Euphausiids (Crustacea: Euphausiacea) from a hotspot of marine biodiversity, Isla del Coco, Costa Rica, Eastern Tropical Pacific Juan Carlos Azofeifa-Solano1, Marco Corrales-Ugalde2, Iván Castellanos-Osorio3 & Álvaro Morales-Ramírez1,4 1. Escuela de Biología, Universidad de Costa Rica, San Pedro, 11501-2060 San José, Costa Rica; eazofeifa2@gmail.com, juan.azofeifa@ucr.ac.cr 2. Oregon Institute of Marine Biology, University of Oregon, Eugene, OR, 97403 USA; mcugalde88@gmail.com 3. El Colegio de la Frontera Sur, Unidad Chetumal. Av. Centenario km 5.5, Apdo. Postal 424. C.P.77014, Chetumal, Quintana Roo, México; ivancast@ecosur.mx 4. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Ciudad de la Investigación, Universidad de Costa Rica, San Pedro, 11501-2060 San José, Costa Rica; alvaro.morales@ucr.ac.cr Received 05-V-2015. Corrected 25-IX-2015. Accepted 15-X-2015. Abstract: 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. Key words: krill, holozooplankton, species composition, epipelagic zone, Costa Rica. Euphausiids (also known as krill) are a of the Norway pout (Trisopetrus esmarkii), group of shrimp-like holoplanktonic crusta- a krill predator, could lead to an increase of ceans that inhabit all oceans (Baker, Boden, euphausiid abundance, which in turn prey on & Brinton, 1990; Everson, 2000). They are an copepods, an important food source for other important part of the energy transfer between commercial fishes, such as cod and saithe. trophic webs of marine ecosystems, being Recently, large-scale commercial krill fisheries effective phytoplankton grazers and preyed have been developed in South Atlantic along upon by diverse organisms including large the Antarctic Peninsula, off the Japanese coast, invertebrates, fishes, sea birds, seals and whales and off the coast of British Columbia (Nicol, (Mauchline, & Fisher, 1969; Takashi, 1983; & Endo, 1997). Euphausiids have specific Williams, 1985; Agersted, Nielsen, Munk, distributional patterns associated with distinct Vismann, & Arendt, 2011). Their carcasses water masses, and thus are used as indicators and fecal pellets transport organic matter to of oceanographic environments (Brinton, 1981; deep waters and sediments (Wheeler, 1967; 1996; Lavaniegos, Lara-Lara, & Brinton, 1989; Fowler, & Small, 1972). Euphausiids may Lavaniegos, 1994). also affect the fisheries of other organisms, for The biogeography of euphausiids in the example Pauly, Christensen, Dalsgaard, Froese Pacific Ocean has been extensively described & Torres (1998) mentioned that overfishing by Brinton (1962), and several aspects of Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (Suppl. 1): S221-S230, February 2016 S221 their biology have been also studied in this delimiting areas in need for protection (Hen- region (Brinton, & Townsend, 1980; 2003; drickx, & Harvey, 1999). The present study is Mauchline, & Fisher, 1969; Mauchline, 1980; the first attempt to record the euphausiid spe- Everson, 2000; Letessier, Cox, & Brierley, cies around Isla del Coco. 2011). The Eastern Tropical Pacific (ETP) had been determined as a distinct biogeographic province (Spalding, Agostini, Rice, & Grant, MATERIALS AND METHODS 2012). Fernández-Álamo & Färber-Lorda Isla del Coco (also known as Cocos Island) (2006) reported euphausiids as a very well- is located in the ETP, and represents the core studied taxon in this region. The first records of the Isla del Coco Marine Conservation Area of euphausiids in the ETP were made by Ort- (Fig. 1), declared UNESCO World Heritage mann (1894) and Hansen (1912). Later, Brinton in 1997 and RAMSAR site in 1998 (Cortés, (1962; 1979) described in detail the distribu- 2008). The island is located ~500km southwest tional patterns of euphausiid species and their of Cabo Blanco, Costa Rica, and it is the only relation to oceanographic parameters. Recent exposed point of the Coco Cordillera (Castillo studies have been conducted in the Mexican et al., 1988; Rojas, & Alvarado, 2012). The Central Pacific, which include descriptions of waters around Isla del Coco are influenced euphausiid distribution, abundance, biomass, by the seasonal movement of Inter-Tropical biochemical composition, and effects of wind Convergence Zone (Broenkow, 1965; Alfaro, forcing, upwelling and downwelling systems, 2008), periodic El Niño events (Fiedler, & Tal- and climate-oceanographic phenomena such ley, 2006), and even the seasonal upwelling in as El Niño on krill populations (López-Cor- the Gulf of Papagayo (Lizano, 2008). Physico- tés, 1990; Färber-Lorda, Lavín, Zapatero, & chemical analyses from waters around Isla del Robles, 1994; Färber-Lorda, Lavín, & Guer- Coco revealed influence from both coastal and rero-Ruiz, 2004; Färber-Lorda, Trasviña, & oceanic waters (Acuña, García, Gómez, Var- Cortés-Verdín, 2010; Ambriz-Arreola, Gómez- gas, & Cortés, 2008). Gutiérrez, Franco-Gordo, Lavaniegos, & In order to describe the zooplankton com- Godínez-Domínguez, 2012; Gómez-Gutiérrez munity from Isla del Coco, two oceanographic et al., 2014). The distribution of euphausiids expeditions were carried out in March 2011 had been also studied in the Colombian Pacific and June 2012 aboard the MV Argo and MV (López-Peralta, & Medellín-Mora, 2010). In Undersea Hunter, respectively. For a more the Central American Pacific, there have been detailed explanation of the two oceanographic studies on crustacean larvae (including krill) expeditions see Brenes et al. (2011) and Cortés (Sánchez-Maravilla, 1986), and diel vertical et al. (2012). A total of 35 stations in March migrations of euphausiids (Sameoto, Gugliel- 2011 and 25 in June 2012 were sampled around mo, & Lewis, 1987). Isla del Coco. In this paper we present results Despite the extensive research on euphau- from eight of them (one from 2011 and seven siids from the ETP, there is less specific infor- from 2012) (Fig. 1). mation regarding euphausiids in the Costa During both oceanographic expeditions, Rican Pacific and Isla del Coco (Castellanos, zooplankton samples were collected using a Suárez-Morales, & Morales-Ramírez, 2009). It standard General Oceanics net (202μm mesh, is important to fill the gaps on taxonomic and 50cm diameter, 1.5m length) towed vertically diversity knowledge in marine ecosystems to from 100m and 200m deep to the surface in identify and understand the economic and eco- 2011 and 2012, respectively (Table 1). All logical relevance that these organisms might the zooplankton samples were preserved in have on several oceanic areas (Costello et al., seawater with 4 % formalin and transported 2010). Regional checklists of marine species to the Zooplankton Laboratory at CIMAR, are also important tools for recognizing and UCR. Only adult euphausiid specimens were S222 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (Suppl. 1): S221-S230, February 2016 95º0’0” W 90º0’0” W 85º0’0” W 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 DOME de 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 Station Date Time of collection Latitude Longitude Depth (m) 23 29/03/2011 18:44-20:07 3.0995 -88.31035 0-100 6 08/06/2012 20:46-21:40 5.19252 -87.72465 0-200 7 09/06/2012 00:33-01:32 4.8591 -87.72538 0-200 12 09/06/2012 23:35-00:35 4.52662 -86.3895 0-200 16 10/06/2012 19:27-20:27 5.19191 -86.38947 0-200 20 11/06/2012 19:10-20:20 5.85736 -87.05848 0-200 21 11/06/2012 22:58-23:58 6.19191 -87.0587 0-200 25 12/06/2012 18:51-19:50 6.8774 -87.0587 0-200 separated from the samples, counted and iden- distributed in four genera, all belonging to the tified following Baker et al. (1990) and Brin- family Euphausiidae (Table 2; Figs. 2, 3, 4). All ton, Ohman, Townsend, Knight & Bridgeman the species are new records for Isla del Coco in (2000). All the specimens were deposited in the the Costa Rican Pacific. The most frequent spe- crustacean collection at the Zoology Museum, cies were Euphausia distinguenda, Euphausia University of Costa Rica (Museo de Zoología, diomedeae, Nematoscelis gracilis and Stylo- Universidad de Costa Rica, MZUCR). cheiron affine, with more than 10 specimens. RESULTS DISCUSSION A total of 130 specimens were analyzed. The 13 euphausiid species found in Isla The present study reports 13 krill species, del Coco were previously recorded in the ETP Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (Suppl. 1): S221-S230, February 2016 S223 5º0’0” N 10º0’0” N 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 Species Number of specimens Stations Catalog number Euphausia diomedeae Ortmann, 1894 18 6, 7, 12, 16, 23 3319-06, 3339-07, 3356-02, 3358-01, 3359-02 E. distinguenda Hansen, 1908 43 6, 7, 12, 16, 20, 21, 25 3319-07, 3320-02, 3339-04, 3355-05, 3356-05, 3357-04, 3358-06 E. eximia Hansen, 1911 5 20, 25 3355-03, 3357-01 E. gibboides Ortmann, 1893 3 6, 23 3319-023359-01 E. lamelligera Hansen, 1911 2 25 3355-04 E. tenera Hansen, 1905 4 6, 7, 16 3319-08, 3356-04, 3358-03 Nematobrachion flexipes (Ortmann, 1893) 6 6, 16, 21 3319-01, 3320-01, 3358-02 Nematoscelis gracilis Hansen, 1910 23 6, 7, 12, 16, 20, 25 3319-05, 3339-05, 3355-02, 3356-01, 3357-02, 3358-04 N. tenella G.O. Sars, 1883 1 12 3339-06 Stylocheiron affine Hansen, 1910 13 6, 7, 12, 16, 20, 21, 25 3319-03, 3320-03, 3339-01, 3355-01, 3356-03, 3357-05, 3358-05 S. carinatum G.O. Sars, 1883 8 6, 12, 21 3319-04, 3339-02 S. longicorne G.O. Sars, 1883 3 20 3357-03 S. maximum Hansen, 1908 1 12 3339-03 and waters near Costa Rica by the “Shellback” Brinton (1979) grouped the euphausiids expedition in 1952 (Brinton, 1962). Sameoto from ETP by biogeographic and hydrographic et al. (1987) reported 17 euphausiid species affinities. The non-migrating warm cosmopo- near the Costa Rica Dome outside the Eco- lites are N. tenella, S. affine, Stylocheiron nomic Exclusive Zone of Costa Rica (Fig. 1). carinatum, Stylocheiron longicorne and Stylo- The higher species richness reported for the cheiron maximum. The species that proliferate Costa Rica dome is probably related with the in the north and south margins of ETP are depth range sampling (0-1000m depth) and Euphausia eximia, Nematobrachion flexipes technique (multiple opening and closing net) and Euphausia gibboides. These species are (Sameoto et al., 1987), while this study only found in the low oxygen layer, but are more analyzed samples from 200m and 100m depth abundant in its margins. The equatorial endem- using a standard net. Only 65 % of euphausiid ic species are adapted to migrate into the low species found in Costa Rica Dome are reported oxygen layer. This group includes E. diomed-eae, E. distinguenda, Euphausia lamelligera for Isla del Coco. Moreover, Euphausia tenera and N. gracilis. Finally, E. tenera is a widely and Nematoscelis tenella were not reported distributed species, thus it was not included in by Sameoto et al. (1987) from the Dome sta- any group by Brinton (1979). We emphasize tion; however, both species were collected in that the most common species in the present the BIOSTAT station (off Central American study were mainly from the equatorial endem- coast). The euphausiid species assemblage of ics group (E. distinguenda, E. diomedeae and Isla del Coco should be determined by the N. gracilis), and S. affine, a non-migrating particular oceanographic dynamics surround- warm cosmopolite species that can also be ing the island (Broenkow, 1965; Fiedler, & found through the low oxygen layer. Talley, 2006; Acuña et al., 2008; Alfaro, 2008; Isla del Coco hosts a high marine biodiver- Lizano, 2008). sity (Cortés, 2012), which might also apply for S224 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (Suppl. 1): S221-S230, February 2016 Fig. 2. (A) Euphausia diomedeae, bifid lappet in first antennular segment; (B) Euphausia distinguenda, conspicuous keel in the third antennular segment with a little denticule; (C) Euphausia eximia, pectinate lappet in the first antennular segment; (D) Euphausia gibboides, conspicuous keel in the third antennular segment pointed forward; (E) Euphausia lamelligera, movable plate in the second antennular segment; (F) Euphausia tenera, third antenular segment without a keel, eyes are little and oval. Scale in A, B, C, D, E, and F=500μm. Fig. 2. (A) Euphausia diomedeae, proceso antenular bífido en el primer segmento antenular; (B) Euphausia distinguenda, quilla conspicua en el tercer segmento antenular; (C) Euphausia eximia, proceso antenular pectinado en el primer segmento antenular; (D) Euphausia gibboides, quilla conspicua en el tercer segmento antenular apuntando hacia adelante; (E) Euphausia lamelligera, placa móvil en el segundo segmento antenular; (F) Euphausia tenera, el tercer segmento antenular sin quilla, ojos pequeños y ovales. Escala en A, B, C, D, E y F=500μm. Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (Suppl. 1): S221-S230, February 2016 S225 Fig. 3. (A) Nematobrachion flexipes, rounded lappet in the first antennular segment; (B) N. flexipes, mid-dorsal spines in the abdominal segments 3-6; (C) Nematoscelis gracilis, size of upper lobe of the eye very similar to lower lobe; (D) N. gracilis, dactylus and propodus of the first thoracic leg; (E) Nematoscelis tenella, upper lobe of the eye bigger than the lower lobe. Scale in A, C, D, E and F=500μm. Scale in B=1mm. Fig. 3. (A) Nematobrachion flexipes, proceso antenular redondeado en el primer segmento antenular; (B) N. flexipes, espinas medio-dorsales en los segmentos abdominales 3-6; (C) Nematoscelis gracilis, tamaño del lóbulo superior del ojo similar al lóbulo inferior; (D) N. gracilis, dáctilo y propodo de la primera pata torácica; (E) Nematoscelis tenella, lóbulo superior del ojo mucho más grande que el lóbulo inferior. Escala en A, C, D, E y F=500μm. Escala en B=1mm. S226 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (Suppl. 1): S221-S230, February 2016 Fig. 4. (A) Stylocheiron affine, upper ocular lobe with 4-8 enlarged crystallines in transversal row; (B) Stylocheiron carinatum, upper ocular lobe short and narrow, with parallel anterior and posterior margins that sharply join in the lower lobe; (C) S. carinatum, the posterior margin of the propodus in the third thoracic leg bears a tubercule with a setae; (D) Stylocheiron longicorne, upper ocular lobe with 19 enlarged crystallines in transversal row; (E) S. longicorne, abdominal segments; (F) Stylocheiron maximum, eyes whit a sharp constriction between the upper and lower lobes, the upper lobe is smaller than the lower. Scale in A, B, C and D=500μm. Scale in E and F=1 mm. Fig. 4. (A) Stylocheiron affine, lóbulo superior con 4-8 cristalinos alargados en línea transversal; (B) Stylocheiron carinatum, lóbulo ocular superior corto y delgado, con los márgenes que se unen abruptamente al lóbulo inferior; (C) S. carinatum, el margen posterior del propodo de la tercer pata torácica porta un tubérculo con una seta; (D) Stylocheiron longicorne, lóbulo ocular superior con 19 cristalinos alargados en línea transversal; (E) S. longicorne, segmentos abdominales; (F) Stylocheiron maximum, ojos con una constricción marcada en medio de los lóbulo superior e inferior, el lóbulo superior es más pequeño que el inferior. Escala en A, B, C y D=500μm. Escala en E y F=1mm. Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (Suppl. 1): S221-S230, February 2016 S227 euphausiids. The waters around the island host RESUMEN 22 % of the 59 species reported for the Pacific Ocean (Brinton, 1962; 1979) and 55 % (20 spe- Eufáusidos (Crustacea: Euphausiacea) de un punto caliente de biodiversidad marina, Isla del Coco, cies) for Central American Pacific waters (Cas- Costa Rica, Pacífico Tropical Oriental. Los eufáusidos tellanos et al., 2009). Compared with studies han sido ampliamente estudiados en el Océano Pacífico, from the Central Pacific coast of Mexico (Fär- sin embargo existe poca información respecto a los eufáu- ber-Lorda et al., 1994; 2010; Ambriz-Arreola et sidos que habitan aguas costarricenses. Analizamos 130 al., 2012) that have reported ten or less species, especímenes de eufáusidos provenientes de muestras de zooplancton recolectadas alrededor de la Isla del Coco del this study reports 13 species with less sampling 2011 y 2012. Identificamos 13 especies pertenecientes a effort. Here we present useful pictures that may cuatro géneros y una familia. Se presenta un listado de help in identification of specimens from Costa especies y fotografías con detalles que facilitan su identifi- Rican Pacific. The specimens analyzed in the cación. Todas las especies encontradas representan nuevos present study were the first euphausiids depos- informes para aguas de la Isla del Coco en el Pacífico cos- tarricense. Las especies más frecuentes fueron Euphausia ited at the crustacean collection of the Museum distinguenda, Nematoscelis gracilis, Euphausia diomedeae of Zoology, University of Costa Rica. y Stylocheiron affine. Although this is the first effort to record the euphausiid diversity from Isla del Coco, Palabras clave: kril, Pacífico Tropical Oriental, composi- samples from deeper waters are needed to ción de especies, holozooplancton, zona epipelágica. found deep-water distributed species reported for Central American waters (Brinton, 1962; REFERENCES 1979; Sameoto et al., 1987; Castellanos et al., 2009). 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