Echinoderms from the Gulf of Venezuela, north-western coast of Venezuela

Echinoderms are a major group of marine invertebrates that often play integral roles within the marine ecosystem. Studies about their occurrence, abundance, and distribution in Venezuela are focused in the central-eastern coasts; hence the aim of this study is to describe the echinoderm community in the north-western coast of the Gulf of Venezuela. Samples were collected from three sites in the Venezuelan Guajira Peninsula (Castilletes, Porshoure, and Kazuzain) where patchy coral reefs and seagrass meadows are abundant. According to the substrate, two methods were performed using quantitative (1 m2 quadrates), and qualitative free-diving observations. All organisms were counted and identified to the lowest possible taxonomic level; finally, diversity (Shannon diversity index), richness (number of species), and dominance in the different sampled substrates were recorded. The updated list of echinoderms of the Gulf of Venezuela reported in this research, includes 20 genera, 15 families, 10 orders, four classes, and 28 species. The richest class was Ophiuroidea, with 18 species, followed by Asteroidea, Echinoidea and Holothuroidea, with three species each. Castilletes was the sampling site with the higher number of species (18 species), followed by Porshoure (15 species), and lastly Kazuzain (12 species). Our observations indicate that the number of species and abundance were higher when found in coral reefs (21 species, 80.69% of the total collected individuals) in contrast to the species found in seagrass beds (16 species, 19.31% of the total of individuals collected). This updated list of echinoderms represents 11.54% of the total diversity of the phylum in the marine areas from the coast of Venezuela; it is suggested that this percentage is greatly influenced by the differences of habitats and substrates alongside the north-western coast in the Gulf of Venezuela.


INTRODUCTION
The phylum Echinodermata is, except for a few brackish water forms, a group of marine animals with radial symmetry that includes sea lilies (Crinoidea), brittle stars, basket stars (Ophiroidea), starfish (Asteroidea), sea urchins, sand dollars (Echinoidea), and sea cucumbers (Holoturoidea) (Hendler et al., 1995;Pawson, 2007;Azofeifa-Solano et al., 2017;Kuk-Dzul et al., 2019). This phylum consists of approximately 7,000 living species and 13,000 extinct species (Pawson, 2007). It is well known that the Caribbean Sea is considered a unique bio-geographic region, and it is among the top five hotspots in the world for marine biodiversity (Rivera-Monroy et al., 2004). In the Wider Caribbean, the echinoderm diversity is composed of 433 species, 237 genera, 80 families, and 29 orders, catalogued in five classes, with four endemic species (Alvarado, 2011;Alvarado & Solís-Marín, 2013), which represents 6.5% of the total diversity of the phylum worldwide (Alvarado, 2011).
Thirteen ecoregions were described for the Venezuelan coast, characterized by their ecological, physical, and oceanographic features (Miloslavich et al., 2003). Previous research has found that the Gulf of Venezuela has the smallest number of echinoderms species recorded for the country (1.67%), with only eight species identified, distributed in six genera, six families, and five orders (Lodeiros et al., 2013). Studies on taxonomy, ecology of echinoderm populations and communities have been focused primarily in the central-eastern coasts of the country, mostly referring to abundance and distribution of Echinoidea, Holothuroidea, and Ophiuroidea (Lodeiros et al., 2013); hence the small representation of the phylum in the Gulf of Venezuela. The aim of this study is to describe the echinoderm community from the north-western coast of the Gulf of Venezuela and present an updated list of the echinoderms for this region.

Study area
The study sites are located in the Gulf of Venezuela, northern South America (00°45′-15°40′N, 59°47′-73°22′W), and comprise the northwest coast Venezuelan Guajira Peninsula. This border area has an extension of approximately 88 km, from the town of Neima to Castilletes. Within this coastline, three sampling sites with coral reefs and seagrass meadows were chosen: Castilletes, Porshoure, and Kazuzain (from north to south) ( Fig. 1) (Morán et al., 2014).
These localities present an arid-semiarid climate, which is marked seasonally in its precipitation and the action of the northeast trade winds (Masciangioli & Febres, 2000;Medina & Barboza, 2003). The total annual rainfall is 1,000 mm and it is distributed in different amounts throughout the annual cycle, with two marked periods (dry and wet). The dry period is from December to April, with its peak between February and March; these months are characterized by the total absence of rain. The rain period is from July to November, with maximum precipitation records in October, with approximately 200 mm. From April to June, it is known to be a transition stage between these two periods (Masciangioli & Febres, 2000;Álvarez-León et al., 2003).

Data collection and analysis
Data was collected between April and September 2010, following two methodologies depending on the substrate where the specimens were collected: seagrass beds and coral reef patches. For the patches of seagrass beds, we established a 100 m transect perpendicular to the coast, and at every 20 m we placed a 1 m² quadrate to count and collect all visible echinoderms, together with a random sediment sample using an Ekman dredge (capture area 0.022 m²) to identify small, buried echinoderms (Gómez Gaspar, 2000;Pernía, 2011).
In places with coral reefs, we evaluated three randomly chosen patches. Each patch was measured and checked to identify and collect by hand any visible echinoderms. In addition, a coral sample (500-7,000 cm³) and a sediment sample (with an Ekman dredge 0.022 m²) were taken to collect small echinoderms inside the rocky/coral substrate and buried in the surrounding areas (CARICOMP, 2001;Pernía, 2011).
Samples were placed in hermetically sealed and properly labelled plastic bags. Echinoids, asteroids, and ophiuroids were relaxed with progressive decreases in salinity, while holothuroids were narcotized by adding effervescent antacid tablets, then both ends were tied to prevent evisceration (Smaldon & Lee, 1979). Subsequently, all organisms were preserved in 70% ethyl alcohol, changing it every 48 hours until the liquid remained clear (Smaldon & Lee, 1979;Pernía, 2011).
In the laboratory, all specimens were identified to the lowest possible taxonomic level by direct observation, using a stereoscopic magnifying glass and the identification keys by Zoppi de Roa (1967) and Hendler et al. (1995). All species names were confirmed and updated according to the WoRMS (2020). Indices of diversity and richness were calculated (Pernía, 2011;Morán et al., 2014). All data were inserted and analized in an Excel® 2010 spreadsheet. Diversity indices were compared across the sampling sites with a Kruskal-Wallis analysis (STATISTICA, 2004;Pernía, 2011;Morán et al., 2014).

RESULTS
A total of 259 specimens were collected at the three sampling sites. The list of echinoderms of the Gulf of Venezuela reported in this research, includes 28 species (Table 2), 20 genera, 15 families, 10 orders and four classes ( Table 1). The richest class was Ophiuroidea with 18 species, then Asteroidea, Echinoidea and Holothuroidea with three species each. All 18 ophiuroid species are reported as new species for the Maracaibo Lake System. Castilletes was the sampling site with the highest number of species (18 species), followed by Porshoure (15 species), and lastly Kazuzain (12 species) (Fig. 2).
The Shannon-Weiner diversity index (H') presented a slight difference regarding the order of the most diverse sampling site; Porshoure showed the highest diversity (H' = 3.44), followed by Castilletes (H' = 3.03), and Kazuzain (H' = 3.01). It is important to mention that this index is biased towards the relative abundance of the species, and even though Castilletes showed the highest number of species, this locality did not show large numbers of individuals per species, which results in no sig-nificant differences among the sampling sites (H = 26.00; p = 0.4631).

DISCUSSION
The Gulf of Venezuela is known as an important area for recruitment and development of marine organisms (Alió, 2000). It is considered as a refuge (alongside the Caribbean coast of Colombia) due to the occurrence of cold and nutrient-rich upwelling waters (Miloslavich et al., 2010;Rueda-Roa & Muller-Karger, 2013). Filled with an enormous biotic richness (Rodríguez & Morales, 2000) it has a total of 28 species of echinoderms, representing 11.54% of the total diversity of the phylum in marine areas from the coast of Venezuela (Lodeiros et al., 2013). The composition of echinoderm species in the Gulf of Venezuela is similar to that of the Caribbean, presenting an apparent homogeneous distribution mostly attributed to the local current patterns and semi-enclosed nature (Alvarado, 2011;Alvarado & Solís-Marín, 2013). This area has been recognized as an important region for other species of marine benthic faunal groups, with many habitats ideal for the development of echinoderms that are known to be key species in several marine ecosystems (Alvarado, 2011;Lodeiros et al., 2013).
Our records indicate that the number of species and abundance were higher in coral reef habitats (21 species, 80.69% of the total of individuals collected) in contrast to seagrass beds (17 species, 19.31% of the total of individuals collected) (Table 3) (Fig. 2). García et al. (2008) explain that coral reefs provide not only nutrients, but also larger spectrum habitats for refuge and growth of several species. The Gulf of Venezuela could also be recognized as an important region for coral reef settlements (Barrios-Garrido et al., 2016), with a few cryptic habitats ideal for the development of the Ophiuroidea, which is the most diverse echinoderm group in the area (18 species, N = 28); our findings are contrary to that of Lodeiros et al. (2013), which documented no records of this class for the Gulf of Venezuela and other regions alongside the Venezuela coast (e.g., Cariaco trench, Tocuyo, and some Oceanic areas). Despite the availability of nutrients found in the Gulf of Venezuela, the distribution of species is likely to be influenced by the substrate for recruitment and development. Similar findings were described by previous researchers (Bitter, 1999;Alvarado, 2011). Further research is needed to understand the role of this ecosys-tem in the distribution of echinoderms in the Southern Caribbean.
Our results show that 13 species (n = 21 species) of ophiuroids were found in coral reef patches. According to the sampling sites, Castilletes exhibits the highest species diversity of echinoderms (18 species, N = 28) (Fig. 2), due in part to the rich coastal habitats (large patches of coral reefs), which are known to be the most diverse ecosystems in the marine realm (Pandolfi et al., 2003;Nava & Severeyn, 2010;Alvarado, 2011;Barrios-Garrido et al., 2016). Previous authors have found ophiuroids as the most diverse group in other coastal areas in Venezuela (Gómez Maduro & Hernández Ávila, 2011, Noriega & Fuentes-Carrero, 2014, mostly recorded in coral reefs, rocky reefs, and mangroves (Noriega & Fuentes-Carrero, 2014). The high diversity of ophiuroids in Castilletes sampling sites may be related to the notorious influence of marine currents, nutrients, and larvae dispersal from the Caribbean as stated by Alvarado (2011) for echinoderm communities within the Caribbean basin.
Although the class Ophiuroidea had the highest number of species in the Gulf of Venezuela, the most dominant species was Echinometra lucunter (23.55%), a sea urchin that, in our study, was found only in Castilletes. This species is frequently associated with rocky reef environments, close to Castilletes in Punta Perret (Pulido-Petit et al., 2017). It is known that species of Echinometra maintain erosion levels in the areas they inhabit and are commonly found in limestone reefs (Hendler et al., 1995). Similarly, other authors have reported E. lucunter in environments closely related to rocky substrates, and it is indicated as common and an abundant species in several places throughout the Caribbean and other areas towards the northeastern coast of Brazil (Hendler et al., 1995;Bolaños et al., 2005;Alvarado et al., 2008, Gaitán Espitia, 2008Gondim et al., 2018;McClanahan & Muthiga, 2020).
The extraction and fishing of sea urchins and sea cucumbers in Venezuela is mainly documented in the eastern coast, although not always commercially exploited under the administration of the corresponding authorities (Lodeiros et al., 2013); and it is suggested that the consumption, extraction and/or fishing of echi- noderm species in the Gulf of Venezuela is non-existant. Nevertheless, an illegal trade of several marine benthic invertebrates has been reported, mainly for ornamental and decorative uses (Lodeiros et al., 2013;Rojas-Cañizales et al., 2020). It is important in the future to understand the ecological role (food webs, erosion functionality, and compartmentalisation of the habitat) of sea urchins and sea cucumber species in the study area, and its potential use as a food item by local human communities if needed (Alió, 2000;Lodeiros et al., 2013). Several studies about benthic communities in the Venezuelan Guajira have been performed mostly focusing on mollusks, due to their economic value in the region, often collected as a protein source, bait, decorations, among others (Alió, 2000;Rodríguez & Morales, 2000). Echinoderms are ranked as the last group of invertebrates studied in the Maracaibo System, mainly due to its estuarine nature (Rodríguez & Morales, 2000), where most echinoderms are not well adapted to develop and survive (Alvarado, 2011;Lodeiros et al., 2013). Marine environments are only found in the Gulf of Venezuela, a region essentially isolated and difficult to access (Rodríguez, 2000). Despite these facts, this study has provided some information on the different classes, families and species of echinoderms in the north-western coast of the Gulf of Venezuela. The spatial-temporal distribution of these echinoderms, as well as their density, growth rates, reproduction, and other population and community parameters require detailed additional studies. The inclusion of other areas (e.g., Cocinetas marine lagoon and its mangrove submerged roots), also will generate information in order to develop strategies for their conservation and management (Alvarado, 2011;Lodeiros et al., 2013;Morán et al., 2014).

ACKNOWLEDGMENTS
Authors would like to acknowledge the inhabitants of the different sampling sites alongside the north-western coast of the Gulf of Venezuela, who were an essential part of the effortless completion of this research. Thanks to the volunteers, assistants, students, and professors who collaborated during the sampling period. We thank the Laboratory of General Ecology and the Aquatic Invertebrate Systematic Laboratories from the Biology Department of the Experimental Faculty of Science at the University of Zulia, as well as every helping hand from the Research Division at the Postgraduate Department, and the Dean office of this distinguished faculty. We also appreciate the effort and help provided by Professor Nicida Noriega from the "Universidad de Oriente-Venezuela" who guided the identification of some of the species documented.