Decapod crustaceans are a diverse group that exploits various types of habitats in Costa Rica, where they represent 8.1% of the marine diversity of the country. This group includes families containing species with strictly symbiotic behavior, e.g., the Palaemonidae and Pinnotheridae. Despite the high diversity of decapods and the importance of symbionts in marine ecosystems, very little research has been done regarding symbiosis in Costa Rica and the Central American region. The objective of the present study is to present a check list of the species of decapods that are associated with macroinvertebrates in Pacific Costa Rica. The research was carried out using different sources, including a literature review, the Crustaceans Collection of the Zoology Museum of the University of Costa Rica, and field surveys between 1970 and 2019 along the Pacific coast of Costa Rica, and Isla del Coco, 500 km offshore. One-hundred associations are reported, of 74 species of symbiotic decapods with six host phyla. Seventy-four associated with Cnidaria, 15 with Echinodermata, four each with Annelida and Mollusca, two with Chordata, and one with Porifera. In total, there were 14 new reports of decapods occurring on Isla del Coco and four new reports of decapods for Costa Rica: Pseudocoutierea elegans, Raytheres clavapedatus, Tuleariocaris holthuisi, and Calyptraeotheres pepeluisi. These results highlight the need to conduct more detailed studies to determine the real diversity and ecological importance of the associations between marine organisms.
The diversity of decapod crustaceans is directly correlated with the abundance of habitats exploited by these organisms, including continental waters, intertidal zones, coral reefs, the deep sea and even the body cavities of other marine organisms (Bruce 1976; Martin and Davis 2001; Macedo et al. 2012; Sal Moyano et al. 2012; Baeza 2015). The different species expend a great deal of energy in habitat selection because the location that they choose should not only allow them to survive, but also to reproduce (Anthony and Cannolly 2004). In their search for shelter, many of these animals are exposed to the presence of spatially and temporarily limited resources. Some of these resources include aggregations of seastars, sea urchins, mussels, algal mats, and kelp forests, among others (Baeza et al. 2002; Ory et al. 2013). The characteristics of the habitat, predation and interspecific competition encourage great specificity of habitat selection and are even considered to be drivers of symbiotic relationships (Montfrans et al. 2003; Baeza 2007; Ory et al. 2013). Symbiosis is a very common type of interaction in marine ecosystems (Thiel and Baeza 2001; Sotka 2005; Baeza 2007; Glynn 2013). It has been defined as “the living together of unlike organisms” (De Bary 1879). Other definitions include the factor of time, since these associations can extend through a part or the entirety of the lifecycle of one or both organisms (Starr et al. 2009).
In Costa Rica, there are 591 species of decapods, 8.1% of the known marine biodiversity of the country in both oceans (Vargas and Wehrtmann 2009; Wehrtmann et al. 2009). The families in this group with the greatest species richness in Pacific Costa Rica are Xanthidae (45 spp.), Porcellanidae (44 spp.), Majidae (43 spp.), Alpheidae (34 spp.), Ocypodidae (28 spp.) and Palaemonidae (23 spp.) (Vargas and Wehrtmann 2009). Similarly, of the 1688 marine species reported for Isla del Coco, 8.2% are decapods (Cortés 2012). Some decapod species are adapted for symbiotic behavior. Among the most well-known groups for establishing associations with other species are the families Palaemonidae, Alpheidae, Pinnotheridae and Porcellanidae (Baeza 2007). The decapods that live in association with other animals in Costa Rica have been scarcely studied and in most publications they are only mentioned in species lists with no indication of their association with other organisms. The objective of the present study is to present a compilation of species of decapod crustaceans associated with macroinvertebrates in the Pacific of Costa Rica.
Materials and methods
This study includes specimens collected in different locations, associated with different biological substrates, along the Pacific coast of Costa Rica, including from the north, Bahía Salinas and Gulf of Papagayo; to the Central Pacific coast: Gulf of Nicoya; and to the south: Golfo Dulce; as well as different sites around Isla del Coco National Park (Fig. 1, Table 1). These sites have different levels of protection and the health status of their ecosystems differs considerably (Cortés 2016a, b).
Locations along the northern coast (Bahía Salinas, Bahía Cuajiniquil, Islas Murciélago and Bahía Culebra) are under the influence of a seasonal coastal upwelling (McCreary et al. 1989; Alfaro et al. 2012). The coral ecosystems in Bahía Cuajiniquil in the Gulf of Santa Elena are dominated by the genus Pocillopora, and the species Porites panamensis and Pavona gigantea, while the reefs in Bahía Salinas are basically made up of P. gigantea (Cortés et al. 2010). In the reefs of Bahía Culebra, coral cover is under 1%; this ecosystem is in a phase shift, where some macroalgae have increased their abundance and become dominant, e.g., Caulerpa sertularioides (Fernández-García et al. 2012; Arias-Godínez et al. 2019). Several collections were done at the Islas Murciélago, an archipelago in Área de Conservación Guanacaste (Cortés 2017). In the Gulf of Nicoya, specimens were obtained from the coral communities of Isla Tortuga, where coral cover is below 5% and of low diversity (Alvarado et al. 2018), as well as from the intertidal mudflat of Punta Morales, where polychaete worms and ostracods predominate (Vargas 1987). Punta Nicuesa is a coral community with one of the highest covers of live coral along the southern Pacific coast (up to 83.4%) (Alvarado et al. 2015). Isla del Coco is the site with the greatest protection in Pacific Costa Rica; coral cover there is reported to be 18.64 ± 3.55% (Alvarado et al. 2016a; Cortés 2016b).
Collection of specimens was carried out in a targeted way. The available environments of most sites were explored from the intertidal zone to ~ 30 m deep, including mudflats, sandy beaches and rocky shores, coral and rocky reefs, rhodolith beds and subtidal soft bottoms. Different organisms that are known to be decapod hosts were collected and accommodated in separate plastic bags. Each of the collected specimens underwent a detailed visual inspection and the water was filtered to separate possible decapod symbionts. In general, echinoids, asteroids, holothuroids, octocorals and scleractinian corals were collected and externally inspected, while the interiors of the bivalves were inspected. Occasionally, sponges and annelids were collected. Most of the samples were collected manually in the intertidal zone and by scuba diving in the subtidal environments (Table 1). In the case of Isla del Coco, samples from two dives in the submarine DeepSee (Cortés and Blum 2008; Cortés 2019) that explored rocks in deep locations (between 60 and 280 m) were inspected. The sampling was opportunistic, which means that search efforts were not the same to all sites.
Our results include a species list of collected decapods associated with other organisms along the Pacific of Costa Rica, and their relative abundance. In addition, information is included from specimens collected in the Costa Rican Pacific, both on the coast and in Isla del Coco, which were in the collection of the Zoology Museum, University of Costa Rica (MZUCR, for its abbreviation in Spanish). These collections were carried out between 1970 and 2019; they included the intertidal zone, scuba diving to 40 m, dives of the submarine DeepSee to depths between 60 and 280 m and a dive of the submarine ALVIN to 1000 m deep (Tables 1 and 2). The list that is presented also includes the decapod associations that have previously been reported in the literature for Pacific Costa Rica. Species identification were done using Rathbun (1918, 1930, 1931), Holthuis (1951), Haig (1960), Williams (1986), Kim and Abele (1988), Kropp (1989), Ramos (1995), Castro (1996), Hendrickx (1999), Vargas (2000), Thoma et al. (2005), Marín and Anker (2009), Campos and Hernández-Ávila (2010). All names are according to WoRMS (http://www.marinespecies.org, last accessed 14 December 2020).
One-hundred associations are reported, which include 74 species of decapods are guests of six phyla of hosts (Table 1). The phylum with the most associated decapods was Cnidaria, with 74 species i.e., 74% of the total), followed by Echinodermata with 15 species, and four each with Annelida and Mollusca, two with Chordata, and one with Porifera. The host order with the greatest diversity of associated decapods was Scleractinia (Table 1). The species that showed the most associations with different hosts was Zenopontonia soror, which was found in five species of seastars (Table 1). This species was recently reported new to Costa Rica by Vargas-Castillo and Cortés (2019). The shrimp Pseudocoutierea elegans was found in hosts from three groups (Octocorallia, Hydrozoa, and Echinoidea). On the other hand, Tetrias scabripes was found associated solely with polychaetes (Table 1).
Of the associations recorded 59% were rare, that is, we observed them in a few occasions or with few individuals. While 36% of the associations were observed many times and with several members of the symbiont species on the host. Four relations were very abundant, three of them, Hemus finneganae, Stenorhynchus debilis and Pachygrapsus transversus with hard corals, and Austinotheres angelicus with a bivalve. On the other extreme was Pontonia simplex of which we found only one specimen in a bivalve. Tuleariocaris holthuisi, associated with two species of sea urchins, was seasonally abundant but rare at other times. A species that was abundant was always abundant, with very few exceptions, Megalobrachium tuberculipes and Pseudoveleronia laevifrons were abundant in one species of octocoral, Eugorgia mutabilis, but not in other octocorals. Symbiotic species were usually associated to the same species or group of related species, being an exception P. elegans that was abundant in an octocoral, a calcareous hydroid and a sea urchin (Table 1).
In total, 74 species of symbiotic decapods have been discovered in Pacific Costa Rica, 13 anomurans, two axiidids, 34 brachyurans, 24 carideans, and one gebiidid (Table 2). The family with the most symbiotic species was Palaemonidae (20 spp.), followed by the families Pinnotheridae and Porcellanidae, with nine species each. The genus with the most species was Trapezia with four, followed by Periclimenes with three. Fourteen new reports of decapods were recorded for Isla del Coco along with the occurrence of four new decapod records for Pacific Costa Rica, Calyptraeotheres pepeluisi Campos and Hernández-Ávila 2010, Raytheres clavapedatus (Glassell, 1935), Tuleariocaris holthuisi Hipeau-Jacquotte 1965 and Pseudocoutierea elegans Holthuis 1951. This is the first time that the genus Calyptraeotheres is reported in Costa Rica (Table 2).
In the following section, the associations are detailed according to the type of host (Table 1).
In this study, only the species Panopeus chilensis is reported to be associated with an intertidal sponge, genus Halichondria. However, this is probably because the few studies on sponges have not focus on documenting the associated organisms.
Fifty-six species of decapods, distributed in five orders, 23 families and 50 genera, were found associated with 21 species of cnidarians. Opecarcinus crescentus has only been found in Pavona gigantea, while Alvarado and Vargas-Castillo (2012) reported 16 species of decapods associated with Pocillopora damicornis, all of which are typically found with this host. Six additional species are reported associated to Pocillopora sp. Seven species were found living on Porites lobata and one, Platypodiella rotundata, exclusively on Tubastraea coccinea. Fifteen species were found associated with Antipatharia. The two species associated with Antipathes sp. were also found in Myriopathes panamensis. Only one associated deep-water decapod, Coralaxius galapagensis, was found on Lillipathes ritamariae. In Octocorallia, 22 associated species were found. Eugorgia mutabilis was the host with the greatest diversity of decapods, six. The two most common decapods in octocorals were Neopontonides henryvonprahli and Pseudoveleronia laevifrons; four crustaceans could not be identified to species. In the hydrozoans, symbionts have only been collected from Stylaster marenzelleri, where Munida sp. and Pseudocoutierea elegans were found.
Four species of decapods, distributed in two orders, two families and three genera, were found associated with four species of molluks. Symbionts have been found primarily in bivalves. In specimens of the pearl oyster Pinctada mazatlanica, pairs of the shrimp Pontonia margarita have been found living inside the oyster on numerous occasions; P. simplex was found in Pinna rugose. In the oyster, Saccostrea palmula, the pinnotherid crab Austinotheres angelicus has been reported as a guest with a prevalence of 38% (Mena et al. 2014). Only pairs of Calyptraeotheres pepeluisi were found living in the interior of the gastropod Crepidula sp. on the mangrove roots at Punta Morales.
Four species of decapods, distributed two orders, two families and four genera, were found associated with three species of polychaetes. The tubes of one species of Onuphidae, one species of Terebellidae and the tube of an unidentified family were inspected in the intertidal zone of Punta Morales, Gulf of Nicoya. The Pinnotheridae crab, Glassella costaricana was found associated with the polychaete Lanicola sp. The species Pinnixa longipes and Polyonyx quadriungulatus were found in the tube of the onuphids.
Nine species of decapods, distributed in two orders, four families and nine genera, were found associated with 12 species of echinoderms. These species were observed living as epibionts in four species of echinoids and five species of asteroids (Table 1). On the sea star Asteropsis carinifera, three species were found: Pachycheles biocellatus, Zenopontonia soror and Calyptraeotheres sp., while in the sea star Pentaceraster cumingi and the sea urchin Diadema mexicanum, several individual symbionts of both sexes and in different stages of development were found in a single host individual. Symbiotic decapods were found both in solitary and in aggregated echinoderms, such as Astropyga pulvinata and D. mexicanum in reef sites in Bahía Culebra, the sea star Nidorellia armata in rocky reefs close to Playa Rajada, Bahía Salinas, the sea star Pentaceraster cumingi on soft bottoms near reefs in Golfo Dulce. Aggregates of P. cumingi are common in the rhodolith beds of Isla del Coco, however, no decapods were found associated.
The shrimp Z. soror was found in the five sea star species collected, which belong to the families Oreasteridae (N. armata and P. cumingi), Ophidiasteridae (Pharia pyramidata and Phataria unifascialis) and Asteropsidae (A. carinifera). The shrimp Tuleariocaris holthuisi was found associated with two species of sea urchins of the family Diadematidae (A. pulvinata and D. mexicanum) in Bahía Culebra. Finally, a female of Gnathophylloides mineri was found associated with Tripneustes depressus in Bahía Wafer, Isla del Coco, at a depth of 8 m.
Only one species of decapod, A. pusilla, was found associated with two species of ascideans. In 1970, Ascidonia pusilla was collected from specimens of the recently described ascidian Rhopalaea birkelandi from Playas del Coco, Bahía Culebra (Fujino 1972), and was described as Pontonia spighti. A specimen of A. pusilla was found in association with an unidentified sea squirt (Ascidiacea) from Isla Bolaños, northern Pacific Costa Rica.
Symbiotic decapods in Isla del Coco
In total, 28 associations of 24 species of decapods, in five ordens and 17 families, were found at Isla del Coco. Of the species found, 10 belong to the infraorder Brachyura and 10 to the infraorder Caridea, associated with nine orders distributed among four phyla (Tables 1 and 2).
In Costa Rica, few studies have focused on symbiotic decapods, with the majority carried out in the Pacific and only one in the Caribbean (Azofeifa-Solano et al. 2014). Most of these studies were focused on reproductive aspects of decapod guests. Fifty percent of the studies deal with pea crabs (Pinnotheridae), 35% are about the shrimp family Palaemoniidae, and the remaining 15% are derived from studies of the diversity of organisms associated with the coral P. damicornis (Cabrera-Peña and Solano-López 1996; Cabrera-Peña et al. 2001; Alvarado and Vargas-Castillo 2012; Azofeifa-Solano et al. 2014; Mena et al. 2014; Salas-Moya et al. 2014). There is a need for more detailed studies of decapod crustaceans associated with macroinvertebrates.
In this study, T. holthuisi is reported from Bahía Culebra, where 24 individuals (juvenile, adult, egg bearing females, females without eggs and males) were associated with D. mexicanum and A. pulvinata collected in 2013 and 2014. This species is distributed from the east coast of Africa (Hipeau-Jacquotte 1965; Bruce 1982), the north east of Australia (Bruce 1990) and in Tahiti (J. Poupin pers. comm. in Marín and Anker 2009). It has also been found in Baja California, Mexico, where two individuals were collected (Wicksten and Hernández 2000) and in Isla Coiba, Panama, where an egg-bearing female was captured (Marín and Anker 2009). Bruce (1982) reported that T. holthuisi was found in different species of sea urchins in the Indo-Pacific, for example Astropyga radiata, Echinothrix diadema, Stomopneustes variolaris and Echinometra mathaei. However, in the eastern tropical Pacific, T. holthuisi has only been found associated with the black sea urchin, D. mexicanum (Wicksten and Hernández 2000; Marín and Anker 2009). We have continued surveying and collecting the sea urchins D. mexicanum and A. pulvinata, but T. holthuisi has not been observed again. These results may be due to the fact that the sea urchins in Bahía Culebra displayed the highest population density levels of the eastern tropical Pacific after serious degradation of the reefs and a series of harmful algal proliferations of phytoplankton between 2005 and 2006 (Alvarado et al. 2012, 2016b). But in recent years the populations of sea urchins have declined, possibly due to the continual degradation of the reefs (Alvarado et al. 2018), which might explain the absence of T. holthuisi.
Knowledge on Psedocoutierea elegans in the region is scarce. It has been reported for the Gulf of California and in the Galapagos Islands (Holthuis 1951). Because the collection method in this case was with the submarine DeepSee, which uses an arm and single specimen container that does not permit the separation of collection events, the authors consider that it is possibly associated with the sea urchin Centrocidaris doederleini, since it has been found associated with this species on three occasions (2009, 2013, 2016). New collection surveys of C. doederleini are recommended to confirm this association at Isla del Coco. It could be assumed that P. elegans tends to be more of a generalist in its host selection due to the low availability of hosts in the deep locations where it has been found (greater than 60 m).
The shrimp Gnathophylloides mineri is the decapod that is most frequently found associated with the sea urchin T. depressus, but we found only one female. It has been reported to represent up to 94% of the decapods associated with Tripneustes ventricosus in Isla Borracha, Venezuela (Vera-Caripe et al. 2017). In Australia, the association of G. mineri with sea urchins of the genus Tripneustes has also been reported (Bruce 1988).
The anomuran (false crab or porcelain crab) Pachycheles biocellatus was found to be associated with the seastar A. carinifera. However, it is known that this crab associates primarily with corals (García-Madrigal 1999), and there are reports of the species in rocky reefs or in sites near small coral colonies (García-Madrigal 2009). Another species that was found associated with A. carinifera is the pea crab from the family Pinnotheridae, Calyptraeotheres sp. This genus has already been reported by Campos (1990) to be associated with seastars, but it is more common to find it associated with mollusks of the genus Crepidula (Campos and Hernández-Ávila 2010).
The cnidarians were the group where the most symbiont organisms were found. This result was influenced by the study done by Alvarado and Vargas-Castillo (2012), which focused on symbionts of the coral P. damicornis. Additionally, in the case of soft corals, collection of associated organisms has been carried out for many years, although not systematically. Possibly, a greater diversity of associated decapod species may be found by increasing research efforts in a systematic way.
Of the 21 species found, 14 are new reports for Isla del Coco, according to the compilation done by Cortés (2012). The host in which the greatest number of symbiotic species at Isla del Coco was the black coral, Myriopathes panamensis. Host information was recorded for some of the decapod specimens of Isla del Coco in the collection of the MZUCR but not for others, as they were not collected in targeted surveys.
A small fraction of Pacific Costa Rica was surveyed. Even so, 14 new records of decapods associated with macroinvertebrates were found in the very well-studied Isla del Coco and four new records were discovered for Costa Rica. These results highlight the need to conduct more detailed studies in which time of year, depth, physico-chemical characteristics of the water, type of environment, the abundance of symbionts and hosts, and location in the hosts. This information will help to determine the real diversity and ecological importance of the associations between marine organisms.
Availability of data and materials
Museo de Zoología (Zoology Museum), Universidad de Costa Rica database.)
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The authors are grateful for the logistical support of the Centro de Investigación en Ciencias del Mar y Limnología (Research Center in Marine Science and Limnology, CIMAR) and Museo de Zoología (Zoology Museum, MZUCR) of the Universidad de Costa Rica (University of Costa Rica). The authors also thank Conservation International for financing some of the trips, as well as Undersea Hunter Group and its crew for trips to Isla del Coco and for the use of the submarine DeepSee. The authors wish to acknowledge Jaime Nivia, Odalisca Breedy, Cindy Fernández, Sebastián Mena, Kimberly García, Andrés Beita, Cristobal Salamé, Yolanda Camacho, Fiorella Vázquez and Benjamin Chomitz for their support with collecting samples. Samples were collected under the following resolutions of the Ministry of the Environment of Costa Rica: 015-2013, 065-2013-SINAC, 2016-I-ACMIC-022, ACMIC-I-2016-012, ACMC-I-2017-06, R-SINAC-PNI-SE-002-2018, ACT-OR-DE-024-18, R-SINAC-ACG-PI-041-2019, R-SINAC-PNI-ACLAP-035-2019, 04-2019-I-ACMC. The detailed review of the manuscript by Marjorie Reaka and of an anonymous reviewer is greatly appreciated.
This work was supported with personal funds from CSM and JCAS; a grant from Conservation International to JJA; grants from the Vicerrectoría de Investigación, Universidad de Costa Rica (UCR) [Grants numbers 808–98-013, 808-A5–037] to JC, [Grants numbers 808-B3–503, 808-B6–520] to JJA; salaries from UCR to RVC, JJA, JCN; and donated space in the vessel and submarine by Undersea Hunter.
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Salas-Moya, C., Vargas-Castillo, R., Alvarado, J.J. et al. Decapod crustaceans associated with macroinvertebrates in Pacific Costa Rica. Mar Biodivers Rec 14, 6 (2021). https://doi.org/10.1186/s41200-020-00199-w
- Isla del Coco
- Coral reefs