Marine biodiversity of an Eastern Tropical Pacific oceanic island , Isla del Coco , Costa Rica

Isla del Coco (also known as Cocos Island) is an oceanic island in the Eastern Tropical Pacific; it is part of the largest national park of Costa Rica and a UNESCO World Heritage Site. The island has been visited since the 16th Century due to its abundance of freshwater and wood. Marine biodiversity studies of the island started in the late 19th Century, with an intense period of research in the 1930’s, and again from the mid 1990’s to the present. The information is scattered and, in some cases, in old publications that are difficult to access. Here I have compiled published records of the marine organisms of the island. At least 1688 species are recorded, with the gastropods (383 species), bony fishes (354 spp.) and crustaceans (at least 263 spp.) being the most species-rich groups; 45 species are endemic to Isla del Coco National Park (2.7% of the total). The number of species per kilometer of coastline and by square kilometer of seabed shallower than 200m deep are the highest recorded in the Eastern Tropical Pacific. Although the marine biodiversity of Isla del Coco is relatively well known, there are regions that need more exploration, for example, the south side, the pelagic environments, and deeper waters. Also, several groups of organisms, such as the flatworms, nematodes, nemerteans, and gelatinous zooplankton, have been observed around the Island but have been poorly studied or not at all. Citation: Cortés, J. 2012. Marine biodiversity of an Eastern Tropical Pacific oceanic island, Isla del Coco, Costa Rica. Rev. Biol. Trop. 60 (Suppl. 3): 131-185. Epub 2012 Dec 01.

Isla del Coco (Cocos Island) is an oceanic island in the Eastern Tropical Pacific Ocean, about 500km from mainland Costa Rica (Cortés 2008), and biogeographically it is part of the Ocean Island Province (sensu Robertson & Cramer 2009). It is a highly diverse area with the highest number of endemic species in Costa Rica (Cortés & Wehrtmann 2009, Cortés 2013a). It was declared a National Park in 1978, a UNESCO World Heritage Site in 1997, and a Ramsar site in 1998. It is important for Costa Rica, due to of its biological and historical richness and also because the Territorial Sea surrounding the island makes the marine area of Costa Rica more than 10 times its terrestrial area (Cortés & Wehrtmann 2009, Cortés 2013b. Marine biodiversity studies at Isla del Coco started in the late 19th Century with the expedition of the US Fisheries Commission Steamer Albatross (see a history of marine research at what is now Parque Nacional Isla del Coco (Isla del Coco National Park) in Cortés 2008). Since then, many studies have been done but there is still more to be discovered. Hertlein (1963) compiled what was known about marine species of the Island. In this paper I update the list of marine organisms of Isla del Coco National Park, compare it with the species from the mainland, and identify areas for future research.

MATERIALS AND METHODS
Published records of marine species of Parque Nacional Isla del Coco (PNIC) were searched and species lists compiled. An important source was the book "Marine Biodiversity of Costa Rica, Central America" edited by Wehrtmann and Cortés (2009). Here I included overlooked and newly published records. The number of species from PNIC is compared to the numbers from the rest of the Pacific of Costa Rica. Including the mainland, the Coco volcanic Cordillera, the pelagic areas, and the Costa Rica Thermal Dome.
The perimeter of Isla del Coco is 28.8km, and it is surrounded by a platform that drops off at around 180-200m. The perimeter at 100m is 54.4km and at 200m is 71.4km. The area less than 50m deep around the island is 91.5km 2 , less than 100m is 133km 2 , and less than 200m deep is 318km 2 (O.G. Lizano, pers. comm. 2011). The Linear Biodiversity Index (LBI) and the Area Biodiversity Index (ABI) were calculated as in Wehrtmann et al. (2009). To calculate the LBI, the number of species was divided by the perimeter of the island. The ABI was calculated by dividing the number of species by the area down to the 200m isobaths; the depth within which almost all the species had been recorded.

MARINE BIODIvERSITY OF ISLA DEL COCO NATIONAL PARK
At least 1688 species of marine organisms (Appendix 1) have been reported from Isla del Coco National Park (PNIC). The most speciesrich groups are the gastropods (383 species), bony fishes (354 spp.) and crustaceans (at least 263 spp.) ( Table 1). Close to 4,700 species of marine organisms have been reported for Costa  Pacific Costa Rica = mainland coast (MC), Coco volcanic Cordillera (CvC) (also known as Cocos Ridge), Costa Rica Thermal Dome (CRTD), and Isla del Coco National Park (PNIC). + = more species than the number indicated are known, but have not been described. n.k. = not known.
Rica (Table 1); of these species, 747 or ~16% have been only reported from PNIC but not from other areas of Costa Rica. The percentages by taxonomic group ranged from 0 to 100%. All brown algae, echiuran, marine insects, and reptiles from PNIC are also found in the rest of Costa Rica. While all reported branchiopods, ostracods, phoronids, and crinoids, represented by one or two species, known from Costa Rica are reported from PNIC. Some groups have a disproportionate percentage of known species at PNIC, scyphozoans (40%), echinoderms as a phylum (42.6%), and its classes, asteroids (66.7%) echinoids (36.4%) and holothurians (40.4%), brachiopods (75.0%), and within the chordates, cephalochordates (50%) appendicularians (70%) and thaliacians (75%). Species of several groups have been reported from other areas of Costa Rica than PNIC ( Table 2). Some of these taxa we know are absent from PNIC, for example the seagrasses and mangroves, and some of the species associated to this ecosystems. Other groups have been observed, photographed or collected but there are no published accounts of them. Within these groups we have nematodes, nemerteans, ascideans, and parasites of fishes and turtles. Free-living flat worms have been observed along the mainland coast of Costa Rica as well as at PNIC, but there are no publications. Of other taxa we do not know if they are present or not, for example, marine fungi, cumaceans and kinorhynchans (Table 2). Plus there must be other marine groups that have been reported from the Eastern Tropical Pacific, for example, loriciferans (Heiner & Neuhaus 2007) that might be present at PNIC.
Forty five species or 2.7% of the species known from PNIC are endemic (Tables 3,  4), and this represents 47.4% of all endemic marine species of Costa Rica (95 spp.). The number of endemic species is relatively low, but that is common in marine environments. The list of endemic marine species is presented in Table 3, as well as the reference to the publication where the species was described. Between 1893 and 1971, 16 species were described, while 29 were described from 1981 to 2011. Most endemic species are fishes (33.3% of all endemics from PNIC) and most were described in the last 30 years (11 of the 15 species). Crustacea is the next group with most endemism, 28.9%, followed by the mollusks, 15.5%, all very well studied groups (Table 4). Within a particular group, the brachiopods have the highest percentage of endemism, 16.7% followed by the sponges and polyplacophorans with 12.5% (Table 4).
Biodiversity indices used to compare species diversity at Isla del Coco with that at the Costa Rican coast revealed significantly higher values at PNIC than at the coast. For example,

STATUS OF THE ENDEMIC SPECIES
Forty five species are endemic to PNIC ( Table 2). While some are abundant, such as the calcified hydrozoan Stylaster cocosensis, described in 1991 by Stephen D. Cairns, others have not been seen since they were described, for example, the sand dollar, Encope cocosi. This species had not been found alive since it was described by H.L. Clark in 1948. However, in January 2007 a specimen recently dead was dredged from deep water. In 1986 using the research submersible Johnson-Sea-Link (Harbor Branch Oceanographic Institution, Fort Pierce, Florida, USA) diving to several hundred meters, collected specimens that resulted in new species and some were endemic (Cairns 1991a, b). We don not know the status of some of those endemics because no submersible with the depth capacity of the Johnson-Sea-Link has been back to the island. There is now another submersible operating more regularly at the island, the DeepSee (Undersea Hunter Group, Puntarenas, Costa Rica), with a depth capability of 450m (Cortés & Blum 2008). We have been able to observed several of the deepwater endemics collected in 1986, some are relatively abundant. Eleven endemic species have been described in the last decade so it's possible that eventually they will be found in other areas. Some species of fishes which were initially classified as endemic to one of the oceanic islands of the eastern Tropical Pacific are now reported from one or more of the other oceanic islands. For example, Stegastes arcifrons which have been found in the three oceanic islands, Galápagos, Malpelo and Isla del Coco or Serranus tico and Halichoeres discolor, found in Isla del Coco and Malpelo. Starr et al. (2012) indicated in their study of deepwater fishes of Isla del Coco National Park and Las Gemelas Seamount that probably deep areas in the eastern tropical Pacific will have similar species, but more studies and collections are needed.

DISCUSSION
Isla del Coco National Park has a rich marine biodiversity with some groups having been studied for many years and numerous scientists. For example, fishes and mollusks, especially gastropods, are relatively well known while other groups such as cyanobacteria, gelatinous zooplankton, nematodes and flatworms have been poorly studied or never at all even though we know they are on the island. As a result of recent expeditions (2006-2012) many new records of species have been Hertlein (1963) did a compilation of published marine species of Isla del Coco, and included a biogeographic analysis of the flora and fauna of the island, plus an annotated bibliography. He reported 334 species (Table 5), with the gastropods (62 species) as the most species-rich group, followed by bony fishes (59) and crustaceans (56). The number of species and of different taxonomic groups has increased significantly but the same pattern of the most species-rich groups is maintained. Wehrtmann et al. (2009) reported 1,142 marine species for Isla del Coco National Park, with the most species-rich groups, in the same order, being the same as above. Here, 546 more species were added to the list of marine species of Isla del Coco National Park, and more will be added in the near future as other groups, depths and areas of the island are being studied.
Hickman (2009), in his study of the marine invertebrate biota of the Galápagos Islands, found that while some groups of species are depauperated others displayed high diversity when compared to mainland Ecuador. Similar patters were observed at Isla del Coco National Park. These patterns can be attributed to several possible factors likely acting in concert, both for source populations from elsewhere as well as established populations at PNIC: variation in the dispersal potential to and from PNIC, the probability of recruitment at PNIC, and the potential for survival and continued recruitment based on local environmental conditions. Species with long-lived larvae will have a chance of dispersing more than others if they find the type of environmental conditions necessary to survive and reproduce. For example, the absence of seagrasses and the low number of species of bivalves may be due to the lack of soft sediments where they can live.

AREAS FOR FUTURE RESEARCH
The least studied area of PNIC is the south side due to the normally rough sea conditions on that side (Lizano 2008). From a few observations, several species and environments in the south are different from the north in species density and composition, probably due to the currents that flow there (Cortés & Blum 2008).  TAxA  Number of species  Foraminifera  17  Cirripedia  3  Cnidaria  24  Copepoda  2  Anthozoa  19  Brachiopoda  1  Hydrozoa  5  Bryozoa  20  Mollusca  90  Echinodermata  45  Polyplacophora  4  Asteroidea  6  Gastropoda  62  Ophiuroidea  15  Bivalvia  12  Echinoidea  13  Cephalopoda  12  Holothuroidea  11  Annelida  9  Chordata  72  Crustacea  56  Chondrichtyes  13  Decapoda  50  Actinopterygii  59  Amphipoda  1  TOTAL 334 species More sampling should be done on that side in the future in the shallow and deepwaters of the south for better understanding the biodiversity of PNIC, and the effect of currents on that biodiversity.
There are several groups of organisms which have been observed and in some cases collected but for which there are no publications. Examples include cyanobacteria, sponges, flatworms, and nematodes (Table 2). For a few groups, especially the best known, there are some publications on their biogeographic relationships. Several species of stomatopods (Manning 1972), most reef building corals (Cortés 1986(Cortés , 2011