Marine biodiversity baseline for Área de Conservación Guanacaste, Costa Rica: published records

Abstract The diversity of tropical marine organisms has not been studied as intensively as the terrestrial biota worldwide. Additionally, marine biodiversity research in the tropics lags behind other regions. The 43,000 ha Sector Marino of Área de Conservación Guanacaste (ACG, Marine Sector of Guanacaste Conservation Area), on the North Pacific coast of Costa Rica is no exception. For more than four decades, the terrestrial flora and fauna has been studied continuously. The ACG marine biodiversity was studied in the 1930’s by expeditions that passed through the area, but not much until the 1990’s, except for the marine turtles. In the mid 1990’s the Center for Research in Marine Science and Limnology (CIMAR) of the Universidad de Costa Rica (UCR) initiated the exploration of the marine environments and organisms of ACG. In 2015, ACG, in collaboration with CIMAR, started the BioMar project whose goal is to inventory the species of the marine sector of ACG (BioMar ACG project). As a baseline, here I have compiled the published records of marine ACG species, and found that 594 marine species have been reported, representing 15.5% of the known species of the Pacific coast of Costa Rica. The most diverse groups were the crustaceans, mollusks and cnidarians comprising 71.7% of the ACG species. Some taxa, such as mangroves and fish parasites are well represented in ACG when compared to the rest of the Costa Rican coast but others appear to be greatly underrepresented, for example, red algae, polychaetes, copepods, equinoderms, and marine fishes and birds, which could be due to sampling bias. Thirty species have been originally described with specimens from ACG, and 89 species are not known from other localities on the Pacific coast of Costa Rica except ACG. Most of the sampling has been concentrated in a few localities in Sector Marino, Playa Blanca and Islas Murciélago, and in the nearby waters of Bahía Santa Elena. In an effort to fill this gap, CIMAR is collaborating with ACG and a private foundation to start an inventory of the marine organisms of the conservation area. The project will be assisted by two marine parataxonomists, and all samples will be catalogued, photographed, bar coded and voucher specimens deposited at the Museo de Zoología, UCR. All the information will be available through Internet. It is anticipated that the BioMar project will fill many of the knowledge gaps and significantly more marine species will be encountered. This project could become a viable model for marine biodiversity inventories in other Costa Rican Conservation Areas (Áreas de Conservación) and in other countries.


Introduction
Marine biodiversity studies have lagged behind terrestrial research, especially in the tropics, with a few exceptions such as Australia (Chapman 2009). Some studies in the Neotropics regarding marine biodiversity have been published, most focused on coral reef areas (Cortés et al. 2017). Several taxonomic groups are fairly well known, such as mollusks and fishes, with monographs, many papers and guides, while others are poorly known, to mention a few, microorganisms and smaller phyla. The same occurs geographically: some countries in the tropics have been relative well studied, for example, Costa Rica (Wehrtmann and Cortés 2009), while in other countries (such as Nicaragua) research and publications on marine biodiversity are scarce.
Costa Rica comprises 11 Conservation Areas (Áreas de Conservación), one of which is Área de Conservación Guanacaste (ACG) on the northwest Pacific coast of Costa Rica (Fig. 1). The ACG contains much of the last remnants of Costa Rican tropical dry forest and its terrestrial biodiversity has been and still is the subject of intensive research and restoration (Janzen and Hallwachs 2016). The ACG covers an area of 163000 hectares, 43000 of them marine, and 150 km of protected coastline (http:// www.acguanacaste.ac.cr/acg/que-es-el-acg). It was declared a UNESCO World Heritage Natural Site in 1999. Compared to the terrestrial area, the marine sector (officially Sector Marino) has not been studied intensively. A new initiative, BioMar ACG (Marine Biodiversity of ACG), was started in 2015 to inventory the marine organisms of the area, and then make all the information publicly available, mainly through the Internet, but also with scientific and popular publications. This project is a 5-year collaboration between the conservation area, a private foundation and academia; all samples are being catalogued, photographed, bar coded, and vouchers deposited at the Museo de Zoología (Museum of Zoology) at the Universidad de Costa Rica (UCR).
The marine sector of ACG has a high diversity of habitats, with high species richness worthy of more study (Beebe 1942, Cortés 1996-1997b. There is a well-represented suite of coastal and marine ecosystems, such as mangrove forest of variable sizes, beaches of different composition and size, bays and coves, rocky intertidal zones with several wave regimens, mud flats, rocky subtidal sites, coral reefs, rhodolith beds and deep areas -more than 50 m, plus an archipelago (Islas Murciélago), shoals, and several more isolated islands Wehrtmann 2009, Cortés 2016). The main  Table 2 for the codes of the sites. Stars = beaches, triangle = mangrove forests, circle = bays; green = protected area; blue circles = shoals.
nesting site in the country of the frigate bird, Fregata magnificens, is on one of the nearby islands, Isla Bolaños, in Bahía Salinas (Alvarado-Quesada 2006). An outstanding oceanographic feature of the region is the seasonal upwelling (the Papagayo Up- welling) that brings deep cold, nutrient-rich and CO 2 -rich waters to the surface during the trade winds season (December to April-May) (McCreary et al. 1989, Alfaro and Cortés 2012, Rixen et al. 2012. Micro-and macroalgal growth increases significantly as a consequence of the upwelling .
What is now ACG's Sector Marino (Fig. 1) was first explored, samples collected, and papers published by several marine expeditions from the United States starting in the 1930's (Cortés 2009a, Table 1). The first expedition was the Templeton Crocker Expedition of the California Academy of Sciences in 1932 aboard the SY Zaca, when they visited Bahía Murciélago and Bahía de Santa Elena (previously known as Port Parker) (Crocker 1933). In 1935, as part of the Allan Hancock Pacific Expeditions aboard the MY Velero III, biologists visited Bahía Santa Elena and Bahía Salinas (Fraser 1943a, b). The SY Zaca was again in the region in 1937-1938, but this time in an expedition of the New York Zoological Society; they collected in Bahía Santa Elena, around Islas Murciélago and around Playa Potrero Grande (Beebe 1938(Beebe , 1942. These three expeditions generated a significant number of publications on ACG marine organisms (Table 1). There were no additional expeditions until 1959, when the MY Stella Polaris visited the country (Dawson and Beaudette 1959). In 1972, the RV Searcher collected samples in the region and new species of fish were described (Bussing and Lavenberg 2003). The next expedition that visited the area was the Eastern Pacific RV Alpha Helix Expedition, in 1978 organized by the Scripps Institution of Oceanography (SIO). They collected samples that are deposited at SIO, but few papers were published (Luke 1995). Chan et al. (2016) recently published on some of the barnacles collected during that expedition. The most recent expedition was the Smithsonian Tropical Research Institute RV Urracá to the northern and central Pacific coast of Costa Rica in 2005(Vargas-Castillo 2008. Many individuals, groups of researchers or institutions have contributed to the knowledge of ACG marine biodiversity (Table 1). Elmer Y. Dawson published several papers on macroalgae of Costa Rica, including the ACG (Dawson 1960(Dawson , 1961. Richard and Hughes (1972) and Cornelius (1975) published on marine turtles of the ACG, with the first observations in 1970-1971, Marques et al. (1997 and Monks et al. (1997) collected and later described several fish parasites. Between 1996 and 2002, the Instituo Nacional de Biodiversidad collected mollusks in the ACG, and generated several papers on the opistobranchs (Valdés and Camacho-García 2004, Camacho-García et al. 2005, Camacho-García and Gosliner 2008. The CIMAR of the UCR has published papers on marine organisms and environments of Costa Rica that include the ACG: e.g., Cutler et al. (1992) on sipunculids, Moran and Dittel (1993) -crustaceans, Cortés and Guzmán (1998) -corals, Dean (2001, 2004 The objective of this contribution is to generate a baseline of the marine biodiversity of ACG's Sector Marino and adjacent unprotected areas, some of which are in the process of being officially protected. This will serve as a starting point for the recently initiated BioMar ACG project (Marine Biodiversity of the Guanacaste Conservation Area). This five-year project (2015-2019), funded by the Guanacaste Dry Forest Conservation Fund, and with support from the Ministry of the Environment and Energy of the Costa Rican government and the UCR, will collect, identify and provide publicly accessible information about most of ACG's species of marine macroorganisms and as many of the microorganisms as feasible.
The resulting list of species was compared to the remainder of the Pacific coast of Costa Rica and to available species lists from other countries in the Eastern Tropical Pacific. Knowledge gaps were identified and potential areas of future research suggested.

Results
Five hundred ninety four marine species have been reported so far for the ACG (Table  3, Appendix 1), which represents 15.5% of the known species of the Pacific coast of Costa Rica. The most diverse groups were crustaceans (193 spp.), mollusks (187 spp.) and cnidarians (46 spp.), comprising together 71.7% of the ACG's marine species. These three groups represent 23.9%, 18.2% and 26.7%, respectively of the known species of the Pacific coast of the country (Table 3). Some groups are well represented in the ACG when compared to the rest of the coast (e.g., species of mangroves and fish parasites), while others are greatly underrepresented. For example, red algae, polychaetes, copepods, equinoderms, and marine fishes and birds are poorly represented in the published reports (Table 3). Other groups of organisms have been observed and identified (e.g., various species of sponges, flat worms, ophiuroids, and ascidian) but there are no published records of these species (Table 4). Other taxa (such as diatoms, nemerteans and appendicularians) undoubtedly inhabit the study area but have not been observed or collected yet (Table 4). Over 85% of the species reported are also found in other areas of the coast of Costa Rica and in the Eastern Tropical Pacific; however, most areas, including the ACG, have not been intensively collected, and the same common species are found repeatedly by collecting expeditions. Thirty new species have been described from specimens collected in the ACG: one foraminiferan, one echinoderm, two octocorals, three parasitic flatworms, four fishes, eight crustaceans and 11 mollusks (Appendix 1). Eightynine species are currently known only from the ACG along the Pacific coast of Costa Rica (Table 3, Appendix 1).
Most of the sampling has been concentrated in a few localities of the marine area of the ACG and those sites therefore have the highest number of reported species. For example, Bahía Santa Elena (371 spp.), Playa Blanca (104 spp.) and in some of the   Cortés et al. 2012). But that number will defi-nitely increase as more taxa, other sites and environments within the ACG are inventoried. Cortés et al. (2017) synthesized the knowledge of marine biodiversity of the Eastern Tropical Pacific, mainly from coral reefs, where most studies have been done. For example, 857 marine species have been reported for Clipperton Atoll, France, (Charpy 2009, Payri et al. 2009, Fourriére et al. 2014, 968 spp. for El Salvador (Barraza 2000(Barraza , 2014a, 2157 spp. for the coast of Oaxaca, México (Bastida-Zavala et al. 2013), 3536 spp. for the Galápagos Islands (Bustamante et al. 2002, Hickman 2009), 3838 spp. for the Pacific coast of Costa Rica (Table 3, this paper), and 5740 spp. for the entire Gulf of California, México (Aburto-Oropeza and Balart 2001, Reyes-Bonilla et al. 2012). In other countries, for example, Panamá and Colombia, there are detailed inventories of some higher taxa, but not a compilation of all macrotaxa (Cortés et al. 2017). None of these inventories attempted to include the microorganisms.
There are large differences in the numbers of species among different sites in the Eastern Tropical Pacific and these differences could be due to several causes. First, the number, diversity and depth of research efforts influence the extent of the knowledge of the marine biodiversity of a region. Second, the extent of each region will also have an effect on species diversity, because larger areas will probably include more habitats and environments, and thus species. The ACG marine area comprises 430 km 2 , while the Gulf of California has about 160000 km 2 . Third, some sites may differ in species richness and diversity because of differences in geomorphology, oceanography, geological history and biogeography. Fourth, natural disturbances such as warming or cooling events can have a long-term impact on local biodiversity.
Knowing and documenting which species occurs where is a critical first step in understanding and conserving the biodiversity of a particular area. As outlined in Tables 3 and 4, there are important gaps in our knowledge in taxonomy and geographic distribution of marine organisms in the ACG. Much more work is needed to have an even approximately complete inventory, understand the ecological role of the species, their habitats, population structure, and distribution. Researchers of the BioMar-ACG project will fill many of these gaps, and together with other researchers from Costa Rica and elsewhere, the understanding of the marine biodiversity of the ACG will increase greatly. The BioMar project incorporates several innovative aspects, including marine parataxonomists, DNA barcoding of all organims and fast accessibility of the information. This project could serve as a viable model for marine biodiversity inventory in other Costa Rican conservation areas and in other countries. entire manuscript by Arturo Angulo, Rocío Córdoba, Cindy Fernández-García, Kimberly García-Méndez, Dan Janzen, Frank Joyce, Carolina Sheridan-Rodríguez, Jeffrey Sibaja-Cordero, Rita Vargas-Castillo, and the journal's editor and reviewers. Finally, I thank the government of Costa Rica, the Wege Foundation of Grand Rapids, Michigan, and the Guanacaste Dry Forest Conservation Fund (GDFCF; http://www.gdfcf.org) for proving the funds for the BioMar ACG project and for the publication of this paper. . Species in bold type reported only for the ACG in Costa Rica (in the case of bacteria some have been reported in people but not in marine organisms). Localities as in Figure 1 and Table 1. Localities in bold type = a ) Type locality, b ) Paratype locality and c ) Neotype specimen. References numbered as in the reference list. Portatrochammina pacifica (Cushman, 1925) as Trochammina pacifica BSE 50