Fauna diversity in Madracis spp. coral patches in the Colombian Caribbean

Abstract

Fauna diversity in Madracis spp. coral patches in the Colombian Caribbean

Madracis spp. coral patches are the main deep–sea framework builder observed on the shelf–break scarp of the Colombian Caribbean, between 107 and 230 m depth. The Marine Protected Area, Corales de Profundidad National Natural Park, was established in 2013 to protect a site of high biodiversity associated with Madracis communities. Our research summarizes the advances in knowledge of its biodiversity as the result of four expeditions and offers insights into the state of its associated fauna. Madracis colonies occur in five areas of the park but corals thrive and build coral patches in only two of the five, both in the southwest area. Our surveys have resulted in the inventory of 337 species. Mollusca (116) dominated the fauna, followed by Bryozoa (70), Cnidaria (50), Echinodermata (39), Arthropoda (14), Annelida (13), Brachiopoda (3), and Chordata (32 fishes). Store voucher specimens at the Museo de Historia Natural Marina de Colombia–Makuriwa and metadata are available online in the SiBM database.

Checklist published through GBIF (DOI: 10.15470/vqshir)

Key words: Marine Protected Area, Benthic, Deep–sea corals, Macrofauna, Megafauna, New records

Resumen

Diversidad faunística en los parches de coral aislados de Madracis spp. del Caribe colombiano

El coral Madracis spp. es el principal bioconstructor de las aguas profundas del borde de la plataforma continental del Caribe colombiano, entre 107 y 230 m de profundidad. El Área Marina Protegida Parque Nacional Natural Corales de Profundidad se estableció en 2013 a fin de proteger una zona de alta biodiversidad asociada a estas comunidades. Nuestra investigación resume los avances en el conocimiento de su biodiversidad como resultado de cuatro expediciones y ofrece una visión del estado de la fauna asociada. Las colonias de Madracis están presentes en cinco zonas del Parque, pero solo en dos de ellas, situadas en la zona suroeste, construye los parches de coral aislados. Nuestros estudios han dado como resultado un inventario de 337 especies. El filo Mollusca (116) domina la fauna, seguido de Bryozoa (70), Cnidaria (50), Echinodermata (39), Arthropoda (14), Annelida (13), Brachiopoda (3) y Chrordata (32 peces). Los especímenes se encuentran en el Museo de Historia Natural Marina de Colombia–Makuriwa y los metadatos están disponibles en línea en la base de datos del SiBM.

Lista de datos publicada en GBIF (DOI: 10.15470/vqshir)

Palabras clave: Área Marina Protegida, Bentos, Corales de profundidad, Macrofauna, Megafauna, Nuevos registros

Resum

Diversitat faunística als esculls de corall aïllats de Madracis spp. del Carib colombià

El corall Madracis spp. és el principal bioconstructor de les aigües profundes de la vora de la plataforma continental del Carib colombià, entre 107 i 230 m de profunditat. L'Àrea Marina Protegida Parc Nacional Natural Coralls de Profunditat es va establir l'any 2013 per tal de protegir una zona d'alta biodiversitat associada a aquestes comunitats. La nostra recerca resumeix els avenços en el coneixement de la biodiversitat com a resultat de quatre expedicions i ofereix una visió de l'estat de la fauna associada. Les colònies de Madracis es troben presents en cinc zones del Parc, però només en dues, situades a la zona sud–oest, construeix esculls de corall aïllats. Els nostres estudis han donat com a resultat un inventari de 337 espècies. El fílum Mollusca (116) domina la fauna, seguit de Bryozoa (70), Cnidaria (50), Echinodermata (39), Arthropoda (14), Annelida (13), Brachiopoda (3) i Chrordata (32 peixos). Els espècimens es troben al Museu d'Història Natural Marina de Colòmbia–Makuriwa i les metadades estan disponibles en línea a la base de dades del SiBM.

Llista de dades publicada a GBIF (DOI: 10.15470/vqshir)

Paraules clau: Àrea Marina Protegida, Bentos, Coralls de profunditat, Macrofauna, Megafauna, Nous registres

Introduction

Like their analogs from shallow waters, deep-sea coral communities are a reservoir of ecological, biological and chemical resources and home to a great biodiversity, including species of commercial interest and potential new species for science (Roberts et al., 2009). In the Caribbean region, knowledge of this valuable ecosystem remains understudied, and vast areas are still unexplored (Lutz and Ginsburg, 2007; Hernández-Ávila, 2014). Due to their vulnerability to environmental disturbances and anthropogenic activities, several global efforts have been oriented to protect and study these unique habitats (Fuller et al., 2008; Hourigan, 2009; Zimmerman et al., 2020).

The Corales de Profundidad National Natural Park (CPNNP) was declared by the Resolution 0339 of 2013 (MADS, 2013) according to IUCN category II, and hosts one of the three deep-sea corals areas identified in the Colombian Caribbean (Reyes et al., 2005; Flórez and Santodomingo, 2010; Santodomingo et al., 2013; Alonso et al., 2021). The highly diverse communities that inhabit the CPNNP are mainly supported by habitat-forming species of Madracis (Santodomingo et al., 2007). In 2001 these communities were accidentally discovered during the 'Macrofauna II' expeditions using epibenthic trawl nets (Reyes et al., 2005). The area was later mapped and characterized in 2005 during the 'Marcoral' expedition, using Van Veen dredge and rock dredges (Santodomingo et al., 2007, 2013). Detailed maps, the first footage and the description of macro-habitats were obtained using ROV and multipurpose drift-cam (CADEM) during the expeditions carried out in 2015 (Alonso et al., 2015, Cedeño-Posso et al., 2022) and 2016 in campaigns 'PNN Corales de Profundidad' and 'PNN Madracis', respectively.

During the campaign PNN Corales de Profundidad (2015), eleven areas of potential development of Madracis were explored and mapped using a digital elevation model of bathymetry and ROV surveys. Madracis colonies were observed in five of the eleven areas surveyed. However, Madracis corals thrive and sustain a large concentration of marine fauna only in two of the areas, both in the southwest where they were discovered (Santodomingo et al., 2007; Alonso et al., 2015; Cedeño-Posso et al., 2022). These two coral patches were targeted for additional multipurpose drift-cam surveys during the PNN Madracis expedition in 2016.

This paper describes and summarizes the state-of-the art of the biodiversity associated with these Madracis spp. coral patches. Here, we integrate the information obtained in four expeditions using several methods in order to provide a physical description of the patches, their distribution, and an inventory of cnidarians, mollusks, bryozoans, brachiopods, annelids, arthropods, echinoderms and fishes that inhabit these important deep-sea coral communities in the CPNNP.

Material and methods

The CPNNP is located in the Colombian Caribbean (fig. 1) on thecontinental margin off the Gulf of Morrosquillo and the Archipelago of San Bernardo, approximately 12 km from one of the areas with major development of shallow-water coral reefs in Colombia, Corales del Rosario y de San Bernardo National Natural Park, and 32 km from the nearest point on the continent (Barú Peninsula). The area is characterized by a strong influence of continental inputs, relatively transparent waters, and large mosaics combining bio-clastic sediment plains and extensive development of coral reefs (Díaz et al., 2000).

The work circumscribed biodiversity data where Madracis spp. coral patches occur southwest of the CPNNP, at depths of 107 and 230 m. These patches are located within the coordinates 9° 46' 18.208" N-9° 50' 33.101" N and 76° 11' 10.099'' W-76° 14' 39.688'' W (fig. 1). Madracis colonies have been identified as a species complex that includes M. myriaster (the most abundant), M. asperula and M. brueggemanni (Santodomingo et al., 2007) (fig. 2) given the difficulty to differentiate M. myriaster from its sister species M. brueggemanni (Ballesteros-Contreras et al., 2022). According to the digital elevation model (DEM), they are on a moderate slope between 4º to 11º in the transition between the continental shelf and the shelf-break scarp, probably covered by recent sediment flows, and over a sliding crown (Santodomingo et al., 2007; Moraleset al., 2017). Biodiversity data were compiled from four research expeditions carried out in the southwest area of the CPNNP (table 1): (1) 'Macrofauna II' (2001), a baseline survey on soft bottoms in the Colombian Caribbean with collections made with an epibenthic trawl net (9 × 1 m opening; 3 knots for 10 min) (fig. 3A) (Reyes et al., 2005). (2) 'Marcoral' expedition (2005), a study for mapping and characterizing the occurrence of Madracis corals using a single-beam echo sounder, collections with a Van Veen dredge (60 l, 0.03 m²) (fig. 3B) and a heavy-chained rocky dredge (1 × 0.4 m opening; 1.5 knots for 5 min) (Santodomingo et al., 2007; Santodomingo et al., 2013). (3) 'PNN Corales Profundidad' expedition (2015), to perform detailed geomorphological mapping (Morales et al., 2017) supported by the first footage obtained using ROV Diavolo II (fig. 3C) with a front camera (¼'' CCD 380 I TV-lines, 0.1 Lux/F = 1.2) and 10 cm parallel lasers for scale. Positioning was estimated using an ultra-short baseline (USBL) mounted on the vehicle (Cedeño-Posso et al., 2002). (4) 'PNN Madracis' expedition (2016), a complementary expedition for sampling areas using a multipurpose drift-cam (CADEM) with a modified Van Veen grab (0.066 m²) to collect samples of sediments (fig. 3D). The drift-cam incorporates high-definition cameras capable of acquiring color images with 61° range, 120 x zoom and 2,200 lumen LED lights, both with titanium casing resistant up to 4,000 m depth, a multimedia tracking console, and adaptable protection cages for different environments.

The quality of the videos (380 TV-lines) allowed recognition only of common taxa larger than 10 cm (cnidarians, crustaceans, echinoderms and fish), with exceptional cases of fauna > 5-10 cm such as cup corals with extended polyps and crustaceans. Biological samples that remained unsorted from Marcoral and PNN Madracis (Bryozoa and Annelida) were identified to the lowest taxonomic level possible. Identifications were confirmed from videos based on specimens deposited in the collections of the Museo de Historia Natural Marina de Colombia (MHNMC)–MAKURIWA of INVEMAR in Santa Marta, Colombia.

Data quality controls were applied to the species previously identified in 'Macrofauna II' and 'Marcoral' campaigns through the validation of their current taxonomic status. Likewise, taxonomic levels higher than family were excluded from the analysis to avoid uncertain identifications and data duplicity, except for specimens identified in the orders Antipatharia, Comatulida and Ophiurida that correspond to unique specimens observed in the ROV videos. Consulted updated taxonomic identities and classifications in the World Register of Marine Species (WoRMS, 2022) and Eschmeyer's Catalog of Fishes (Fricke et al., 2020). All biological data and collections are available in the Marine Biodiversity Information System (SiBM-OBIS, Colombia) and it stored voucher specimens at the Museo de Historia Natural Marina de Colombia (MHNMC)–MAKURIWA of INVEMAR in Santa Marta, Colombia. Our analyses use the concept of species diversity in terms of species/morphospecies richness. Geo references for stations were verified by the Geographic Information Systems Laboratory of INVEMAR (LabSiS) through ArcGIS Desktop-ArcMap 10.6 (2018) Software. Coordinates and sampling methods for the 14 stations analyzed in this review are summarized in table 1.

Results

Structural description and distribution

Madracis spp. are located at the south-west of the CPNNP. They cover an area of approximately 2.1 ha. Their delicate branches form small bushy colonies of about 50-80 cm high and up to 1 m wide. They are situated along the shelf-break scarp at between 107 and 230 m depth, and they are irregularly distributed on the muddy sand substates (fig. 2) forming coral patches. The area is characterized by warm waters with temperatures between 19º and 23°C, strong currents at the surface between 0.2 and 0.3 m/s, and milder currents near the bottom between 0.1 and 0.2 m/s.

Diversity associated

Our compiled dataset from the SiBM and MARIKUWA Museum collections and imagery resulted in a biodiversity inventory of 337 species belonging to eight phyla (see checklist published through GBIF, DOI: 10.15470/vqshir). Mollusca is the phylum of highest species richness with 116 species (34.4%), followed by Bryozoa with 70 species (20.8%), Cnidaria with 50 species (14.8%), Echinodermata with 39 species (11.6%), Chordata (Fishes) with 32 species (9.5%), Arthropoda with 14 species (4.1%), Annelida with 13 species (3.8%) and Brachiopoda with three species (~1%). Most records come from the early collections of 'Macrofauna II' and 'Marcoral' (87.5%), accounting for almost the total list of species of mollusks, cnidarians, echinoderms, crustaceans, and brachiopods and about three-quarters of the compiled fish list. Although 43 species were identified in the videos, they account only for 10% to additional records of the associated fauna contributed by the collections of the projects PNN Corales de Profundidad and PNN Madracis, and 8% correspond mainly to the inventory of bryozoans and annelids. General characteristics of the studied taxa are summarized from the most diverse to the least diverse phylum. A complete list of species is shown in appendix 1 and checklist published through GBIF, DOI: 10.15470/vqshir).

Mollusca
With 116 morphospecies, mollusks are by far the most diverse. Records mainly come from collections of the 'Macrofauna II' and 'Marcoral' expeditions. The malacofauna comprised four classes: Gastropoda (104 species), Bivalvia (10 species), Cephalopoda (one species) and Scaphopoda (one species). From these morphospecies, 76 were identified at species level, 36 at genus level and four at family level (appendix 1). Gastropoda included seven orders represented by 50 families. Among these, the most diverse were Muricidae with nine species, followed by Fissurellidae and Mangeliidae with seven species each, and Drilliidae with six species. Bivalvia had representatives in five orders, of which Pectinida was the most outstanding with three families. Cephalopoda and Scaphopoda were represented by only one species each, Semirrossia tennera and Dentalium laqueatum, respectively. The most frequent species were Arene variabilis, Nassarius sp., Olivella myrmecoon, Olivella watermani, Polystira albida, Trivia candidula and Vexillum styria.

Bryozoa
Seventy morphospecies were found (appendix 1), of which 52 were identified at species level and 18 remained with open nomenclature, three in confer (cf.) and 15 in genus. It classified the specimens into 34 families belonging to the orders Cheilostomatida (89%) and Cyclostomatida (11%). The most diverse families were Cupuladriidae and Phidoloporidae (fig. 4A, 4B) with seven and six species, respectively, followed by Colatooeciidae, Lepraliellidae, Smittinidae and Schizoporellidae with four species each. Within cupuladriids, the genus Cupuladria is highlighted as the most diverse with five species, while for phidoloporids it was Plesiocleidochasma with three species. Within other families, outstanding genera were Trematooecia (two species), Celleporaria (three species), Parasmittina (two species) and Stylopoma (three species). The species Aimulosia palliolata, Celleporaria magnifica, Colatooecia serrulata, Gemelliporina hastata, Micropora acumminata, Steginoporella connexa, Stylopoma smitti, Trematooecia arborescens, Turbicellepora pourtalesi, and the genera Drepanophora and Metrarabdotos, are new records for the Colombian Caribbean (appendix 1 indicated by asterisks *). Regarding growth type, the majority of species were encrusting colonies (70%), followed by erect, flexible and rigid forms (17%) and free-living colonies (11%). Bryozoans were found with Madracis spp. coral patches between 117 m and 217 m depth in six of the seven bottom-sampled locations. Bryozoans form small colonies, from one millimeter to a few centimeters, so none were observable in the video transects.

Cnidaria
Fifty morphospecies were identified, with representatives of five orders, Scleractinia (25 species) Alcyonacea (12 species), Antipatharia (10 species), Zoanthidea (two species) and Stylasterida (one species) (appendix 1). Thirty-three were identified to species level, 14 at genus level, two at family level and one to order. The most diverse families were the scleractinian Caryophylliidae with nine genera, followed by the black corals Antipathidae with five genera (fig. 6B), and the octocorals Ellisellidae with three genera. Besides colonies of the Madracis spp. complex (Madracis myriaster, M. bruggemanni and M. asperula) also identified were other frequent scleractinians from the family Caryophylliidae, Caryophyllia berteriana, Coenosmilia arbuscula, Oxysmilia rotundifolia, from the family Dendrophylliidae, Balanophyllia cyathoides and Eguchipsammia cornucopia (fig. 4F), and Javania cailleti from the family Flabellidae.

Echinodermata
The 39 Echinodermata records are based on the collections made during the 'Macrofauna II' expedition and a few records made with video-transects. Five classes were identified: Ophiuroidea (21 species), Crinoidea (nine species), Echinoidea (seven species), Asteroidea (one species) and Holothuroidea (one species). The expedition  identified thirty-five at species level, two at genus level (Amphilimna and Ophiacantha), one at order level (Comatulida) and one to class (Ophiuroidea) (appendix 1). Ophiuroidea presented 12 families, with Ophiosphalmidae as the richest, with three species, followed by Ophiotomidae with two species, Ophiacanthidae (two species), Amphiuridae (two species) and Gorgonocephalidae (two species). Among Crinoidea, six families have been recorded, of which Comatulidae is the richest with three species (fig. 6D, 6E); the other families each have one species. Echinoidea, on the other hand, presented five families, of which Clypeasteridae and Paleopneustidae were the richest with two species each.

Arthropoda (Crustacea)
Records are based on the collections made during the 'Macrofauna II' expedition (appendix 1). It identified twelve at species level, one at genus level (Iridopagurus) and one at family level (Callianassidae). Overall, this phylum comprised 11 families from the Bachyura infraorder: Aethridae, Goneplacidae, Inachidae, Inachoididae, Leucosiidae, Mithracidae, Palicidae, Plagusiidae, Portunidae, Paguridae (Anomura infraorder) and Callianassidae (Axiidea infraorder). Inachidae and Inachoididae were the richest families found with the species Anomalothir frontalis, Stenorhynchus seticornis, Stenorhynchus yangi, Collodes trispinosus and Pyromaia propinqua (fig. 5H and 5I).

Annelida
Records are based exclusively on the collection made during the last expedition using the multipurpose drift-cam (CADEM). Eleven were identified at genus level and two at family level (Enchytraeidae and Opheliidae), belonging to three subclasses, Oligochaeta (one species), Errantia (four species) and Sedentaria (eigth species). Amphinomidae was the richest family found. Two genera are new records for the Colombian Caribbean (Linopherus sp. and Aglaophamus sp.) and two are new records for the Greater Caribbean (Galathowenia sp. and Eclysippe sp.) (appendix 1 indicated by asterisks *).

Brachiopoda
Records of three species were mainly based on the collections of the 'Marcoral' expedition and some samples of 'Macrofauna II' (appendix 1). The identified species were Tichosina plicata, Terebratulina cailleti, and Argyrotheca barrettiana. Tichosina plicata and T. cailleti were the first records for the Colombian Caribbean (Rojas et al., 2015), increasing the number of brachiopod species known for the Colombian Caribbean Sea to five.The three species represent three families.

Fish (Chordata)
Records are based on the collections made during the 'Macrofauna II' expedition and a few additional observations made with video-transects, as fish are easily disturbed by submersibles. Twenty-seven were identified at species level, three at genus level, one at family level and one at order level (Pleuronectiformes) (appendix 1). Findings comprised nine orders, Perciformes (13 species), Scorpaeniformes (six species), Pleuronectiformes (four species), followed by Gadiformes, Lophiiformes and Zeiformes with two species each. And finally, orders with only one species each were Batrachoidiformes, Gasterosteiformes and Tetradontiformes. The families with the highest richness of species were Scorpaenidae with four species (Neomerinthe beanorum, Pontinus nematophthalmus, Pterois volitans and Scorpaena agassizii) and Serranidae also with four species (Epinephelus sp. fig. 6G, Serranus atrobranchus fig. 5L, Pronotogrammus martinicensis and Serranus phoebe fig. 6H).

Biodiversity data that settled the basis for the creation of the Marine Protected Area (MPA), include the first description of the Madracis communities by Reyes et al. (2005) and the series of papers to compile the status of knowledge of the anthozoan fauna of 'Marcoral' expedition by Santodomingo et al. (2007, 2013). The initial report of the fauna associated from one locality (two samples between 155 m and 160 m depth) recorded a total of 134 species of fishes (20 species) and invertebrates, including four main taxa Cnidaria (34 species), Mollusca (23 species), Echinodermata (38 species) and Crustacea (19 species) (Reyes et al., 2005). Subsequently, during the 'Marcoral' expeditions, the record of invertebrate richness increased to 333 species for the MPA, including both coral associated fauna and their adjacent soft bottoms: Cnidaria (40 species) (Santodomingo et al., 2007, 2013), Mollusca (215 species), Bryozoa (33 species), Echinodermata (14 species) and Crustacea (27 species). Under the framework of the 'Marcoral' project, one of the main goals was to identify biological criteria to support the creation of the MPA, so a more comprehensive study by Urriago et al. (2011) compiled the available biodiversity data of the shelf-break scarp in the MPA that resulted in a total of 528 species: 154 species of mollusks, 129 species of fishes, 110 species of crustaceans, 97 species of echinoderms and 38 species of cnidarians. Differences in the species numbers vary depending on the number of taxonomic groups at family or genera level included in the compilations, the number of localities, the type of habitat (coral, soft bottoms, hard grounds, etc.) considered in the analyses and multi-gear sampling (Reyes et al., 2005; Urriago et al., 2011 for methods). Within this context, the outcomes of our research are constrained to the specific localities in which Madracis spp. coral patches were found in abundance, in the sense that we have more certainty that we can refer to them as the biodiversity directly associated with the coral patches they build. As a result, a comparison between the original report of Reyes et al. (2005) where Madracis communities were discovered (one locality) and our up-to-date compilation (14 localities) evidenced an increase of more than two-fold for the species record from 134 species (Reyes et al., 2005) to 337 species (this review). New data include new 96 mollusks, 25 cnidarians, six echinoderms, three crustaceans, and 12 fish species, plus 70 species of bryozoans, 14 annelids, and three brachiopods that were not initially listed. This increase has been achieved thanks to the all the different collection methods and sampling efforts invested in exploring this area.

Regarding the physical environment where Madracis spp. corals patches develop, evidence from echo sounder profiles and video footage suggests that coral colonies are in low mounds (10 to 20 m high), and therefore they may be able to participate in the construction of coral mounds (Santodomingo et al., 2007). Regional geological characterizations have shown that mounds in this area are related to active mud diapirism and tectonism, which in turns result in a complex diversity of geoforms (Reyes et al., 2005; Rangel-Buitrago and Idárraga-García, 2010). More detailed mapping supported by geological sampling is still needed to better understand the geomorphology of Madracis coral patches occur and to what extent they may be able to build up bioherms on the seafloor. Independently of their ability to construct bioherms, there is no doubt that Madracis species are habitat-forming providing ecological niches for associated species (Rogers, 1999) and in this study we have found that their occurrence is related to a high number of species. As proposed for deep-sea coral frameworks, the construction of a three-dimensional structure is favored by sediment inputs that enhance the vertical growth, providing physical support around the corals (Wheeler et al., 2005, 2011). Sediment inputs also allow the delivery of organic particulate material to the epifaunal suspension-feeders (Wheeler et al.,2005, 2011; Mastrototaro et al., 2010). Most of the invertebrate fauna found here are suspension-feeders (scleractinians, octocorals, bryozoans, brachiopods, bivalves, crinoids, ophiurans, and polychaetes) inhabiting the mud/sand substrate where the colonies of Madracis settle. Sediment samples from the seafloor are mainly composed of mixed sand-mud sediments and coral rubble (Santodomingo et al., 2007) which also offer suitable substrates and nutrients for the colonization of sessile invertebrates (Buhl-Mortensen and Fosså, 2006; Henry and Roberts, 2007; Mastrototaro et al., 2010; Buhl-Mortensen et al., 2016; Winston, 2016).

Sampling and museum collections

Our outcomes highlight the importance of systematic sampling and museum collections (Funk, 2018) because most knowledge on the biodiversity of Madracis spp. coral patches is based on identifications of voucher specimens. Indeed, 97% of the species listed is based on museum specimens with accurate accompanying metadata. To date, footage collected with ROV and CADEM has provided a valuable overview of the seascapes where Madracis colonies occur -including growth forms, colony sizes, distribution and relation to some of the associated fauna. However, these data have been limited by the quality of the images and low-tech manipulator arm for collections. Underwater footage has shown about 12.9% of the morphospecies have been identified as they show diagnostic characters that can be recognized (mostly megafauna > 5 cm), yet they only add 28 morphospecies to our collection-based inventory. In general, studies of deep-water coral fauna have also found that images and videos alone are only useful to identify common taxa, and for most organisms access to physical samples for taxonomic purposes or fragments for molecular studies are recommended (Etnoyer et al., 2006; Henry and Roberts, 2016). Such is the case of Arthropoda, which we consider an underestimated group in the samples, either because of its mobility, which makes it difficult to capture, or because of its small sizes. Future collections will surely increase the number significantly. Further surveys with ROVs equipped with high-definition cameras and high-tech manipulator arms for the collection of target fauna are still needed to gain more insight into the extension and structure of these important communities.

This study must be understood as an effort to review the state-of-the art of our knowledge on the diverse fauna associated with Madracis spp. coral patches in the CPNNP. The collections of Makuriwa Museum hold an extensive number of specimens collected in other environments of the CPNNP, such as soft substrate, rubble, solitary corals, rock/ledges and rugged stones, other hard grounds and pockmarks, from 46 to 354 m depth (Cedeño-Posso et al., 2022). Moreover, specimens of important taxa such as sponges, foraminifera, tunicates and other cnidaria (Actiniaria and Hydrozoa), and tunicates are yet to be identified. In addition, greater efforts are underway to complete the inventories of Annelida, Bryozoa and Arthropoda (Crustacea), and the study of the food supply for the deep-sea corals, zooplankton (copepods, euphasian, cumaceans and chaetognaths) (Freiwald et al., 2002). Although mollusks are a more well-known group than other invertebrates, some of the collected material also requires further identification; for some morphospecies, it is essential to include an integrative approach. A full assessment of these collections is needed and will contribute to the planning and better management of this MPA.

Diversity and ecology of associated fauna

The habitat provided by Madracis offers shelter and food to an abundant and diverse fauna, as has been described for deep-sea coral communities (Lutz and Ginsburg, 2007). Fauna can be (1) intimately associated with the coral, or (2) associated with the substrate where the coral is established, or (3) in the case of demersal fauna, it can move between the coral patches and the rocky macro-habitats that surround them. Among the eight phyla recorded here, most species benefit from the habitat in these three different ways, while others, such as demersal fishes, fall mainly into the third category.

Mollusca
The high nutrient availability in this deep-sea environment is suitable for the establishment of mollusks because it supports a great diversity of detritivorous gastropods and bivalves, greatly surpassing the species record for other taxa (Janssen and Taviani, 2015). About one third of species that occur in the Madracis habitats belong to the class Gastropoda (104 species). Many deep-sea gastropods are detritivorous and may contribute to nutrient recirculation on the seafloor of the CPNNP because of their ecological traits (Ponder et al., 2019). One finding was the high frequency of snails with different feeding specializations, such as the spongivorous snail Calliostoma sp., detritivores like Nassarius sp., Olivella myrmecoön, Olivella watermani, and Euchelus sp., the carnivorous Conus sp., Trivia candidula, Antillophos chazaliei, Polystira albida and Cosmioconcha nitens and interestingly, the molluscivore Vexillum styria.

Bryozoa
Bryozoans are the second most diverse group associated with Madracis spp. coral patches. Their ability to colonize diverse substrates and to cope with environmental fluctuations such as temperature, salinity, turbidity and depth, have conferred them an adaptive success over other benthic marine competitors (O'Dea and Okamura, 1999). The relatively high species richness in these habitats and the notable prevalence of encrusting forms can be explained by the ability of bryozoan colonies to settle on the high availability of substrates provided by dead Madracis branches, coral rubble, and mollusk shells, similarly that have been described for Florida Oculina reefs (Winston, 2016). For example, in samples of the National Natural Park, specimens of Cribrilaria, Plesiocleidochasma, Celleporaria, and Stylopoma were observed attached to the branches of dead Madracis corals. On the other hand, the mud/sand sediments that surround Madracis spp. coral patches allow the development of free-living colonies (O'Dea, 2009), such as Cupuladria, the most diverse genus in this study and common and abundant in the Colombian Caribbean, up to 500 m depth (Flórez et al., 2007; Montoya-Cadavid and Flórez, 2010). It is worth mentioning that some bryozoan specimens reported here were found without tissues or opercula (appendix 1 indicated by cross +), suggesting that they may have been transported here through sediment flows from surrounding environments.

The high species richness of bryozoans associated with Madracis becomes more significant if it is compared with similar deep-sea coral environments of the continental shelf of Colombia (Flórez et al., 2007) and Florida (Winston, 2016). Even in the Mediterranean (Spain and France), where the sampling effort has been greater and included several localities, the richness estimate only reaches 74 species (Zabala et al., 1993; Rueda et al., 2019). The new records found in this MPA complement the Bryozoa inventory in the Colombian Caribbean (Osburn, 1947; Flórez et al., 2007; Montoya-Cadavid et al., 2007; Montoya-Cadavid and Flórez, 2010; Delgadillo-G. and Flórez, 2015; Gracia et al., 2018), encouraging the research of this group in this region.

Cnidaria
Represent the third most diverse fauna found in the area. They include solitary corals, octocorals, antipatharians, hydrozoans and zoanthids, characteristically associated with deep-sea coral habitats, where they can find suitable substrates to attach to such as broken branches of hard corals and shells. It seems that Madracis habitats also enhance the presence of other azooxanthellate scleractinians, as their abundance and richness are also higher than in other localities where they do not occur (Roberts et al., 2006; 2009; Santodomingo et al., 2013). For example, from the Colombian record of scleractinian species, Caryophyllia (Caryophyllia) barbadensis (fig. 4E) and Eguchipsammia cornucopia (fig. 4F) have only been found in these localities (Reyes et al., 2009, 2010; Santodomingo et al., 2013). Among other habitat-forming taxa, it is important to highlight that octocorals and antipatharians also offer shelter to other invertebrates found living in their colonies (Buhl-Mortensen and Buhl-Mortensen, 2005; Chacón-Gómez et al., 2012). Therefore, part of the high diversity of ophiurans, crustaceans and annelids is closely related not only to Madracis colonies but also to the presence of these other colonial anthozoans.

Echinodermata
A significant new diversity of echinoderms has also been observed in these Madracis spp. coral patches, as 21 out of 39 species found here were recorded for the first time in Colombia (Borrero-Pérez et al., 2002; Borrero-Pérez and Benavides-Serrato, 2004; Reyes et al., 2005; Borrero-Pérez et al., 2008; Benavides-Serrato et al., 2011). Among the most common ophiurans found attached to the coral branches is Ophiothrix (Acanthophiothrix) suensoni (fig. 4G). Currently, this location represents the only one in Colombia where five echinoderm species occur, the crinoids Coccometra nigrolineata and Stylometra spinifera and the brittle stars Asteroporpa (Asteroporpa)annulata, Ophiotreta valenciennesi and Ophiosyzygus disacanthus. The latter is also a first record for the Caribbean Sea, being previously reported for the Gulf of Mexico and the southwestern coast of Japan (Borrero-Pérez and Benavides-Serrato, 2004). In addition, it is important to highlight that the crinoid Endoxocrinus (Endoxocrinus) parrae, and the brittle stars Astrocnida isidis, Ophiothyreus goesi, Ophiopaepale goesiana, Ophiomitrella laevipellis, Ophiopristis hirsuta and Ophiomusa testudo have only been recorded in Madracis spp. coral patches located in the National Natural Park, La Guajira Peninsula (70 m depth) and Santa Marta (200 m depth) (Reyes et al., 2005). Other echinoderms species are typical of soft bottoms mixed with deep-sea corals, including the Asteroidea (Plutonaster agassizi agassizi) and Holothuroidea (Holothuria (Cystipus) occidentalis), some Ophiuroidea (i.e., Ophiomusa spp.) and most of the Echinoidea. Sea urchins are represented by five species of irregular echinoids in the orders Clypeasteroida and Spatangoida, with burrowers and detritivores habits. Regarding the ecology of this phylum, the crinoids and some brittle stars reported here are suspension-feeders (Gorgonocephalidae, Amphiuridae and Ophiothrichidae) (Birkeland, 1989; Hendler et al., 1995) and inhabit different microhabitats,  such as  buried in the muddy bottoms (i.e. Amphiuridae) or they may spend most of their life stages on larger organisms such as corals or crinoids stems, extending their arms to catch organic particles, like copepods and other microscopic organisms, as shown by Hendler et al. (1995) for Asteroporpa (Asteroporpa) annulata (fig. 4H).

Arthropoda (Crustacea)
This Phylum has a low diversity, with 4.2% of the total species found in this study. The infra-order Brachyura is one of the most successful groups of marine organisms worldwide. They can be found in all habitat types, from terrestrial to deep-sea (Ariza et al., 2008), although only a few species are present in the Madracis spp. coral patches. Key aspects for their success are perhaps the adaptation of their photoreceptors which allows most of them to be visually competent in a high variety of marine habitats, including deep-sea ecosystems (Frank et al., 2012) and their strictly benthic habits allow them to inhabit close within the coral framework of the colonies (Mastrototaro et al., 2010). One of the ecological features evidenced by crustaceans in the Madracis rubble is the presence of coral-symbiont predators such as the arrow crab Stenorhynchus seticornis Stenorhynchus yangi and the spider crab Pyromaia propinqua typically found in shallower reef environments (Lemaitre et al., 2009; Antunes et al., 2018) and in the case of Palicus sicus, that is the only species of the family Palicidae found in Colombia in substrates with a predominance of deep-sea corals at 200 m depth (Bermúdez et al., 2005).

Annelida
Even though polychaetes showed a low number of species in this study (13 species) they represented a high number of families (12 families), suggesting that community assessments at family level may be sufficient in marine biodiversity studies of this group (Olsgard et al., 2003). Their abundance was relatively high; most individuals were found in the soft sediment around the coral patch and others were directly associated with Madracis branches in a symbiotic interaction, as previously described by Lópezet al.(2008) for the families Eunicidae (Paramarphysa sp.) and Sabellidae (subfamily Fabricinae). Polychaetes are among the most diverse and perhaps the least studied taxa of coral symbionts (Molodtsova et al., 2016), especially in deep-sea coral communities. Recent studies suggest that these habitats are hidden hotspots for annelid diversity, with many species still undescribed (Molodtsova et al., 2016). They are commonly found associated with sponges, echinoderms, crustaceans, cnidarians, mollusks and even other polychaetes (Martin and Britayev, 1998) in shallower areas. Detritivorous worms such as Linopherus sp. Galathowenia sp. and Eclysippe sp. and the active predator Aglaophamus sp. are new records for the Colombian Caribbean. Commensalism is likely to be another common form of interaction between polychaetes and azooxanthellate corals (Morales de Anda, et al. 2014; Pitacco and Karhan, 2019). Close association and inter-relation of highly host-specific symbionts and cnidarian hosts often lead to dramatic changes in the host morphology (Molodtsova et al., 2016). A recently updated review on symbiotic polychaetes (Martin and Britayev, 2018) identified more than 600 species involved in symbiotic relationships, a number that has almost doubled since the most recent review on the topic 20 years ago (Martin and Britayev, 1998).

Brachiopoda
Brachiopods are not a remarkably diverse group of marine invertebrates in modern faunas. There are roughly 414 species worldwide (WoRMS, 2022). Although the Colombian Caribbean diversity of this group is low, the number of specimens collected suggests that brachiopods in the the Caribbean are probably more abundant offshore than previously thought (Rojas et al., 2009). Some of the species were found within the sediment samples, but it was evident that Madracis spp. coral patches has an important role as a habitat-forming species, lending support and colonization substrate to this type of organisms. Specifically, Tichosina plicata was observed attached to Madracis branches, and in a lower proportion than other corals (Rojas et al., 2022).

Chordata (Fish)
Among the fishes, most of the species are motile between the coral patches and the rocky macro-habitats that surround them. Demersal and bathydemersal species collected in the Madracis coral patches include common shallow-reef species such as Lipogramma evides, Pristigenys alta and Decodon puellaris, with the last two previously reported as new records for the Colombian Caribbean (Polanco et al., 2012). Species observed in video footage are benthopelagic representatives of some highly exploited commercial groups, such as jacks and groupers (fig. 5G). Also, puffers and some reef associated species such as Pristigenys alta, Serranus phoebe, Pterois volitans and Prognathodes guyanensis (fig. 6I) that arenewly recorded for the Colombian Caribbean were previously known from the Bahamas to Guyana and Venezuela (Robertson and Van Tassell, 2019). The presence of the lionfish, Pterois volitans, in these Madracis spp. coral patches is noteworthy. The lionfish is a species native to the Indopacific that was introduced in the Caribbean most likely through the aquarium industry via continuous escapes (Schofield, 2009). First documented in Florida reefs in 1985 (Schofield, 2009), in just a few years its populations expanded south throughout the Caribbean, with records in the Colombian Caribbean in 2009 (Gonzalez et al., 2009), and recent sightings in southern Brazil (Soares et al., 2023). Although lionfish are typically found in highest densities in shallow waters from 30 to 60 m depth (Andradi-Brown, 2019), recent studies have revealed that P. volitans has also moved into mesophotic environments in various regions of the Western Atlantic (Andradi-Brown, 2019; Luiz et al., 2021; Sanjuan-Muñoz et al., 2022), and it has even been observed in the upper bathyal zone (Gress et al., 2017). The remarkable adaptability of the lionfish to different habitats and diets has been key in their successful invasion (Cure et al., 2014), both geographically and bathymetrically. Their adaptability may therefore also account for their presence in Madracis spp. coral patches, as P. volitans tend to aggregate with conspecifics in habitats characterized by high structural complexity (Hunt et al., 2019). Our findings highlight the need to consider deep ecosystems with structural complexity in the management of this invasive species.

The scarce observation of fish in the video-transects is likely because they were easily disturbed by the submersibles, a bias that has previously been suggested to affect results in this type of survey (Trenkel et al., 2004).

Conclusions

The protection of Madracis spp. coral patches and their associated high diversity (eight phyla, 337 species) in the CPNNP has an important role in the conservation of marine diversity in the Colombian Caribbean Sea. These protected habitats host species that have only been found in this environment, such as five echinoderms and two cnidarians, plus new records of nine bryozoans, four genera of annelids, and the fish Prognathodes guyanensis for the Colombian Caribbean. Madracis spp. coral patches are also a refuge for large commercial fish species such as jacks and groupers, highly exploited by artisanal and industrial fisheries. The occurrence of a diverse suspension and filter-feeding invertebrate fauna (scleractinians, octocorals, bryozoans, brachiopods, bivalves, crinoids, ophiurans, and polychaetes) may be related to high availability and retention capacity of food particles supplied to these deep-sea habitats by local hydrodynamics.

Further surveys with advanced ROVs and multibeam bathymetry are strongly recommended to confirm the occurrence of additional patches of these diverse Madracis coral communities in the CPNNP. New research using cutting-edge technologies and targeted sampling will enhance our baseline knowledge by providing a better understanding of the extension and structure of the Madracis spp. coral patches, as well as aspects of the life history (growth and reproduction) of the main habitat-forming species, their associated fauna, and their possible links (connectivity) with both, shallow-coral reefs and other deep-sea communities in the region. Comprehensive investigations will facilitate the establishment of research priorities and targets for long-term monitoring, which, in turn, will strengthen the planning and management of this MPA.

Acknowledgements

This study has been possible thanks to the financial support of the Institute of Marine and Coastal Research-INVEMAR and the Instituto Colombiano para el Desarrollo de la Ciencia y la Tecnología (COLCIENCIAS) with the projects 'Macrofauna II' (code 210509-10401) and 'Marcoral' (code 2115-09-16649). Additional project PNN Corales de Profundidad (Agreement 291-14 ANH-INVEMAR) supported by the Parques Nacionales Naturales, Manchester University and the National Hydrocarbons Agency. Additional funds are from project GEF: GEF-UNDP-INVEMAR Project COL-00075241, PIMS # 3997 Design and implementation of National Subsystem of Marine Protected Areas (SMAP) in Colombia, co-funding by 14 national partners. These institutions supported the acquisition, analysis and identification of specimens, and facilitated technical equipment such as the multipurpose drift-cam (CADEM). To Venus Rocha for the map elaboration. We thank DIMAR for the bathymetric surveys and to the crew of SERPORT and technical staff of MARISCOPE for conducting the Diavolo II ROV surveys in 2015. David Alonso (Head of Biodiversity and Marine Ecosystems program-INVEMAR) for his constant efforts in the creation and support of research at CPNNP. We acknowledge the taxonomic expertise of many researchers that have built the collections of Makuriwa Museum along the years: Javier Reyes, Patricia Lattig and Isabel Chacón-Gómez (Cnidaria), Nestor Ardila, Paola Rachello, Inger Daniel and Erlenis Forntalvo (Mollusca), Alexis Rojas-Briceño (Brachiopoda), Gabriel Navas, Adriana Bermúdez, Norella Cruz and Paola Ariza (Crustacea), and Arturo Acero P., Luz Stella Mejia, Lina Saavedra, Adela Roa and Luz Marina Mejía (Pisces). To all of them and current members of the GTSEM team (Taxonomy, Systematics and Marine Ecology Research Group of INVEMAR) thanks for their collaboration and good friendship. We highly appreciate the technical support of Miguel Martelo in the management and care of the collections of Makuriwa Museum. NS thanks the Rutherford Fellowship granted by the UK Department for Business, Energy and Industrial Strategy-BEIS. Contribution No. 1358 of the Marine and Coastal Research Institute–INVEMAR. Also, thanks to the reviewers for their helpful comments and suggestions.

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