Abstract
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.
Similar content being viewed by others
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.) (Vargas 2009) 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 focused primarily on the terrestrial part. In order to expand the knowledge of marine biodiversity in this region, the project entitled “Marine Biodiversity of Área de Conservación Guanacaste” (BioMar-ACG) was launched in 2015. The project has been funded by the Guanacaste Dry Forest Conservation Fund (GDFCF), and carried out by the Centro de Investigación en Ciencias del Mar y Limnología (CIMAR) and Museo de Zoología, both from Universidad de Costa Rica (UCR) (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.
New records of crustaceans for Costa Rica, with their BioMar-ACG sample code: (a) Cyrtoplax panamensis,, 17-BMACGRV-02644-ACG001862; (b) Glyptoxanthus labyrinthicus, 16-BMACGRV-02104-ACG005676; (c) Neogonodactylus pumilus, 16-BMACGRV-02407-ACG006086; (d) Pachyches marcortezensis, 15-BMACGRV-00507-ACG006967; (e) Petrolisthes donadio, 16-BMACGRV-02177-ACG009006; (f) Pylopagurus holmesi, 16-BMACGRV-02414-ACG007167; (g) Synalpheus pinkfloydi, 16-BMACGRV-02245-ACG003908; (h) Typton granulosus, 16-BMACGRV-01941-ACG001783, and (i) Zenopontonia soror, 15-BMACGRV-00590-ACG009037
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.
Resumen
El sector marino del Area de Conservación Guanacaste (ACG) posee 43,000 ha y 150 km de costa, en su mayoría poco estudiada. En un esfuerzo por conocer mejor la biodiversidad de todos los taxones marinos presentes en el área, se inicio en el 2015 un inventario (Proyecto BioMar-ACG). Esta iniciativa está siendo sustentada por la Guanacaste Dry Forest Conservation Fund (GDFCF) y desarrollada por el Centro de Investigación en Ciencias del Mar y Limnología (CIMAR) y el Museo de Zoología, ambos de la Universidad de Costa Rica (UCR). Transcurridos cuatro años del proyecto, se han recolectado 2650 especímenes de crustáceos decápodos y estomatópodos marinos pertenecientes a 209 especies, de las cuales 99 son nuevas para el ACG, cuatro podrían ser nuevas especies para la ciencia y nueve (Cyrtoplax panamensis, Glyptoxanthus labyrinthicus, Pachyches marcortezensis, Petrolisthes donadio, Pylopagurus holmesi, Synalpheus pinkfloydi, Typton granulosus, Zenopontonia soror y Neogonodactylus pumilus) son ampliaciones de ámbito y nuevos informes para el país. Con esta contribución aumenta el número de decápodos a 257 spp. y de estomatópodos a 14 spp. para un total de 271 spp. para ACG. Esto es más de la mitad las especies conocidas de estos grupos para Costa Rica y más una cuarta parte de las especies conocidas para el Pacífico Tropical Oriental. En cuatro años el proyecto BioMar-ACG ha aumentado el número de especies de decápodos y estomatópodos del ACG en 37% más que lo que se conocía a partir de estudios en los últimos 85 años.
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.
Availability of data and materials
Data will be made available in the project website. The specimens are deposited in the Museo de Zoología, Universidad de Costa Rica, and can be checked there.
References
Bastida-Zavala JR, del S G-MM, Rosas-Alquicira EF, López-Pérez RA, Benítez-Villalobos F, Meraz-Hernando JF, Torres-Huerta AM, Montoya-Márquez A, Barrientos-Luján NA. Marine and coastal biodiversity of Oaxaca, Mexico. Check List. 2013;9:329–90.
Boschi E. Species of decapod crustaceans and their distribution in the American marine zoogeographic provinces. Rev Invest Des Pesq. 2000;13:1–63.
Castro M, Vargas R. Annotated list of species of marine crustaceans (Decapoda and Stomatopoda) from Golfo Dulce, Costa Rica. Rev Biol Trop. 1996;44(Suppl 3):87–95.
Cortés J. Marine biodiversity of an eastern tropical Pacific oceanic island, Isla del Coco. Costa Rica Rev Biol Trop. 2012;60(Suppl 3):131–85.
Cortés J. Marine biodiversity baseline for Área de Conservación Guanacaste, Costa Rica: published records. ZooKeys. 2017;652:129–79. https://doi.org/10.3897/zookeys.652.10427.
Cortés J, Enochs IC, Sibaja-Cordero J, Hernández L, Alvarado JJ, Breedy O, Cruz-Barraza JA, Esquivel-Garrote O, Fernández-García C, Hermosillo A, Kaiser KL, Medina-Rosas P, Morales-Ramírez Á, Pacheco C, Pérez-Matus A, Reyes-Bonilla H, Riosmena-Rodríguez R, Sánchez-Noguera C, Wieters E, Zapata FA. Marine biodiversity of eastern tropical Pacific coral reefs. In: Glynn PW, Manzello D, Enochs I, editors. Coral reefs of the eastern Pacific: persistence and loss in a dynamic environment. Dordrecht: Springer Science+Business Media; 2017. p. 203–50.
Cortés J, Samper-Villarreal J, Bernecker A. Seasonal phenology of Sargassum liebmannii J. Agardh (Fucales, Heterokontophyta) in an upwelling area of the eastern tropical Pacific. Aquat Bot. 2014;119:105–10.
Cortés J, Vargas-Castillo R, Nivia-Ruiz J. Marine biodiversity of Bahía Culebra, Guanacaste, Costa Rica: published records. Rev Biol Trop. 2012;60(Suppl 2):39–71.
Faxon W. Reports on an exploration off the west coast of México, Central and South America, and off the Galápagos Islands by the U.S. Fish Commission Steamer “Albatross”, during 1891. XV. The stalk-eyed Crustacea. Mem Mus Comp Zool. 1895;18:1–292.
Hendrickx ME. Chapter 10. Crustacea 2: Stomatopoda. In: Hendrickx ME, Brusca RC, Findley LT, editors. A distributional checklist of the macrofauna of the Gulf of California, Mexico. Tucson, Arizona: Part I. Invertebrates. Arizona-Sonora Desert Museum; 2005a. p. 127–30.
Hendrickx ME. Chapter 14. Crustacea 6. Decapoda: Dendrobranchiata, Caridea, Palinura, Anomura & Brachyura. In: Hendrickx ME, Brusca RC, Findley LT, editors. A distributional checklist of the macrofauna of the Gulf of California, Mexico. Tucson, Arizona: Part I. Invertebrates. Arizona-Sonora Desert Museum; 2005b. p. 159–94.
Hickman CP, Zimmerman TL. A field guide to the crustaceans of Galápagos. Lexington, Virginia: Galápagos Marine Life Series, Sugar Spring Press; 2000.
Lemaitre R, Álvarez-León R. Crustáceos decápodos del Pacífico colombiano: Lista de especies y consideraciones zoogeográficas. An Inst Inv Mar Punta Betín. 1992;21:33–76.
López RH, Jaimes JC. Aspectos de la distribución larval de Stomatopoda (Crustaacea) en aguas superficiales del pacífico colombiano. Rev UDCA Actual Divulg Cient. 2014;17:227–36.
Morales-Ramírez A. La diversidad marina del Golfo Dulce, Pacífico sur de Costa Rica: amenazas a su conservación. Biocenosis. 2011;24:9–20.
Moran DA, Dittel AI. Anomuran and brachyuran crabs of Costa Rica: annotated list of species. Rev Biol Trop. 1993;41:599–617.
Poupin J, Bouchard J-M, Albenga L, Cleva R, Hermoso-Salazar M, Solis-Weiss V. Les crustacés décapodes et stomatopodes, inventaire, écologia et zoogéographie. In: Charpy L (ed) Clipperton, environnement et biodiversité d’un microcosme océanique. Patrim Nat. 2009;68:163–216.
Reaka ML, Manning RB. The distributional ecology and zoogeographical relationships of stomatopod Crustacea from Pacific Costa Rica. Smithson Contr Mar Sci. 1980;7:1–29.
Robertson DR, Cramer KL. Shore fishes and biogeographic subdivisions of the tropical eastern Pacific. Mar Ecol Prog Ser. 2009;380:1–17.
Salgado-Barragán J, Hendrickx ME. Clave ilustrada para la identificación de los estomatópodos (Crustacea: Hoplocarida) del Pacífico oriental. Rev Mex Biodiv. 2010;81:S1–S49.
Schmitt WL. The stomatopods of the west coast of America based on collections made by the Allan Hancock expeditions, 1933-38. Allan Hancock Pac Exp. 1940;5:129–225.
Vargas R. Stomatopods. In: Wehrtmann IS, Cortés J, editors. Marine biodiversity of Costa Rica, Central America. Dordrecht: Springer & Business Media BV; 2009. p. 193–7. https://doi.org/10.1007/978-1-4020-8278-8_17.
Vargas R, Cortés J. Biodiversidad marina de Costa Rica: Orden Stomatopoda (Crustacea: Hoplocarida). Rev Biol Trop. 1997;45:1531–9.
Vargas R, Cortés J. Biodiversidad marina de Costa Rica: Crustacea: Decapoda (Penaeoidea, Sergestoidea, Stenopodidae, Caridea, Thalassinidea, Palinura) del Caribe. Rev Biol Trop. 1999a;47:877–85.
Vargas R, Cortés J. Biodiversidad marina de Costa Rica: Crustacea. Decapoda (Penaeoidea, Sergestoidea, Caridea, Astacidea, Thalassinidea, Palinura) del Pacífico. Rev Biol Trop. 1999b;47:887–911.
Vargas R, Cortés J. Biodiversidad marina de Costa Rica: Crustacea: Infraorden Anomura. Rev Biol Trop. 2006;54:461–88. https://doi.org/10.15517/rbt.v54i2.13894.
Vargas R, Wehrtmann IS. Decapods crustaceans. In: Wehrtmann IS, Cortés J, editors. Marine biodiversity of Costa Rica, Central America. Dordrecht: Springer & Business Media BV; 2009. p. 209–28. https://doi.org/10.1007/978-1-4020-8278-8_19.
Vargas-Castillo R, Wehrtmann IS. Stomatopods and decapods from Isla del Coco, Pacific Costa Rica. Rev Biol Trop. 2008;56(Suppl 2):79–97.
Wehrtmann IS, Cortés J (eds) (2009) Marine biodiversity of Costa Rica, Central America. Dordrecht: Springer & Business Media BV.
Acknowledgements
The authors acknowledge and thank the following people and organizations for their efforts and significant support to the BioMar-ACG project: Daniel Janzen, Winnie Hallwachs, Frank Joyce, María Marta Chavarría, Roger Blanco, Eric Palola, Yelba Vega, Gilberth Ampie, Diving Center Cuajiniquil, the Santa Elena Lodge, the Guanacaste Dry Forest Conservation Fund, the Wege Foundation, the New England BioLabs Foundation, the Wallace Genetic Foundation and the Centre for Biodiversity Genomics, University of Guelph. We thank Francilena Carranza for preparing the photographs and Eric Palola and anonymous reviewers for the review of the manuscript. Michel E. Hendrickx was very helpful in the preparation of the reviewed draft of the paper.
Funding
Funding source indicated in the Acknowledgement section.
Author information
Authors and Affiliations
Contributions
RV collected and identified the specimens, wrote a first draft of the manuscript. JC, conceived the main project, helped with logistics and obtaining the funds, wrote some sections of the paper, helped prepared the images and the final draft of the paper. All authors read and approved the final manuscript.
Authors’ information
Rita Vargas: Collection Manager and curator of Crustaceans of the Zoology Museum of the University of Costa Rica.
Jorge Cortés: Senior researcher at the Center for Research in Marine Science and Limnology, and professor at the School of Biology, both at the University of Costa Rica.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
About this article
Cite this article
Vargas-Castillo, R., Cortés, J. New records of marine decapods and stomatopods in Área de Conservación Guanacaste (ACG): four years of marine biodiversity inventorying. Mar Biodivers Rec 12, 21 (2019). https://doi.org/10.1186/s41200-019-0181-6
Received:
Accepted:
Published:
DOI: https://doi.org/10.1186/s41200-019-0181-6