New records of marine decapods and stomatopods in Área de Conservación Guanacaste (ACG): four years of marine biodiversity inventorying

The marine area of Área de Conservación Guanacaste (ACG) contains a 43,000 ha formal marine protected area, a 732 ha special management zone in Bahía Santa Elena, and 150 km of wild protected coastline. In an effort to broaden the biodiversity knowledge of all marine taxa present in the area, an inventory was started in 2015 (BioMar-ACG Project). This initiative is being funded by the Guanacaste Dry Forest Conservation Fund (GDFCF) in collaboration with government staff at ACG, and is carried out by Centro de Investigación en Ciencias del Mar y Limnología (CIMAR, Center for Research in Marine Science and Limnology) and Museo de Zoología (Zoology Museum), both from Universidad de Costa Rica (UCR). After four years of the project, 2650 specimens of marine decapod crustaceans and stomatopods have been collected, belonging to 209 species, out of which 99 are new records for ACG, four may be new species and nine (Cyrtoplax panamensis, Glyptoxanthus labyrinthicus, Pachyches marcortezensis, Petrolisthes donadio, Pylopagurus holmesi, Synalpheus pinkfloydi, Typton granulosus, Zenopontonia soror, Neogonodactylus pumilus) are new records for Costa Rica. With this contribution the total number of decapods (257 spp.) and stomatopods (14 spp.) for ACG is 271 species, more than half the species reported for Costa Rica, and more than a quarter of all crustaceans reported for the eastern tropical Pacific. The high concentration of species in ACG may be attributed to the diversity of habitats, the seasonal upwelling and to the recent sampling efforts. In only four years, the BioMar-ACG has increased the number of species in these groups of crustaceans by 37% over the past 85 years of previous studies in the ACG.


Introduction
The first study of marine decapods of Costa Rica was completed by Faxon (1895), and on stomatopods by Schmitt (1940) and Reaka and Manning (1980). Compilations of the biodiversity of marine decapod crustaceans and stomatopods in Costa Rica began with a publication by Moran and Dittel (1993), with an annotated list of anomuran and brachyuran crabs from the Pacific and Caribbean coasts. Castro and Vargas (1996) published an annotated list of decapods and stomatopods from Golfo Dulce, while Vargas and Cortés (1997) a list of stomatopods of the country. Afterwards, two other compilations on crustaceans were published for Penaeoidea, Sergestoidea, Caridea, Astacidea, Thalassinidea and Palinura in the Caribbean (Vargas and Cortés 1999a) and in the Pacific (Vargas y Cortés 1999b). Vargas and Cortés (2006) published a compilation of the Infraorder Anomura. Some years later, compilations were published in the book "Marine Biodiversity of Costa Rica, Central America" (Wehrtmann and Cortés 2009), which examines all groups of marine organisms reported for Costa Rica. Chapters include all crustacean groups known to be present in this country on the Pacific and Caribbean, including the best-known taxa: stomatopods (35 spp.) ) and decapods (549 spp.) (Vargas and Wehrtmann 2009).

Área de Conservación Guanacaste (ACG) includes several terrestrial National Parks and Reserves and a Marine
Sector that is 43,000 ha and 150 km of protected coastline (http://www.acguanacaste.ac.cr/acg/que-es-el-acg). It is one of the best-studied conservation areas in Central America, but previous biological research has    (Cortés & Joyce in prep). The project has also received necessary support from the government staff of ACG, local marine "parataxonomists" supported by GDFCF and private foundations. Following the compilation on marine biodiversity in ACG published by Cortés (2017), this paper presents an update of the inventory of marine decapod crustaceans and stomatopods, with new records for ACG as well as new records for the country. This is the result of work from mid 2015 to early 2019 by the BioMar-ACG project.

Methodology
Sixty sites were visited in ACG, from Punta Descartes to Islas Murciélago (Table 1), including rocky beaches (most common) and muddy beaches, shallow and deep reefs, shallow and deep rocky areas, estuaries, mangroves and areas deeper than 45 m. The location, geographic coordinates, depth and substrate type were registered.
In the rocky beaches during low tide, rocks were lifted to collect the organisms that live beneath them and the substrate was dug up to collect the organisms that live buried in the sediments. In the muddy beach areas, organisms were also collected from the mud. To collect the organisms that live within coral reefs, an indirect method was used: dead coral rocks were brought to the surface and broken apart to collect the organisms that mutually live inside. A similar method was used areas of rocky ocean floor, where collected specimens were brought to the surface. In the mangroves, specimens  were collected during walks in the forest and intertidal zone, and they were taken from the roots and ground. Using a shovel, the substrate was dug up and sifted to look for those organisms that live buried in the mud. In the external part of the mangrove, a similar process was followed, but also fallen leaves and tree trunks were examined for organisms. Deep dredging sampling (down to 50 m depth) was carried out with a Van Veen dredge with a 25 × 25 cm opening. Other organisms were manually collected during dives, and some samples of crustaceans were associated with octocorals. Collected specimens were placed in plastic containers with a net and then submerged in a bucket filled with seawater. Afterwards, the organisms were photographed in an improvised lab, a code was assigned to each specimen, a preliminary identification was provided and a sample of tissue was taken for barcoding. Once this process was finished, the organisms were sent to the Zoology Museum at Universidad de Costa Rica, where a definite identification was provided and the samples were catalogued and stored. The names of the species used are as in WoRMS (http://www.marinespecies.org).

Results and discussion
By early 2019, 2650 specimens have been collected (Table 2), corresponding to 209 species, 99 of which are new records for ACG, four could be new undescribed species, and nine are also new records for Costa Rica: Cyrtoplax panamensis (Fig. 1a), Glyptoxanthus labyrinthicus (Fig. 1b), Neogonodactylus pumilus (Fig. 1c), Pachyches marcortezensis (Fig. 1d), Petrolisthes donadio (Fig. 1e), Pylopagurus holmesi (Fig. 1f), Synalpheus pinkfloydi (Fig. 1g), Typton granulosus (Fig. 1h) and Zenopontonia soror (Fig. 1i). Cortés (2017) reported 172 species from ACG, 162 decapods and 10 stomatopods. In this study 209 species have been collected so far, 200 decapods and 9 stomatopods. Of the decapod species reported by Cortés (2017), 57 species of decapods and 5 species of stomatopod have not been collected yet. These belong mainly to organisms commonly found at depths greater than 40 m, that were collected by dredging. Taking this into account, the total number of species found in the area is 271, which includes 257 decapods and 14 stomatopods. During the last four years since the BioMar-ACG project started, 99 new records have been added to the known species from ACG (Table 2) This represents an increase of 37% over the almost 85 years of previous studies in the region.
The number of species of decapods and stomatopods reported for ACG (271) is the highest number found in Costa Rica and among the highest reported in the eastern tropical Pacific ETP (Table 3). The ETP extends from the Gulf of California to southern Ecuador and include several oceanic islands (Robertson and Kramer 2009). ACG has more than half the species reported for Costa Rica and about a quarter of decapods and stomatopods crustaceans reported for the ETP (Boschi 2000;Cortés et al. 2017) (Table 3). The high diversity of decapods and stomatopods at ACG may be due to the diversity of habitats: beaches of different wave and sediment regimes, islands and continental shorelines, mangrove forests, seagrass beds, coral reefs (live and dead), intertidal and submerged rocky platforms, sandy and muddy bottoms and deep areas (Cortés 2017). The region is exposed to season upwelling, with temperatures ranging from 15°to 30°C (Cortés et al. 2014). And finally, the sampling effort makes a difference in how many species are reported from an area, as demonstrated in this paper.
Up to now 60 sites have been sampled, with many more still to explore, such as the coastal area of Península Santa Elena, south of Playa Naranjo and offshore, as well as some habitats such as sandy beaches, and deep rocky and muddy bottoms. Definitely more species of decapods and stomatopods will be found increasing the biodiversity of crustaceans in Área de Conservación de Guanacaste.

Conclusions
The model for marine biodiversity inventory developed with the BioMar-ACG project, the partnership between government, academia, private funding and local parataxonomists, accelerates the rate of species discovery and reporting. It also makes species information and project results available in an open access format. In only for years of the project the number of decapods and stomatopods of ACG increased by 37% over the past 85 years of previus studies, for a total of 271 species. This number represnets more than half the species reported for Costa Rica, and more than a quarter of all decapods and stomatopods reported for the eastern tropical Pacific.