Macroalgae associated with aerial roots of Rhizophora mangle in Islas del Rosario, Colombia, Southwestern Caribbean Macroalgas asociadas a las raíces aéreas de Rhizophora mangle en las Islas del Rosario, Colombia, Caribe suroccidental

The roots of the red mangrove, Rhizophora mangle, provide a nursery habitat for many species, due to the tridimensional structure they provide, which delimits an area difficult to access to large predators. Moreover, they provide a hard substrate for many benthonic species, which attach to the roots and contribute to the tridimensional structure of the ecosystem. Among these organisms, there are several macroalgae, which contribute to the primary productivity of the ecosystem and provide food and shelter to herbivores. In the present study we identified the macroalgae associated with the roots of Rhizophora mangle, in Cholón beach, Rosario Islands National Park, Caribbean Colombia. We report a total of 36 species of macroalgae: 21 Rhodophyta, eleven Chlorophyta, and four Phaeophyceae. Of these, 19 are new records for the islands, and six are new records for Colombia. This is the first study on the macroalgae associated with mangrove roots in the Colombian Caribbean, and it highlights both the high diversity of the marine flora of the Southwestern Caribbean, as well as the paucity of studies on the topic.


INTRODUCTION
Mangrove forests are tropical coastal ecosystems with a very high productivity and a complex food web, which support a great variety of organisms (López et al. 2009) and provide many ecosystem services. The aerial roots of the red mangrove, Rhizophora mangle L., provide a hard substrate in an area usually devoid of it, and form a threedimensional habitat for sessile invertebrates and algae, as well as a refuge for juveniles of mollusks, crustaceans, and fish (Guerra-Castro and Cruz-Motta 2014, Ruiz- Guerrero and López-Portillo 2014).
The food web in this habitat has long been assumed to be based on detritus derived from mangrove litter (Odum and Heald 1972, Lugo and Snedaker 1974, Saifullah and Ahmed 2007. However, it has been proved that the algae on the prop roots may equal or surpass the primary productivity of mangrove trees (Rodriguez and Stoner 1990), and the macroalgal-derived detritus is exported from mangrove forests to adjacent ecosystems.
There is a plethora of studies on macroalgal communities associated with mangrove prop roots (i.e. Coppejans and Gallin 1988, Akil and Jiddawi 2001, Youseef et al. 2004, Schaffelke et al. 2005, Satpati et al. 2013, Shamina et al. 2014) around the world. In the Caribbean, the phytocenosis associated with mangrove roots is species-rich (López et al. 2009), and this has been attributed to water transparency and the stability of salinity and temperature year-round . At present, there are no studies on the macroalgal flora associated with mangrove roots along the Caribbean coast of Colombia , despite the great extension of mangrove forest (54 010 hectares, INVEMAR 2019) the region harbors. We present the first study on the macroalgae epiphytic on aerial roots of Rhizophora mangle L. at Cholón beach, Islas del Rosario National Park, Colombia.

MATERIAL AND METHODS
The National Park of Rosario Islands (10°8´-10° 15´North, 75°40´-75°48´West) is a protected area with an extension of about 120 000 hectares. The protected area harbors the most iconic coastal ecosystems of the Caribbean, including seagrass beds, coral reefs, mangrove forests and rocky shore habitats.
The region faces two rainy periods (May-June and October-November) and two dry periods (December-April and July-September). The mean temperature is 27.7 °C, and the relative humidity reaches 80-85 % (Valle et al. 2011).
The study site is in a small island on the west side of the Baru island ( Fig. 1), facing a coastal lagoon, which RESUMEN Las raíces de Rhizophora mangle proveen un hábitat de guardería para muchas especies debido a la estructura tridimensional que forman, lo cual delimita un área de difícil acceso para depredadores grandes. Adicionalmente, proveen un sustrato duro para muchas especies bentónicas, que se atan a las raíces y contribuyen a la estructura tridimensional del ecosistema. Entre esos organismos, encontramos varias macroalgas, que contribuyen a la productividad primaria del ecosistema y proveen alimento y refugio a los herbívoros. En el presente estudio se identificaron las macroalgas asociadas a las raíces de Rhizophora mangle, en playa Cholón, en las islas del Rosario, Caribe colombiano. Se reportan 36 especies of macroalgas: 21 Rhodophyta, once Chlorophyta y cuatro Phaeophyceae. De esas 36 especies, 19 son nuevos registros para las islas, y otros seis son nuevos registros para Colombia. Este es el primer estudio sobre las macroalgas asociadas a las raíces de manglar en el Caribe colombiano, e ilustra tanto la alta diversidad de la flora marina en el Caribe suroccidental, como la falta de estudios sobre el tema.

Palabras clave. Bostrychia, Ceramium, diversidad, epifitos, Rhodophyta
communicates with the open sea through shallow channels (UAPNN 1998). The area is under the influence of the Dique Channel, which brings part of the freshwater and sediments of the Magdalena River, the main river in Colombia and the Caribbean basin. Salinity ranges between 32.2 and 33.0 ppt.
Three aerial roots of R. mangle were collected in September 2014, less than 50 m apart, and preserved in a 4 % formalin/seawater solution. In the laboratory the roots were analyzed, measured and photographed (Fig. 2a). The algae were removed, and their zonation on the root was recorded, dividing the root in sections of 5 cm (Coppejans and Gallin 1988). Algae were identified using an Olympus BX50 light microscope connected to a Moticampro 282B.
Nomenclature of the algal species follows Wynne (2017) and Guiry and Guiry (c2020). Voucher specimens were deposited in the herbarium of the Biology Department, Universidad Nacional de Colombia.

RESULTS
We report a total of 36 species: 21 species of Rhodophyta, four Phaeophyceae and eleven Chlorophyta ( Table 1) We found that some species (Bostrychia montagnei, Ceramium brevizonatum var. caraibicum, Hypnea spinella (C.Agardh) Kützing, Dictyopteris delicatula J.V.Lamouroux, Bryopsis hypnoides J.V.Lamouroux and Bryopsis pennata J.V.Lamouroux) were restricted to the upper portion of the root. In the middle part of the root we observed Antithamnion antillanum Børgesen and Laurencia sp., while Hypnea valentiae (Turner) Montagne and Parviphycus setaceus were restricted to the deeper portion of the root. All the other taxa did not have a clear pattern of distribution; they were observed along the whole length of the root.

DISCUSSION
The number of algae registered in the present study is rather high if compared to previous works: El-Sharouny The diversity that we observed is close to that reported from the studies carried out by Moreira et al. (2003), who  new findings reflect the lack of studies, rather than new introductions to the area.
The genus Bostrychia, together with the genera Murrayella, Caloglossa and Catenella, form the Bostrychietum, an association of specialized red algae that grows on roots of different species of mangroves (Seixas et al. 2014). The presence of the species B. montagnei in this environment is therefore not surprising. To date, for the The taxon Ceramium brevizonatum var. caraibicum, originally described for Dominican Republic (Hispaniola island, Børgesen 1924) has been widely reported for all the Caribbean Sea from Bermuda to Brazil as well as at some localities in the Indian Ocean (Guiry and Guiry c2020). The genus Dasya C. Agardh (1824) includes red algae with a hairy and delicate appearance and rigid to flaccid texture. The genus currently includes over 90 species distributed in sub-polar, temperate and tropical seas (Guiry and Guiry c2020), nineteen of which are reported for the Western Atlantic (Wynne 2017). Dasya caraibica, originally described by Børgesen (1919), is one of the two species reported for the Caribbean with light rhizoidal cortication (Fig 3b). Dasya rigidula (Kützing) Ardissone, the other lightly corticated taxon, differs mainly in   (Fig. 3a).

Melanothamnus pseudovillum, originally described as
Polysiphonia pseudovillum by Hollenberg (1968) is a creeping species with closed-connected rhizoids, four pericentral cells, ecorticated, and branches replacing trichoblasts. In the Western Atlantic it has been reported for North Carolina (Schneider and Searles 1991), Florida (Littler and Littler 2000), Parviphycus setaceus is a species originally described for the Antilles (Guiry and Guiry c2020) and widely distributed in the Caribbean Sea (as Gelidiella setacea (Feldmann) Feldmann and Hamel, Littler and Littler 2000). It is typically observed on mangrove prop roots Littler 2000, Littler et al. 2008), where it grows inconspicuously.
Wittrockiella salina Chapman is a species originally described for New Zealand and distributed along Australia, Tasmania, and Japan, in the Pacific Ocean. In 1984 van den Hoek et al. (1984) reported the species as epiphytic on aerial roots of Rhizophora mangle and on pneumatophores of Avicennia nitida Jacq. on the island of Curacao, Netherland Antilles, in the Southern Caribbean Sea. The alga is small, inconspicuous, grows as an epiphyte on larger algae, so it may go easily undetected. It is difficult to determine if this species has been introduced in the Caribbean Sea, and expanding, or if mangrove aerial roots in the southern Caribbean basin have always been its natural environment. Although the overall diversity of the biocenosis associated with mangrove prop roots is high (e.g. Riosmena-Rodriguez et al. 2011), single studies seldom report a high number of species. Some authors have regarded mangrove habitats as having a low diversity of epiphytes (Huisman et al. 2015); King (1981) suggested that these habitats are unfavorable due to a lack of stable substratum (excluding the mangroves), mud in suspension, and the physiological stress due to fluctuating salinity. Riosmena-Rodriguez et al. (2011) associated a high diversity of algae on mangrove roots to the presence of other habitats close-by, such as seagrass or rhodoliths beds and hard substrate such as rocky shores. When these habitats are not present, the algal diversity is much lower. In Cholón, the mangroves were adjacent to seagrass beds, and coral reef patches were observed in the area. Furthermore, artificial hard substrate is present close by in the form of spurs.
Considering that we analyzed only three roots, the diversity of this phytocenosis in the Park is grossly underestimated. Most species are microscopic, filamentous, and easily overlooked. Furthermore, for red algae, the reproductive structures are needed to be able to identify the sample to species. More research is needed to understand if stochastic events are structuring the epiphytic flora on single roots, or if other factors are involved. Eston et al. (1992) determined that on mangroves, early algal colonizers are also the final community, with no opportunistic species present and virtually no succession, as it has been reported for seagrass communities (den Hartog 1971(den Hartog , 1987.  reported that for the Caribbean basin, the phytocenosis associated with mangroves was dominated by green algae. In our study, 59.4 % of the species belonged to Rhodophyta, 29.7 % were Chlorophyta and only 10.8 % were Phaeophyceae. These percentages correspond to the average composition of the marine flora in the Caribbean (e.g. Taylor and Rhyne 1970, Betancourt-Fernandez and Herrera-Moreno 2001, Suárez 2005. Diaz-Pulido and Díaz-Ruiz (2003) reported, for the Rosario islands, a marine flora dominated by red algae (50.8 %) followed by green algae (39.7 %) and then brown algae (9.3 %). For the mangrove roots, we report a higher percentage of red algae, which also corresponds to the majority of the new records. Recent studies on the seaweeds of another region of the Colombian Caribbean (e.g. Albis-Salas and Gavio 2011, Ortiz and Gavio 2012, Gavio et al. 2013, Rincón-Díaz et al. 2014, registered a high number of red algal species previously overlooked.

Cordeiro
The The high diversity observed supports the importance of this community to the food web of mangrove ecosystems. This study by no means pretends to be comprehensive; considering the mangrove cover along the Caribbean coast of Colombia, more research is needed to address algal species diversity, distribution, seasonality and turn-over, to better understand the dynamics shaping these habitats.

ACKNOWLEDGEMENTS
The samples were collected during a field trip financed by the Facultad de Ciencias, Universidad Nacional de Colombia, sede Bogotá. We thank Johanna Paola Echeverry Hernández for her help in elaborating the map, and two anonymous reviewers to help improve the manuscript. The present contribution is part of the project codigo Hermes No. 33153.

AUTHORS PARTICIPATION
CESF collected the samples, identified the specimens, and wrote the manuscript. BG identified the specimens and wrote the manuscript. MJW identified some specimens and wrote the manuscript.