Euphausiids ( Crustacea : Euphausiacea ) from a hotspot of marine biodiversity , Isla del Coco , Costa Rica , Eastern Tropical Pacific

Euphausiids have been well studied in several regions of the Pacific Ocean; however, there is less information regarding euphausiids in Costa Rican waters. We analyzed euphausiid specimens collected around Isla del Coco National Park during 2011 and 2012. A total of 130 specimens were analyzed and 13 euphausiid species were identified, belonging to four genera and one family. An annotated list of species is presented, with photographs and details for their identification. All species found represent new records for waters around Isla del Coco in the Costa Rican Pacific. The most frequent species were Euphausia diomedeae, Euphausia distinguenda, Nematoscelis gracilis and Stylocheiron affine. Rev. Biol. Trop. 64 (Suppl. 1): S221-S230. Epub 2016 Febrary 01.

Euphausiids (also known as krill) are a group of shrimp-like holoplanktonic crustaceans that inhabit all oceans (Baker, Boden, & Brinton, 1990;Everson, 2000).They are an important part of the energy transfer between trophic webs of marine ecosystems, being effective phytoplankton grazers and preyed upon by diverse organisms including large invertebrates, fishes, sea birds, seals and whales (Mauchline, & Fisher, 1969;Takashi, 1983;Williams, 1985;Agersted, Nielsen, Munk, Vismann, & Arendt, 2011).Their carcasses and fecal pellets transport organic matter to deep waters and sediments (Wheeler, 1967;Fowler, & Small, 1972).Euphausiids may also affect the fisheries of other organisms, for example Pauly, Christensen, Dalsgaard, Froese & Torres (1998) mentioned that overfishing of the Norway pout (Trisopetrus esmarkii), a krill predator, could lead to an increase of euphausiid abundance, which in turn prey on copepods, an important food source for other commercial fishes, such as cod and saithe.Recently, large-scale commercial krill fisheries have been developed in South Atlantic along the Antarctic Peninsula, off the Japanese coast, and off the coast of British Columbia (Nicol, & Endo, 1997).Euphausiids have specific distributional patterns associated with distinct water masses, and thus are used as indicators of oceanographic environments (Brinton, 1981;1996;Lavaniegos, Lara-Lara, & Brinton, 1989;Lavaniegos, 1994).
Despite the extensive research on euphausiids from the ETP, there is less specific information regarding euphausiids in the Costa Rican Pacific and Isla del Coco (Castellanos, Suárez-Morales, & Morales-Ramírez, 2009).It is important to fill the gaps on taxonomic and diversity knowledge in marine ecosystems to identify and understand the economic and ecological relevance that these organisms might have on several oceanic areas (Costello et al., 2010).Regional checklists of marine species are also important tools for recognizing and delimiting areas in need for protection (Hendrickx, & Harvey, 1999).The present study is the first attempt to record the euphausiid species around Isla del Coco.

MATERIALS AND METHODS
Isla del Coco (also known as Cocos Island) is located in the ETP, and represents the core of the Isla del Coco Marine Conservation Area (Fig. 1), declared UNESCO World Heritage in 1997 and RAMSAR site in 1998 (Cortés, 2008).The island is located ~500km southwest of Cabo Blanco, Costa Rica, and it is the only exposed point of the Coco Cordillera (Castillo et al., 1988;Rojas, & Alvarado, 2012).The waters around Isla del Coco are influenced by the seasonal movement of Inter-Tropical Convergence Zone (Broenkow, 1965;Alfaro, 2008), periodic El Niño events (Fiedler, & Talley, 2006), and even the seasonal upwelling in the Gulf of Papagayo (Lizano, 2008).Physicochemical analyses from waters around Isla del Coco revealed influence from both coastal and oceanic waters (Acuña, García, Gómez, Vargas, & Cortés, 2008).
In order to describe the zooplankton community from Isla del Coco, two oceanographic expeditions were carried out in March 2011 and June 2012 aboard the MV Argo and MV Undersea Hunter, respectively.For a more detailed explanation of the two oceanographic expeditions see Brenes et al. (2011) and Cortés et al. (2012).A total of 35 stations in March 2011 and 25 in June 2012 were sampled around Isla del Coco.In this paper we present results from eight of them (one from 2011 and seven from 2012) (Fig. 1).
During both oceanographic expeditions, zooplankton samples were collected using a standard General Oceanics net (202μm mesh, 50cm diameter, 1.5m length) towed vertically from 100m and 200m deep to the surface in 2011 and 2012, respectively (Table 1).All the zooplankton samples were preserved in seawater with 4 % formalin and transported to the Zooplankton Laboratory at CIMAR, UCR.Only adult euphausiid specimens were separated from the samples, counted and identified following Baker et al. (1990) and Brinton, Ohman, Townsend, Knight & Bridgeman (2000).All the specimens were deposited in the crustacean collection at the Zoology Museum, University of Costa Rica (Museo de Zoología, Universidad de Costa Rica, MZUCR).

RESULTS
A total of 130 specimens were analyzed.The present study reports 13 krill species, distributed in four genera, all belonging to the family Euphausiidae (Table 2; Figs. 2, 3, 4).All the species are new records for Isla del Coco in the Costa Rican Pacific.The most frequent species were Euphausia distinguenda, Euphausia diomedeae, Nematoscelis gracilis and Stylocheiron affine, with more than 10 specimens.

DISCUSSION
The 13 euphausiid species found in Isla del Coco were previously recorded in the ETP   and waters near Costa Rica by the "Shellback" expedition in 1952 (Brinton, 1962).Sameoto et al. (1987) reported 17 euphausiid species near the Costa Rica Dome outside the Economic Exclusive Zone of Costa Rica (Fig. 1).The higher species richness reported for the Costa Rica dome is probably related with the depth range sampling (0-1000m depth) and technique (multiple opening and closing net) (Sameoto et al., 1987), while this study only analyzed samples from 200m and 100m depth using a standard net.Only 65 % of euphausiid species found in Costa Rica Dome are reported for Isla del Coco.Moreover, Euphausia tenera and Nematoscelis tenella were not reported by Sameoto et al. (1987) from the Dome station; however, both species were collected in the BIOSTAT station (off Central American coast).The euphausiid species assemblage of Isla del Coco should be determined by the particular oceanographic dynamics surrounding the island (Broenkow, 1965;Fiedler, & Talley, 2006;Acuña et al., 2008;Alfaro, 2008;Lizano, 2008).Brinton (1979) grouped the euphausiids from ETP by biogeographic and hydrographic affinities.The non-migrating warm cosmopolites are N. tenella, S. affine, Stylocheiron carinatum, Stylocheiron longicorne and Stylocheiron maximum.The species that proliferate in the north and south margins of ETP are Euphausia eximia, Nematobrachion flexipes and Euphausia gibboides.These species are found in the low oxygen layer, but are more abundant in its margins.The equatorial endemic species are adapted to migrate into the low oxygen layer.This group includes E. diomedeae, E. distinguenda, Euphausia lamelligera and N. gracilis.Finally, E. tenera is a widely distributed species, thus it was not included in any group by Brinton (1979).We emphasize that the most common species in the present study were mainly from the equatorial endemics group (E.distinguenda, E. diomedeae and N. gracilis), and S. affine, a non-migrating warm cosmopolite species that can also be found through the low oxygen layer.
Although this is the first effort to record the euphausiid diversity from Isla del Coco, samples from deeper waters are needed to found deep-water distributed species reported for Central American waters (Brinton, 1962;1979;Sameoto et al., 1987;Castellanos et al., 2009).Moreover, information regarding the vertical distribution, ecological relationships, and temporal patterns of species composition is still needed to understand the dynamics of krill, which might be an important component for ecosystems and fisheries in Costa Rican waters.Therefore, our future goal is to assess the euphausiid community diversity and ecology in the Costa Rican Pacific waters, and we are currently preparing an ecologically focused work.

ACKNOWLEDGMENTS
We are very grateful with Octavio Esquivel and Fabiola Jiménez who collected the zooplankton samples and Keats Conley for her linguistic revision of the manuscript.This research was financially supported by the Consejo Nacional de Rectores (CONARE) through FEES fund and to Vicerrectoría de Investigación of the Universidad de Costa Rica through the projects 808-B0-654 and 808-B0-060.We are greatly thankful to five anonymous reviewers that helped improve the quality of this manuscript.

Fig. 1 .
Fig. 1.Surveyed area and location of sampling stations of the present work in adjacent waters to Cocos Island, Costa Rica.BIOSTAT and DOME stations from Sameoto et al., 1987.Fig. 1.Área de estudio y localización de las estaciones de muestreo en aguas adyacentes a la Isla del Coco, Costa Rica.Estaciones BIOSTAT y DOMEde Sameoto et al., 1987.

TABLE 1 Date
, time of collection, geographic coordinates and depth of sampling stations in adjacent waters to Cocos Island, Costa Rica CUADRO 1 Fecha, hora de colecta, coordenadas geográficas y profundidad de las estaciones de muestreo en aguas adyacentes a la Isla del Coco, Costa Rica

TABLE 2
List of euphausiid species, number of specimens and sites of collection in waters around Isla del Coco, Costa Rica CUADRO 2 Lista de especies de eufáusidos, número de especímenes y sitio de recolecta en aguas alrededor de la Isla del Coco, Costa Rica