. The presence of widespread seagrass meadows and mangrove forests, in addition to the dominating coral reefs, certainly provide breeding habitats for many species (Bertness et al., 2014;Ruiz-Abierno & Armenteros, 2017). Therefore, it is expected that the polychaete fauna inhabiting the Caribbean Sea is composed of many more species than the current records indicate (Dean, 2012). In Chinchorro Bank, about 800 species of flora and fauna have been listed, of which about 280 are invertebrates, mainly corals, gastropoda, bivalvia and porifera (INE, 2000). In particular, the polychaetes are virtually unknown in this marine reserve, since there have been few studies on these worms and the existing reports were the result of occasional samplings in very restricted localities. From the Chinchorro Bank region, there were about 35 polychaete species, belonging to 10 families: Amphinomidae, Eunicidae, Euphrosinidae, Lumbrineridae, Maldanidae, Nereididae, Onuphidae, Sabellidae, Serpulidae and Terebellidae (Salazar-Vallejo, 1996, Carrera-Parra & Salazar-Vallejo, 1998Bastida-Zavala & Salazar-Vallejo, 2000;Carrera-Parra, Fauchald, & Gambi, 2011, among others). Polychaetes are among the dominant invertebrates in dead coral fragments, followed by sipunculans, mollusks and crustaceans (Hutchings, 1983;Tribollet, Decherf, Hutchings, & Peyrot-Clausade, 2002;Fernández et al., 2012). Usually, boring sponges, molluscs and sipunculans are the major bioeroders of corals causing the more importat loss of coraline substrates in mature boring communities (Hutchings, 1986(Hutchings, , 2008. However, the polychaetes are important in the early stages of bioerosion in coralline substrates, since a succession of polychaetes colonizing those substrates facilitates subsequent recruitment by sponges, molluscs and sipunculans (Hutchings, 2008). In Chinchorro Bank, the high abundance and wide ocurrence at all the sampled stations of polychaetes of the family Eunicidae, could contribute to important modifications and degradation of the coralline skeletal structure due to their known bioeroder effects. Although few quantitative studies on the cryptic polychaetes have been carried out in the Caribbean Sea, they have shown that the eunicids are one of the most abundant and diverse families of polychaetes in dead coral environments (Ochoa-Rivera, Granados-Barba, & Solís-Weiss, 2000;Fernández et al., 2012). On the other hand, in Chinchorro Bank, the Amphinomida group was only represented by the family Amphinomidae, which includes some large and coral reef-dwelling polychaetes, known commonly as "fireworms", Eurythoe complanata and Hermodice carunculata (Borda et al., 2015). Although the presence of amphinomids in the Mexican Caribbean is limited and only six species have been recorded, they are usually abundant in coral reefs, where they feed on anemones and coral polyps. That is why the aim of the present study is to provide a more comprehensive database on the occurrence of the polychaete families, specifically focusing on the Eunicida and Amphinomida groups associated with dead coral fragments in the Chinchorro Bank Biosphere Reserve. These results may provide a useful tool to establish a baseline for the spatial characterization of this important invertebrate group and help in future analyses of the marine biodiversity of the Caribbean Sea.

Material and methods
The biological material (dead coral) was collected in April 2008, at eight stations of the north and central regions of the Chinchorro Bank Biosphere Reserve (18°23' -18°47' N; 87°14' -87°27' W) (Fig. 1). The samples were collected betweeen 4 and 16.2 m depth, and environmental data were also taken: salinity with a refractometer (±0.5 psu) and temperature (°C) with a field mercury thermometer (±0.1 °C) ( Table 1). Coral fragments from the genus Porites were manually collected by SCUBA diving, which were selected because, among the stony fragmented corals, they showed the best porosity and potentially more opportunities for galleries (natural or digged), to shelter a higher number of individuals. About 5.6-12.4 kg were collected at each sampling site and the volume of fragments was measured in the field by water displacement. Samples were directly placed in a plastic bag and then fixed with 10 % formalin in seawater. In the laboratory, the rocks were washed with freshwater and carefully broken into small pieces to extract the specimens. The fragmented substrates were then washed through a 0.5 mm mesh sieve to retain the remaining organisms. Following fixation, all biological material was preserved in 70 % ethanol. Polychaetes were separated, classified into families and quantified. The polychaete cryptofauna in Chinchorro Bank was represented by 19 families (Table 2), and as has been observed in other Caribbean Sea regions (Ochoa-Rivera et al., 2000;Fernandez et al., 2012;Dean, 2016) the Syllidae was the most abundant family (563 individuals; 28 %), followed by the Eunicidae (479 individuals; 24 %), Nereididae (339 individuals; 17 %) and Lumbrineridae (187 individuals; 9 %). In the present study, we included the taxonomic revision of Eunicida and Amhinomida groups, which were so widely distributed in Chinchorro Bank that they represented 37 % of the collected fauna; they were identified to species level. Of course, taxonomic revisions of the remaining families, yet under study, will be important in the future for a complete understanding of the occurrence and distribution of the polychaetes in Chinchorro Bank. The Eunicida polychaetes were identified to species following the taxonomic keys of Gathof (1984a), Uebelacker (1984), Wolf (1984), , 1998, Carrera-Parra (2006) (2015) were used. The validity of the identified species names was verified with recent systematic reviews and with the World Polychaeta database (Read & Fauchald, 2018 (Table 3). Eunice imogena was collected for the first time in the whole Caribbean Sea; previously, this eunicid had only been recorded from Hotspur Bank, Brazil (Fauchald, 1992a).   (Núñez, Brito, & Ocaña, 1991); in shallow waters, mixed sediments, seagrass beds, in rocky shores (Salazar-Vallejo, 1997 Hermodice carunculata (Pallas, 1766) Type locality: West Indies. Habitat: Shallow waters, associated with algae or in soft bottoms, with or without seagrasses. (Núñez et al., 1991;Salazar-Vallejo, 1997 Although specimens from Chinchorro Bank displayed a branchial distribution similar to that reported in the original description (chaetiger 2 to 6 with one to five filaments), in small individuals the caruncle is very small, its shape difficult to observe, and only in the largest organism the bifurcate, stout denticulate setae with a small basal spur and denticulate capillary chaetae were observed. It is evident that an examination of the type material is neccesary to clarify the taxonomic status of this species, justifying the "cf." adopted in this study.  (Wolf, 1986); in coarse to fine sand, silty to fine sand (Wolf, 1984(Wolf, , 1986. Chinchorro Bank: in dead coral fragments, 5 m depth, 26.6 ˚C, 35.79 psu.

Notopygos crinita Grube, 1855
Distribution: off Florida and Alabama (Wolf, 1984); Puerto Rico; east coast of Florida (Wolf, 1986); Cuba (San Martín & Major, 1988); Grand Caribbean (Salazar-Vallejo & Salazar, 2008). Chinchorro Bank: Southwest of Cayo Centro. Remarks: According to Wolf (1986), in the specimens with 45 chaetigers, the antennae have 7 articles. However, in the specimens from Chinchorro Bank with 61 chaetigers, the antennae have 11 articles and the simple serrated chaetae in those individuals possess a very small distal tooth, not easy to detect, but not mentionned in the original diagnosis.

Remarks:
The specimens agree well with the redescription made by Fauchald (1992a) based upon type material.

Discussion
According to the marine biogeography classification system suggested by Spalding et al. (2007), the Grand Caribbean is included in the Northwestern Atlantic Province and the coasts of Mexico are part of the Western Caribbean ecoregion, one of the regions where a lower number of polychaete species (417, including records of the present study) has been reported. On the contrary, the highest species richness has been found in the Greater Antilles (652 species), specifically around Cuba (533 species) (Dean, 2012), but we assume that this is, at least in part, since more intense polychaete surveys have been done more frequently. According to Dean (2012) (Table 2). Although only the Eunicida and Amphinomida groups were examined to species level, their observed data also showed that the 48 species from six families found in Chinchorro Bank could be similar or even greater than the 42 species from 19 families recorded in dead coral substrates from Cozumel Island, Mexican Caribbean (Ochoa-Rivera et al., 2000), or the 68 polychaete species from 22 families reported from intertidal coralline rocks and some subtidal localities of the Caribbean coasts of Costa Rica (Dean, 2016). Although in the present study only the Eunicida and Amphinomida were examined, the great abundance and number of species of eunicids in coral environments was evident in this area, since it is one of the most important families of polychaetes in Chinchorro Bank and, up to now, the taxon with the largest number of species recorded. Eunicids are one of the more diverse and abundant families of polychaetes found in dead coral fragments in the Caribbean Sea. The exception is the Costa Rican coasts where rocks and rootmats of seagrasses were also sampled and the syllids were the most diverse with 12 species. The present study also showed that the 29 species of eunicids found in Chinchorro Bank were clearly larger than the 17 species recorded in northern Venezuela (Fernández et al., 2012), the 11 species reported in Costa Rica (Dean, 2016) or the 7 species collected in Cozumel Island (Ochoa-Rivera et al., 2000). Eunicids live in well developed borings, which they dig with their complex and well developed jaws; acid secretions may also occur, but this has not been verified (Hutchings, 2008). Although their densities change with the habitat and local peculiarities, large eunicids, often reaching many centimeters in length, are usually most abundant as the boring communities mature (Hutchings, 2008). This could be evidence of the high level of fragmentation of the corals and maturity of the polychaete assemblages populating these environments in Chinchorro Bank. On the contrary, although the amphinomids reach their highest diversity in shallow tropical and subtropical environments, playing an important ecological role in coralline and rocky habitats (Kudenov, 1995), in Chinhorro Bank they were not as abundant as expected. Some species, such as Hermodice carunculata, which is a common resident of coral reefs and littoral zones of the Caribbean Sea, has been considered a major and voracious predator of both soft and hard corals, and prey on zoanthids, anemones, gorgonids, hydrocorals, scleractinians and octocorals, among others (De Assis, Dias, & Christoffersen, 2017). However, the occurrence of this species, but also of all other amphinomid species, on dead coral environments, clearly decreases in Chinchorro Bank and other Caribbean regions (Ochoa-Rivera et al., 2000;Fernández et al., 2012;Dean, 2016). So, the few abundant species identified (four), compared to the 20 species reported from the Caribbean Sea (Dean, 2012), showed that their populations do not reach a significant development in the examined dead coral environments. This is the first sistematic revision of the polychaete species inhabiting the Chinchorro Bank Biosphere Reserve, and the taxonomic information presented here contributes to the understanding of the occurrence of the polychaete fauna in the Western Caribbean ecoregion, where the relatively limited number of studies and low sampling effort do not emphasize adequately the importance of the marine biodiversity in this invertebrate group.
Ethical statement: authors declare that they all agree with this publication and made significant contributions; that there is no conflict of interest of any kind; and that we followed all pertinent ethical and legal procedures and requirements. All financial sources are fully and clearly stated in the acknowledgements section. A signed document has been filed in the journal archives.