Marine biodiversity of Bahía Culebra , Guanacaste , Costa Rica : published records

A survey of the published records of marine organisms of Bahía Culebra, an enclosed embayment on the north Pacific coast of Costa Rica, is analyzed resulting in a list of 577 species representing 22 phyla. The most diverse groups documented were crustaceans, cnidarians and mollusks in order of species number. The first published record of any marine organism from the area, a polychaete, occurred in 1922, with a peak of published records of species between 1940 and 1949 and, more recently, from 2000 to the present. Several additional taxa are known from the region but there are no published records of their occurrence. This is especially evident for such groups as the free living flatworms and black corals. Additionally, several habitats, including soft bottom sediments, have not been sampled. Because of the paucity of knowledge on the biodiversity of Bahia Culebra, much more research is needed in order to evaluate and understand the effect of climate change and increasing anthropogenic activities. Rev. Biol. Trop. 60 (Suppl. 2): 39-71. Epub 2012 April 01.

Bahía Culebra (10º36'N-85º39'W) is located on the north Pacific coast of Costa Rica.It is a relatively deep (30 m) and enclosed bay covering about 24 km 2 .This region of Costa Rica is undergoing the greatest coastal alteration due to tourism and other anthropongenic activities (Jiménez 2001, Fernández-García 2007).The bay is protected and deep enough to serve as an anchorage for US battleships between 1933and 1937(Sánchez -Noguera 2012).Based on his review of the history of marine research in Bahía Culebra by Cortés (2012a) the first period of active research in the area occurred between 1933and 1938. During 1933and 1934 the motor yacht Velero III on an expedition sponsored by the Allan Hancock Foundation, visited the bay (Fraser 1943).These expeditions have resulted in a significant number of publications and reports.In 1933, core samples were taken with the USS Hannibal, deposited at Scripps Oceanographic Institution, and the foraminifera analyzed (Bandy & Arnal 1957).The other important expedition was conducted by the New York Zoological Society as part of their eastern Pacific Expeditions.The steam yacht Zaca, visited Bahía Culebra in 1938 (Beebe 1938) and resulted in a significant number of publications.Few studies subsequently occurred until the 1950's when individual researchers studied the bay's fauna and flora, e.g., Elmer Y. Dawson who collected algae (Dawson 1960).
Since the mid 1980's scientists from the Centro de Investigación en Ciencias del Mar y Limnología (CIMAR: Marine Science and Limnology Research Center), Universidad de Costa Rica, have been carrying out research on the marine environments of Bahía Culebra, mainly on the coral reefs (Cortés & Murillo 1985).This work has been later expanded by Carlos E. Jiménez in the 1990s (Jiménez 1998) and also included studies of the diversity of marine organisms.The contributions by Arturo Dominici-Arosemena and co-workers (2001) added an important number of fishes to the list of Bahía Culebra.Karina Rodríguez (Rodríguez-Sáenz 2005, Rodríguez-Sáenz & Gasca 2009, Rodríguez-Sáenz & Segura-Puertas 2009) significantly increased the knowledge on the diversity of the gelatinous zooplankton of Bahía Culebra.Jorge Cabrera-Peña and his team from the Universidad Nacional, Heredia, Costa Rica, published three ecological papers in which marine species were mentioned (Madrigal-Castro et al. 1984, Cabrera-Peña et al. 1994, Cabrera-Peña & Solano-López 1996).Ángel Valdés and Yolanda E. Camacho-García (2004) add seven species of gastropods to the list of species of Bahía Culebra.
As emphasized by Knowlton and Jackson (2008) baseline information is fundamental to evaluate changes.This is important for regions rich in coralline environments (Cortés & Jiménez 2003) with high marine biodiversity (this paper), and applies especially for areas that are being altered at a rapid rate such as Bahía Culebra.For this reason we have compiled this list of published records as a historical document and as baseline for other papers published both in this issue and in the future.

MATERIALS AND METHODS
We have compiled all reports of marine species and related topics dealing with Bahía Culebra (Cortés 2012b) and a list of all the species reported, organized by taxonomic group, has been organized.The numbers of species per taxa and the year they were reported were recorded.For the algae we used the classification and updated names proposed by Guiry and Guiry (2010).For marine animals we referred mostly to WoRMS (World Register of Marine Species, http://www.marinespecies.org)and ITIS (Integrated Taxonomic Information System, http://www.itis.gov).

RESULTS AND DISCUSSION
The published records of marine species of Bahía Culebra are listed in Table 1 together with their references.A total of 577 species have been documented, in 22 phyla (Table 1  and 2).The Crustacea had the most species reported (147 spp., mostly decapods: 94 spp.); followed by the cnidarians (100 spp., mostly hydroids: 75 spp.);mollusks (93 spp., mostly bivalves: 55 spp.); and chordates (92 spp., mostly fishes: 82 spp.) (Table 2).These numbers is a reflection of marine biodiversity in general (IUCN 2010) but also the interest and dedication of certain researchers such as is the case of the hydroids by Charles McLean Fraser and Karina Rodríguez-Sáenz, or bivalves where most reports are by Leo G. Hertlein and Archibald M. Strong.
Most reports were published in the 1940's and 2000's (Fig. 1).The first pulse of publications resulted from the support of the Allan Hancock Foundation based on collections made aboard the Velero III (Fraser 1943), and the American Museum based on the collections of the New York Zoological Society Pacific expeditions aboard the Zaca (Beebe 1938).The second pulse of publications has occurred in the last ten years based on investigations sponsored by the Universidad de Costa Rica through the Centro de Investigación en Ciencias del Mar y Limnología (CIMAR: Marine Science and Limnology Research Center) and the Museo de Zoología (Zoology Museum).
Though known to be present in Bahía Culebra there are no published accounts for several groups of marine organisms, including the black corals, flatworms and nemerteans.Furthermore, conspicuos species such as marine turtles have been seem in the bay but not reported anywhere.Even important ecosystems, such as the soft bottom benthos as well as the rocky intertidal communities have not been studied and much more work needs to be done in the mangrove forests.
At present corals reefs, coral communities, sea urchins and some environmental parameters are being monitored by CIMAR, but other environments and organisms should be assessed periodically.The only way to determine changes due to anthropogenic and natural effects is through monitoring.

ACKNOWLEDGMENTS
We thank Cindy Fernández for help with the algae, Juan José Alvarado with the echinoderms, Harlan Dean with the polychaetes.We appreciate the review of the manuscript by Richard Heard, Harlan Dean and Juan José Alvarado.Projects in Bahía Culebra have been funded over the years by the Vicerrectoría de Investigación (Universidad de Costa Rica), Ecodesarrollo Papagayo, USAID-CDR program, and the Centro de Investigación en Ciencias del Mar y Limnología (CIMAR).

Fig. 1 .
Fig. 1.New reports or species described of marine species for Bahía Culebra per decade.

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Continued)List of marine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica

TABLE 1 (
Crouch & Poag (1987)rine species reported in the literature for Bahía Culebra, Guanacaste, Costa Rica As reported in the original publication.?= Doubtful record. a = species reported byCrouch & Poag (1987)but not found in any database.