Introduction

The Caribbean Sea is a large sea, closed off to the west and to the south by the Americas, and partly screened to the north and to the east by the island chains of the Greater and Lesser Antilles (Spalding 2004). The region extends over about 2,754,000 km2 in which 36–40 politically independent countries and territories can be found (Miloslavich and Klein 2005). Two large currents sweep towards this region from the Atlantic, the North Equatorial Current and Guyana current. A portion of their flow runs between the islands and into the Caribbean Sea, forming a generally westward flow known as the Caribbean current. The rest of the current is deflected to the northwest, fusing with the Gulf Stream (Spalding 2004).

The Caribbean is considered a unique biogeographic region. It is among the top five hotspots in the world for marine and terrestrial biodiversity, and it has many endemic species (Rivera-Monroy et al. 2004). Its complex geological history, begining 130 million years ago (Ma) and involving emergence of the Isthmus of Panama in the Pliocene (around 3.0–2.8 Ma), had major effects on the marine biodiversity. The separation of the tropical American ocean into two different realms produced isolation and environmental change that resulted in increased evolutionary divergence and radiation of species in extensive coral reefs, mangroves, seagrass beds, deep-shelf ecosystems and partially isolated deep basins and trenches (Collins 1996).

The echinoderm research on the Caribbean began in the middle of the nineteenth century with dredging explorations in Florida and Cuba (Agassiz 1869; Lyman 1869). The first half of the twentieth century increased the number of species described with collections from Puerto Rico (Clark 1901), the Lesser Antilles (Engel 1933), Jamaica (Fointaine 1953a, b, c), and the publication of monographs on groups such as Holothuroidea (Deichmann 1926, 1930, 1940, 1963). During the second half of the twentieth century research increased the number of local records in Cuba (Suárez 1974), Belize (Devaney 1974; Kier 1975; Hotchkiss 1982; Macurda 1982; Hendler and Pawson 2000), Panama (Chesher 1972), Venezuela (Zoppi de Roa 1967; Rodríguez 1969, 1973; Martínez and Mago 1975; Martínez 1987, 1989), Jamaica (Meyer 1973), Honduras (Lessios 1998; Hasbún and Lawrence 2002). During this period information on groups such as Asteroidea (Downey 1973; Clark and Downey 1992) and Crinoidea (Meyer et al. 1978) was augmented. This increase in research is partially a consequence of the work in Panama conducted by the Smithsonian Tropical Research Institution and research in other parts of the Caribbean by the Smithsonian Institution in Washington DC.

During the 1970s, there was an increase in ecological studies that continues to our times, mostly focused on Diadema antillarum (Ogden et al. 1973; Sammarco 1980, 1982a, b; Lessios et al. 1984; Lessios 2005; Weil et al. 2005; Mumby et al. 2006; Steiner and Williams 2006; among others). However, one of the most important works was the compilation by Hendler et al. (1995), containing keys, pictures and a detailed description of 144 species. It also contained general comments on their habitat, distribution and biology. In addition to taxonomy, research in the region has focused on topics such as bioerosion (Scoffin et al. 1980; Bak et al. 1984; Griffin et al. 2003; Brown-Saracino et al. 2007), biodiversity (Price et al. 1999), reproduction (Lessios 1981a; Guzmán and Guevara 2002a, b; Guzmán et al. 2003; Montealegre-Quijano and Gómez-Gaspar 2005), aquaculture (Buitrago and Lodeiros-Seijo 2005; Gómez and Gómez 2005), evolution (Lessios 1981b; Lessios et al. 2001; Lessios et al. 2003; Zigler and Lessios 2004), and competition (Parker and Shulman 1986). The majority of this research was focused on echinods. The Caribbean region likely ranks among the top tropical regions for echinoderms research.

More recently, more research has being carried out, in Colombia (Benavides-Serrato and Borrero-Pérez 2000; Benavidez-Serrato et al. 2005; Borrero-Pérez et al. 2002a, b, 2008), Cuba (Abreu-Pérez et al. 2005; Del Valle-García et al. 2005, 2008), Mexico (Laguarda-Figueras et al. 2005), Hispaniola Island (Herrera-Moreno and Betancourt 2004) and Puerto Rico (Benavides-Serrato 2006). In the past decade scientist from the Instituto de Investigaciones Marinas y Costeras (INVEMAR) have publish most on echinoderm diversity in both shallow and deep water habitats.

The aim of this review is to present an updated list of the echinoderms in the Caribbean region based on information from the literature and museum collections. A list of species is presented indicating their presence in each country, the similarities in species composition, and the possible causes of those patterns of distribution.

Material and methods

I reviewed the echinoderm species composition of the Caribbean coast from the Yucatán Peninsula in Mexico (Quintana Roo State) to Venezuela, including the arc of the Caribbean islands from Cuba to Trinidad & Tobago (Fig. 1). The ecoregions covered by this review included the Eastern Caribbean, Greater Antilles, Southern Caribbean, Southwestern Caribbean and Western Caribbean of the Tropical Northwestern Atlantic Province (Spalding et al. 2007). Existing published echinoderm studies were reviewed (Zoppi de Roa 1967; Chesher 1968, 1970; Flores and Martínez 1970; Serafy 1970; Meyer 1973; Devaney 1974; Martínez and Mago 1975; Meyer and Macurda 1976; Meyer et al. 1978; Caycedo 1978, 1979; Alvarez-Larrauri 1981; Hotchkiss 1982; Macurda 1982; Miller and Pawson 1984; Martínez 1987; Hendler 1988, 1995; Clark and Downey 1992; Hendler et al. 1995; Schoppe 1996; Lessios 1998; Benavides-Serrato and Borrero-Pérez 2000; Hendler and Pawson 2000; Pawson et al. 2001; Borrero-Pérez et al. 2002a, b; Gómez-Gaspar 2002; Gonzalez et al. 2002; Hasbún and Lawrence 2002; Fonseca and Arrivillaga 2003; Herrera-Moreno and Betancourt 2004; Abreu-Pérez et al. 2005; Benavidez-Serrato et al. 2005; Del Valle-García et al. 2005; Laguarda-Figueras et al. 2005; Benavides-Serrato 2006; Alvarado et al. 2008; Borrero-Pérez et al. 2008; Francisco and Pauls 2008), and extracted information from the Geology Collection of the California Academy of Sciences, San Francisco (http://www.calacademy.org/research/izg/iz_coll_db/index.asp). The taxa were validated with the Integrated Taxonomic Information System (http://www.itis.gov/), and the Ophiuroidea (Stöhr and O’Hara 2007) and Asteroidea databases (Mah 2009). For the taxonomic list, the criteria used in Alvarado et al. (2008) were applied.

Fig. 1
figure 1

a Caribbean Sea countries and ecoregions. b Radial diagram of the number of species of echinoderms (axes) per country on the Caribbean. Gray circle countries with under the average number of species. Ecoregions: W Western Caribbean (blue dots), SW Southwestern Caribbean (green dots), GA Greater Antilles (red dots), E Eastern Caribbean (yellow dots), S Southern Caribbean (orange dots). PRC Puerto Rico, RDO Dominican Republic, HAI Haiti, JAM Jamaica, CUB Cuba, MEX Mexico, BEL Belize, GUA Guatemala, HON Honduras, NIC Nicaragua, CRC Costa Rica, PAN Panama, COL Colombia, VEN Venezuela, TYT Trinidad & Tobago, LESAN Lesser Antillers

I used the year of publication of the description of each currently valid species to examine patterns in the rate of species descriptions over time, and to construct species accumulation curves for the entire described fauna. I followed the criteria from Zapata and Robertson (2007), to predict the total fauna size using the logistic model in the PAST computer program.

Composition similarities for each country were estimated by a presence/absence matrix per class and for the complete phylum. With those matrixes, I applied a Euclidean distance similarity matrix and I compared the diversity of echinoderms with a cluster tree and non-metric multidimensional scaling (nMDS). I estimated the average taxonomic distinctness (Δ+) and its variation (Λ+) (Clarke and Warwick 2001). This index evaluated the taxonomic distance between each pair of individuals, defined by a Linnaean classification tree, and could be used with a presence/absence matrix without taking into consideration the sampling methodology used. This index is considered as one of the most precise indicators in a strict biodiversity sense (Clarke and Warwick 2001). It was used on five taxonomic levels: species, genus, family, order and class, with their respective weights ω = 20 (species in the same genera), 40 (same family but different genus), 60 (same order but different family), 80 (same class but different order) and 100 (different class). The statistical analysis was performed with the PRIMER 6.0 software.

Results

The list of echinoderms of the Caribbean includes 433 species, 237 genera, 80 families, 29 orders and five classes (Table 1), with four endemic species. The richest class was Ophiuroidea with 148 species, followed by the class Asteroidea with 116 species, then Echinoidea and Holothuroidea with 76 and 63 species respectively, and finally the class Crinoidea with 30 species (Table 2). Mexico and Colombia are the richest countries with 182 and 180 species respectively, followed by Panama with 155 species and Cuba with 145 species (Table 3). Eight countries possess between 100 and 182 species, six between 50 and 99 species, and only two countries possess less than 50 species, Costa Rica and Guatemala with 44 and 23 species respectively. There is an average of 105 species per country (Table 3). The average number of species per kilometer (spp./km) of coastline is 0.13 ± 0.07 spp./km, Belize being the richest country with 0.26 spp./km, and Cuba, Haiti, and Venezuela the poorest with 0.04 spp./km. The average number of spp./km2 of Economic Exclusive Zone (EEZ) is 0.0022 spp./km2 of EEZ. Based on this metric, Guatemala is the richest country with 0.0140 spp./km2 of EEZ, followed by Honduras (0.0052 spp./km2), and Venezuela and Jamaica are the poorest with 0.0003 spp./km2 of EEZ (Table 3).

Table 1 Taxonomic classification of the echinoderm fauna from Caribbean countries. PRC Puerto Rico, RDO Dominican Republic, HAI Haiti, JAM Jamaica, CUB Cuba, MEX Mexico, BEL Belize, GUA Guatemala, HON Honduras, NIC Nicaragua, CRC Costa Rica, PAN Panama, PAN Colombia, VEN Venezuela, TYT Trinidad & Tobago, LESAN Lesser Antillers, NCA no country assigned; X indicates presence
Table 2 Species, genera, families and orders of Caribbean echinoderms
Table 3 Number of echinoderm species per class in each country. Coastline information taken from the The world fact book (https://www.cia.gov/library/publications/the-world-factbook/geos) and Economic Exclusive Zone (EEZ) information was taken from www.seaaroundus.org/eez/eez.aspx

Among the Class Crinoidea, the Dominican Republic (RDO) is the richest country with 17 species, followed by Panama and Jamaica with 15 each (Table 3), while Trinidad & Tobago and Guatemala are the poorest with three and two respectively. Davidaster discoidea and D. rubiginosa were reported from 12 countries, while eight species were reported only from one country. The genera Davidaster and Democrinus were the most diverse with three species each.

Colombia was the richest country for the class Asteroidea with 51 species followed by Mexico with 44 species. For this class, Astropecten is the most diverse genus with 12 species. Astropecten articulatus and Oreaster reticulatus are reported from 13 countries, and 38 species are reported for only one country. Laetmaster spectabilis is endemic to Cuba. Four species were reported for international waters: Styracaster elongatus, Benthopecten simplex simplex, Cladaster rudis and Henricia sexradiata.

With respect to the Class Ophiuroidea, Mexico, Colombia, Belize and Panama exhibited the highest species richness with 63, 62, 58 and 56 species respectively, while Nicaragua and Guatemala were the least diverse with six and four species each (Table 3). Ophioderma was the most diverse genus with 11 species. Ophiocoma echinata was the only species reported in the entire region (16 countries or territories), while Astrophyton muricatum was reported from 15 countries and Ophioderma appressum from 14. For this class 71 species were reported from only one country, and the species Ophiothrix synoecina is endemic to Colombia, and O. stri and O. cimar are endemic to Costa Rica and Panama.

With respect to Echinoidea, Colombia was the richest country with 47 species, followed by the Dominican Republic with 41 (Table 3). Clypeaster was the most diverse genus with ten species; Meoma ventricosa ventricosa was reported in 15 countries and Echinometra lucunter and Eucidaris tribuloides in 14. In this class, 18 species were reported from only one country.

Mexico was the richest country for the Holothuroidea with 32 species, followed by Panama and Puerto Rico with 30 species each, while Guatemala, Costa Rica, and Nicaragua were the least diverse (Table 3). Holothuria was the most diverse genus with 16 species; Holothuria (Halodeima) mexicana was reported for 15 countries and Isostichopus badionotus for 12. Within this class, 23 species were reported for only one country.

Initially, the publication of echinoderm species descriptions in the Caribbean Sea was slow (Fig. 2a, b), with an average of 0.47 species described per year between 1740 and 1840. Between 1840 and 1920, there was a substantial increase (3.83 species described per year), followed by a slower rate between 1920 and the present, with 0.91 species described per year. Taking the entire period of 1740 to 2010, there were on average 1.61 species described per year. According to the logistic model (Fig. 2b), the curve will be reaching an asymptote in the next 50 years, with seven probable undescribed species to be named.

Fig. 2
figure 2

a Number of new species of echinoderms from the Caribbean described by decade. b Accumulation curves of species descriptions for the total (gray line) and with the fitted logistic model (black line)

Colombia and Mexico, the most diverse countries, are the most dissimilar in comparison relative to the rest of the region (Figs. 3, 4, gray areas). The difference is primarily due to the composition of Asteroidea (Figs. 3c, 4c), Ophiuroidea (Figs. 3d, 4d) and Echinoidea (Figs. 3e, 4e), and to the influences from other regions like the Gulf of Mexico, Florida and Brazil. In general terms, the Caribbean is very homogenous in species composition between countries (Figs. 3, 4).

Fig. 3
figure 3

Cluster tree (Euclidean distance) based on species presence/absence Bray-Curtis resemblance matrix: a Echinodermata, b Crinoidea, c Asteroidea, d Ophiuroidea, e Echinoidea, f Holothuroidea; between the Caribbean countries. Gray areas most similar countries

Fig. 4
figure 4

Non-metric multiple dimensional scaling (NMDS) based on species presence/absence Bray-Curtis resemblance matrix: a Echinodermata, b Crinoidea, c Asteroidea, d Ophiuroidea, e Echinoidea, f Holothuroidea; between the Caribbean countries. Gray areas most similar countries

The taxonomic distinctness index (∆+) indicated that most of the countries are inside the 95% confidence limit of composition; Panama, Cuba, Mexico and Colombia (Fig. 5) being closer to the average of distinctness. Guatemala possesses few species (23 spp.) but exhibits a high value of distinctness (∆+), because those species represent many different groups with few representatives in each one, making the taxonomic distance greater. In Guatemala, each class is represented more or less equally by two to eight species, with very low variation (Fig. 5b). On the other hand, Trinidad & Tobago, which also has few species (55 spp.), has a lower distinctness value (∆+), because the species are unequally represented. The 55 species are dominated by two groups, Ophiuroidea (29 spp.) and Holothuroidea (15 spp.), while the other classes possess fewer species, so the average taxonomic distance is lower (Fig. 5a), with a greater variation (Fig. 5b).

Fig. 5
figure 5

Taxonomic distinctness index: a average (delta: ∆+), and b their variation (lambda: Λ+) of the Caribbean echinoderms. Continuous line 95% confidence limit, discontinuous line+ average value

Discussion

The Caribbean Sea is a marine province rich in echinoderm species. It has 433 species, representing 6.5% of the total diversity of the phylum, according to numbers presented by Pawson (2007). This region possesses almost 10% of the world’s Ophiuroidea, and between 4 and 6% of the other classes. The Caribbean is second in the tropical Americas with respect to species numbers, after the Gulf of Mexico (522 species; Pawson et al. 2009). The Caribbean ranks above other regions like Brazil (329 species; Hadel et al. 1999), the Pacific of Central America (287; Alvarado et al. 2010), Baja California and the Gulf of California (231 species; Solís-Marín et al. 2005; Honey-Escandón et al. 2008), and the Galapagos Archipelago (198 species; Maluf 1991).

The Caribbean, with an apparent well-known echinoderm fauna (Fig. 2b), is highly homogeneous in composition, due mostly to the current patterns and the semi-closed nature of the region (Spalding 2004). This sea has been recognized as one of the most important coral reef biogeographic provinces (Spalding et al. 2001), with many cryptic habitats ideal for the development of the Ophiuroidea, which is the most diverse in the region. Moreover, additional species will probably be described when the deep areas of the Caribbean are studied, altering the predictive species description curve in Fig. 2b.

Mexico, Belize, Panama, Colombia and Cuba exhibit the highest species diversity, due in part to the rich coastal habitats, which are the most diverse in the region (Spalding et al. 2001), and to intensity of research in these areas. Relative to species description and publications, Colombia has taken the lead, with a higher sampling effort along all of its Economic Exclusive Zone, with collections from shallow and deep waters (Borrero-Pérez et al. 2002a, b, 2008; Benavidez-Serrato et al. 2005). An important feature of the region is the presence of the Mesoamerican reef, in Mexico, Belize, Guatemala and Honduras. This area could be considered a diversity hot spot.

In terms of ecoregions, the Southwestern Caribbean is the richest (Fig. 6), due to its central location in the region, the current patterns, and the influence of species from the north and the south. The Western Caribbean and the Greater Antilles ecoregions are the most similar due to their proximity but also due to the influence of species from the Gulf of Mexico, Florida and Bahamas. On the other hand, the Southern and Eastern Caribbean ecoregions are influenced by the faunas from Guyana and Brazil. This can also help explain why Mexico and Colombia are located on opposite sides of the nMDS (Fig. 4), having faunal influences from two different regions. All the countries from one ecoregion are very similar in composition (Figs. 3, 4).

Fig. 6
figure 6

Cluster tree (Euclidean distance) based on species presence/absence Bray-Curtis resemblance matrix of echinoderms by ecoregion. W Western Caribbean, SW Southwestern Caribbean, GA Greater Antilles, E Eastern Caribbean, S Southern Caribbean

The Central American countries like Guatemala, Honduras, Nicaragua and Costa Rica, and the Lesser Antilles are the least studied. It is important to notice that in the case of the Central American countries, the social movements of the 1960s and 1970s shifted the attention to issues other other than science. This combined with the lack of economic resources, research institutions, and reduced science investments have resulted in this lack of knowledge. However, according to Fig. 1b, countries with low species numbers are probably undersampled, especially those in close proximity to highly diverse countries. Trinidad & Tobago, the Lesser Antilles, Haiti, Jamaica, Guatemala, Honduras, Nicaragua and Costa Rica are likely undersampled, when compared with the number of species reported from neighboring countries (Fig. 1). However, it is necessary to look at these analyses with care, because in some cases it could reflect the reality of the species richness due to the small size of the coastal zone, the degraded state of some coasts from natural and anthropogenic disturbances, and the lack of complex coastal morphology and habitat diversity.

Along the Caribbean Sea, seven species of echinoderms (four holothuroids and three echinoids) are extracted for commercial use. Among them are the sea cucumbers Astichopus multifidus, Holothuria mexicana, Actinopyga agassizi, and Isostichopus badionotus, the last being the most intensely harvested (Toral-Granda 2008). Extractions occur primarily in Panama, Nicaragua, Colombia, Venezuela, Mexico and Cuba. The exploitation of sea cucumbers without the use of a calculated fisheries management approach is probably the biggest threat to their populations within the region. For many of the species under legal or illegal fishing pressures there is little or no scientific information available on the biology, ecology, population abundance and dynamics (Toral-Granda 2008). Moreover, the situation is exacerbated because the majority of sea cucumber exploitations along the Caribbean (Buitrago and Boada 1996; Rodríguez-Millet and Pauls 1998; de la Fuente-Betancourt et al. 2001; Guzmán and Guevara 2002b) started with the consent of the local authorities, but without any knowledge about the ecology of the species (Guzmán et al. 2003). In the case of Panama, this activity is now banned, due to overfishing in 1997, during which 750,000 sea cucumbers were extracted in 30 days (Guzmán and Guevara 2002b).

Along the Caribbean there are small sea urchin fisheries focused on Echinometra spp., Lytechinus variegatus and Tripnesutes ventricosus. Granada and Martinique sea urchin harvests are the largest (Williams 2002). In the Margarita and Coche islands, Venezuela, L. variegatus and E. lucunter are extracted and processed on a small scale for human consumption (Gómez 1999). However, there is the fear that due to their naturally low population numbers these resources could be reduced by overfishing (Gómez and Gómez 2005).

In the case of the souvenir trade, Lunn et al. (2008) analysed the situation in Mexico, finding that annually 87,600 Oreaster reticulatus are extracted, with no regulation, and sold at prices between 1.8 and 60 US dollars. Similarly, Sloan (1984) indicated that this seastar might be under threat throughout the Caribbean, where some populations have been devastated. Mexico, Jamaica, Trinidad and Venezuela, among others, allow Oreaster extraction without apparent restrictions, which could increase demand in other countries (Guzmán and Guevara 2002a). Lunn et al. (2008) also mentioned the extraction of other echinoderms like Astropecten, Mellita and Tripnesutes as souvenirs in Mexico. However, there are no complete analyses of the exploitation of echinoderms in other places, like Colombia, Venezuela or Panama, where Oreaster as well as other echinoderms are extracted.

The lack of control in echinoderm extraction is a major threat in the Caribbean region. However, the greatest threats to this group of animals come from anthropogenic disturbances like sedimentation and coastal pollution. Sedimentation reduces recruitment success for some key species, such as sea urchins (i.e., Diadema antillarum; Vázquez-Domínguez 2003). Moreover, the loss of architectural complexity of the majority of coral reefs on the area (Alvarez-Filip et al. 2009), reduces the availability of substrate for recruitment and development. Agricultural pollution can produce endocrine disruptions in many species, slowing the recovery of critical populations (Rawlins et al. 1998). Coastal development has become a serious threat for endemic and cryptic species of ophiuroids in Colombia, Panama and Costa Rica, where the rock cavities made by sea urchins are being seriously degraded (Hendler 2005; Monroy-López and Solano 2005).

The research priorities for this group of animals in the Caribbean should be focused on the discovery of new species from deep waters, increased research in Central America and the Lesser Antilles, and increased ecological research in groups other than the echinoids. Future studies should also focus on (1) the role of marine protected areas for the recovery of key species, (2) population changes in fishing grounds, and (3) the impact of diseases in the region. Moreover, due to its rich biodiversity, relative to other tropical American waters, research and conservation efforts must be directed toward the preservation and conservation of that diversity, avoiding illegal extraction, enforcing controls, and improving coastal management.