The sea anemone Exaiptasia diaphana (Actiniaria: Aiptasiidae) associated to rhodoliths at Isla del Coco National Park, Costa Rica

Introduction: The sea anemones diversity is still poorly studied in Isla del Coco National Park, Costa Rica. Objective: To report for the first time the presence of the sea anemone Exaiptasia diaphana. Methods: Some rhodoliths were examined in situ in Punta Ulloa at 14 m depth, by SCUBA during the expedition UCRUNA-COCO-I to Isla del Coco National Park on 24th April 2010. Living anemones settled on rhodoliths were photographed and its external morphological features and measures were recorded in situ. Results: Several individuals of E. diaphana were observed on rodoliths and we repeatedly observed several small individuals of this sea anemone surrounding the largest individual in an area (presumably the founder sea anemone) on rhodoliths from Punta Ulloa. Conclusions: The geographic distribution is extended as well as their bathymetric distribution from the intertidal to 14 m depth. The photographs provide evidence of clonal reproduction by pedal laceration.

The marine biodiversity of Isla del Coco has been the subject of scientific interest particularly for its biogeographic relevance and diversity. A list of published records of the marine organisms found in the area has been compiled by Cortés (2012). The growing interest in these investigations has been demonstrated in the recent International Symposium on Isla del Coco held in February 2018 at the University of Costa Rica. Although there have been many studies on different invertebrate groups, the sea anemones (order Actiniaria) diversity is still poorly studied. In fact, only two species of sea anemones have been recorded for the island, Telmatactis panamensis (Verrill, 1869) (Acuña, Cortés, & Garese, 2012), and Anthopleura nigrescens (Verrill, 1928) (Acuña, Garese, Excoffon, & Cortés 2013). During the expedition UCR-UNA-COCO-I to Isla del Coco National Park in April 2010, we sampled many sites including a rhodolith bed at 14 m depth, in Punta Ulloa. The rhodoliths constituted a benthic community dominated by free-living calcareous algae that can roll over the substrate pushed by the movement of water currents. Rhodoliths are one of the groups of algae with the widest geographical, climatic and bathymetric distribution and they are considered as bioengineers due to their propensity to construct a hard and complex substrate with hollows and sinuosities, which favors the settlement of numerous species and the development of various microhabitats (Foster, Amado-Filho, Kamenos, Riosmena-Rodríguez, & Steller, 2013;Mallol, Barberá, & Goñi, 2015). The sea anemone Exaiptasia diaphana (Rapp, 1829) (= Exaiptasia pallida) was observed among the species associated to the rhodoliths. This paper documents the association and constitutes the first record of this actiniarian in the Isla del Coco National Park.

MATERIAL AND METHODS
Several rhodoliths were examined in situ in Punta Ulloa at 14 m depth, by SCUBA during the expedition UCR-UNA-COCO-I to Isla del Coco National Park on 24 th April 2010. Living specimens of sea anemones settled on rhodoliths were photographed and its external morphological features and measures were recorded in situ. Identification of observed specimens were made following Fautin, Cleveland, Hickman, Daly, and Molodtsova (2007) and Grajales and Rodríguez (2014). The synonymies follow Grajales and Rodríguez (2014), and Daly and Fautin (2018). Characteristics of studied specimens of Exaiptasia diaphana: All taxonomic diagnostic features and measures observed in the specimens examined agree very well with those of the external anatomy described for Exaiptasia diaphana: oral disc from a few to 20 mm in diameter. Pedal disc regularly shaped, wider than column. Column elongated, smooth, not distinctly divisible into scapus and capitulum, translucent with scattered spots distally, mesenterial insertions visible as light lines in some individuals, whitish on the distal end (Fig. 1B). Oral disc brown, translucent, mouth white encircled with a brown ring, mesenterial insertions visible through oral disc as dark lines (Fig. 1C). Tentacles simple, smooth, long, slender, tapering toward tips, occurring only at margin and in variable in number, same color than oral disc, some have white transverse bars around its base or on its oral face (Fig. 1C).

Classification
Natural history: Exaiptasia diaphana can reproduce asexually by pedal laceration, in which the animal is subdivided into generating clones that separate from small portions of the pedal disc (Clayton, 1985). We repeatedly observed several small individuals of E. diaphana surrounding the largest individual in an area (presumably the founder sea anemone) on rhodoliths from Punta Ulloa (Fig. 1D). Based on these observations, we suggest that smaller individuals were clonally produced by pedal laceration of the founder individual.

DISCUSSION
Rhodoliths constitute particular microhabitats that host numerous species of invertebrates. Recent studies on rhodoliths in Isla del Coco have shown a great diversity of invertebrate taxa associated (one hundred and forty five taxa were found), among which the more diverse were polychaetes, arthropods, and mollusks, although crustaceans represent more than the half of the total number of organisms (Solano-Barquero, Sibaja-Cordero, & Cortés-Núñez, 2018). However, other organisms, such as various groups of cnidarians have been recorded but not identified to the species level. In this work we report for the first time the presence of sea anemone Exaiptasia diaphana for Isla del Coco National Park associated with rhodoliths in a subtidal bed. This species belongs to the family Aiptasiidae whose taxonomy was recently revised by Grajales and Rodríguez (2014), including the erected new genus Exaiptasia.
The species E. diaphana was present in many rhodoliths from Punta Ulloa, reaching in many cases more than ten individuals per rhodolith (Fig. 1D), presumably as a result of clonal reproduction by pedal laceration. This type of asexual reproduction is characteristic of this species, even though longitudinal fission has also been reported (Clayton, 1985). The reproduction rate by pedal laceration is very high, so this species can easily become a plague to other organisms such as corals or sponges. In addition, this species reproduce sexually by the release of gametes, external fertilization and the formation of a free swimming planula larvae (Clayton, 1985). This mode of reproduction could facilitate its dispersal to other habitats including other rhodoliths in the same bed or even further away. The presence of anemone E. diaphana in rhodoliths has been reported (as Aiptasia californica) by King (2003) for other localities such as Bahía Concepción (Baja California, Mexico). King (2003) and others (Geller, Fitzgerald, & King, 2005) performed interesting experiments involving rhodoliths' movement as an inducer of pedal laceration. Since rhodoliths and their associates are vulnerable to climate change and other anthropogenic disturbances (McConnico, Hernández-Carmona, & Riosmena-Rodríguez, 2018), similar studies and others related to different aspects of anemone ecology in rhodoliths will allow a better understanding of the role of these algae and their importance in different marine ecosystems.
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.

ACKNOWLEDGMENTS
We are grateful to Jaime Nivia for collecting the rhodoliths during the dives and for images.