New records of benthic marine macroalgae from the Caribbean coast of Costa Rica

Marine macroalgae are highly diverse and play an important role in marine ecosystems, influencing ecological processes. Recording the algae diversity with precise taxonomic identification is required to understand the marine ecosystems. The biodiversity of macroalgae along the southern Caribbean coast of Costa Rica has been studied by several authors, and the updated checklist includes 396 species of benthic marine algae reported for both Pacific and Caribbean coasts of Costa Rica, from which 287 are recorded from the Caribbean. Eighty percent of the total specimens from the Caribbean coast deposited in botanical collections in Costa Rica were collected at Cahuita National Park, an area where most of the studies have been carried out. This study reports on the addition of five new species and one genus of marine benthic macroalgae to the Caribbean Costa Rican flora, found at the poorly studied reefs of Playa Chiquita (Punta Cocles) and Punta Uva. Sampling was directed, searching for benthic macroalgae at Chiquita beach (SCUBA diving and snorkel) and Punta Uva (snorkel only), during October 2014. Specimens were deposited in the Dr. Luis A. Fournier Origgi Herbarium of the University of Costa Rica (USJ). Most of the new records were Chlorophyta, followed by Rhodophyta and Ochrophyta-Phaeophyceae. We recorded four new genera for the Caribbean coast of Costa Rica: Microdictyon Decaisne, 1841, Rhipidosiphon Montagne, 1842, Predaea G. De Toni, 1936, and Augophyllum S.-M. Lin, S. Fredericq & M. H. Hommersand, 2003. In conclusion, is necessary to continue the detailed taxonomic works in the Caribbean coast, focusing on areas poorly studied, in order to improve our knowledge of the marine flora of Costa Rica. Rev. Biol. Trop. 66(Suppl. 1): S328-S339. Epub 2018 April 01.

Marine macroalgae are a highly diverse group including different phyla and thousands of described species.These organisms play an important role in marine ecosystems as primary producers in littoral food webs and act as refuges for fish and invertebrates (Fletcher, 1987;Hay, 1981;Ruitton, Francour, & Boudouresque, 2000).A better understanding of the identity and richness of macroalgae species is a first step for studying ecological processes, such as competition, nutrient flux, and biotic interactions.Recording the biodiversity with precise taxonomic identifications improve efforts to understand ecosystem functioning and the development of management tools (Bruno, Boyer, Duffy, Lee, & Kertesz, 2005;Costello, Michener, Gahegan, Zhang, & Bourne, 2013).
The first records of marine macroalgae from the southern Caribbean coast of Costa Rica were made by Taylor (1933Taylor ( , 1942Taylor ( , 1960)), Dawson (1962) and Wellington (1973Wellington ( , 1974)).Later, Soto (1983), Soto & Ballantine (1986), and Kemperman & Stegenga (1986) provided the first comprehensive check lists of macroalgae.Then, Thomas & Freshwater (2001) reviewed some species from the Order Gelidiales and reported on two new species.Fernández & Alvarado (2004) later described the coral reef from Punta Cocles, including a list of the associated macroalgae.Then, Bernecker (2009) and Bernecker & Wehrtmann (2009) published an updated list of the macroalgae from both the Caribbean and Pacific coasts of Costa Rica.There are 396 species of benthic marine algae reported for both Pacific and Caribbean coasts of Costa Rica (84 Chlorophyta or green algae, 51 Ochrophyta-Phaeophyceae or brown algae, 1 Xanthophyceae or yellow-green algae, and 260 Rhodophyta or red algae), from which 287 are recorded from the Caribbean coast (Bernecker, 2009).Fernández & Alvarado (2004) found high coverage of macroalgae (up to 59 %) at Punta Cocles reef, being the brown algae the predominant group (Dictyota sp., Sargassum sp., Padina sp., and Dictyopteris delicatula J.V.Lamouroux).
Considering the records at the two main herbaria of Costa Rica -Dr.Luis A. Fournier Origgi Herbarium of the University of Costa Rica, and National Herbarium of Costa Ricathe Caribbean coast was relatively well sampled between 2000 and 2007, however there are no records for macroalgae collections from 2007 to 2014.Moreover, 80 % of the total specimens from the Caribbean coast deposited in these two herbaria were collected in the Costa Rica's largest fringing reef at Cahuita National Park, where most prior studies have been carried out.However, other coral reef areas at the southern Caribbean, like Moín-Isla Uvita and Puerto Viejo-Punta Mona, have been far less studied.This study aims to report on the addition of six new marine benthic macroalgae records to the flora of Caribbean Costa Rica, found at the coral reefs from the Puerto Viejo-Punta Mona area.

Sample collection:
Sampling was directed, searching for benthic macroalgae at Chiquita beach (SCUBA diving and snorkel) and Punta Uva (snorkel only), during October 2014.Seaweeds were stored in vials with 4 % formalin, and transported to the laboratory of Phycology at Centro de Investigación en Ciencias del Mar y Limnología (CIMAR-UCR).Vouchers were deposited in the Dr. Luis A. Fournier Origgi Herbarium of the University of Costa Rica (USJ), San José, Costa Rica.Samples were collected under sampling permit (No.SINAC-SE-GCUS-PI-R-082-2015) provided by SINAC-MINAET.

RESULTS
Based on morphological analysis, a total of five new macroalgae species and one new genus were recorded representing six families, five orders, and three classes; from Chlorophyta, Ochrophyta and Rhodophyta (Table 1).Here, we provide a brief description of the collected specimens, including USJ voucher number, habitat, distribution recorded in Costa Rica and some illustrative figures.
Habitat: On dead coral, mixed with Dictyota sp.
Voucher USJ: 73887.Habitat: Growing as large mats on coral reefs.Found at less than 1m to 5m deep.
Habitat: Found at 4 m depth.
Habitat: On coral reef substrate and in sand plains.Found from 7 m to 10 m deep.

DISCUSSION
The six new records increased the diversity of Caribbean Costa Rican seaweeds by 1.9 % over that previously reported by Bernecker & Wehrtmann (2009).Four new genera were recorded for Caribbean Costa Rica: Microdictyon, Rhipidosiphon, Predaea and Augophyllum.Although the majority of these new records were Chlorophyta, followed by Rhodophyta and Ochrophyta-Phaeophyceae they did not change the proportions of this groups within the total flora, where Rhodophyta is the most specious group.This overall pattern is found in all Central American countries (Bernecker & Wehrtmann, 2009) and is typical for tropical regions (Strasburger, Noll, Schenck, & Schimper, 1997).
We found a large mat of A. digitata extending on the reef, although we did not measured its extension, although it spanned for more than 10 m 2 .In its original description, A. digitata was mentioned to present colonies up to 13 cm thick, and large mats of fronds were typically found at shallow waters, <1 m (Littler & Littler, 1992).Siphonal green algae possess a blade abandonment strategy linked to rapid proliferation processes, allowing these algae to dominate standing stocks in most calm-water reef habitats in the Caribbean (Littler & Littler, 1999).However, some siphonal green algae have shown an invasive behavior.For example, Avrainvillea amadelpha (Montagne) A. Gepp & E. S. Gepp, 1908 was first recorded in the Hawaiian archipelago in 1981, were Avrainvillea algae were recorded uncommon in the 50's and 70's, and appeared to spread from a small patch to several localities (Brostoff, 1989;Doty, Gilbert, & Abbott, 1974).A. amadelpha is currently a highly successful invasive species in Hawaii, competing with native species such as Halophila hawaiiana Doty & B. C. Stone, 1966(Smith, Hunter, & Smith, 2002).Recently, A. amadelpha was first recorded in the Mediterranean Sea (Verlaque, Langas, Hmida, Pergent, & Pergent, 2017).The proliferation of this Avrainvillea mats have shown effects on the above-ground polychaete communities (Magalhães & Bailey-Brock, 2014).Since this species have not been previously recorded nor its siphonal mats in these reefs (Fernández & Alvarado, 2004), we suggest to keep a close monitoring on A. digitata coverage and its interactions with other benthic components.
We found some patches of T. tricostata extending for several meters in the reefs of Playa Chiquita and Punta Uva.During previous visits at these reefs, we did not find this patches, therefore we suspect certain seasonality on the occurrence of T. tricostata that should be studied.In a nearby reef, other brown algae, Sargassum sp., do also occur in patches of several meters (Fernández & Alvarado, 2004).Brown algae, such as Turbinaria, tend to dominate on rocky substrates at Cuban reefs (Zayas, Suárez, & Ocaña, 2002).Turbinaria algae have shown seasonal variation in Sardinero, Justicí and Baconao reefs at Cuba, appearing only during the dry season (Jover, Reyes de Armas, Gómez, & Suárez, 2012).
Augophyllum wysorii was found at shallower depths (4 m) than had been previously recorded, 12-15 m (Lin et al., 2004).This specie has a very restricted known distribution (Galeta STRI-Research Station, Colon, Panama) and therefore this Costa Rican record contributes to knowledge of the species range and habitat.
The Predaea sp. was found at a shallower depth than most of the Predaea species previously reported in the Caribbean (Ballantine & Wynne, 1986;Delnatte & Wynne, 2016;Gabriel, Schills, Neto, Paramio, & Fredericq, 2009;Littler & Littler, 2000;Rodríguez-Prieto, Michanek, & Ivon, 1999).Although it is not possible to reach a species level with the observed morphological characteristics, it is probable that the species found corresponds to Predaea feldmannii Børgesen, 1950, a species recently described near to the Caribbean coast of Costa Rica (Gabriel et al., 2010).
This study found five new macroalgae species and one new genus during a short sampling period at two poorly studied localities.Further taxonomic studied including multiple localities and environments will likely reveal and even higher species richness along the Caribbean coast of Costa Rica.A detailed record of this biodiversity is necessary to improve future efforts in management and conservation.Biodiversity records also facilitate the quick detection of invasive species.Moreover, marine biodiversity is increasingly threatened by anthropogenic and natural impacts, and therefore we should improve our efforts to properly record it (Worm et al., 2006).
In addition, new herbarium records allow comparative studies, provide locality data for planning field trips, material for morphological observation, and serve as voucher specimens.Molecular analysis had been proven as an important tool for accurate identification of cryptic species of algae, e.g.Dictyota (Tronholm et al., 2013).Therefore, further studies using molecular analysis will be needed to improve our knowledge on the Costa Rican marine flora.Currently, we are trying to carry out molecular analysis in order to complement the results of the present study.In conclusion, this study provides six new records of marine macroalgae, increasing the known diversity of the Caribbean coast and provides important information for future ecological and taxonomy studies.

Fig. 1 .
Fig. 1.Sampling localities of benthic marine macroalgae at Southern Caribbean coast of Costa Rica.

TABLE 1
Taxonomy of the new records found in the southern Caribbean of Costa Rica