Current knowledge of echinoderms (Echinodermata) from the coast of Paraíba, northeastern Brazil

Estado actual del conocimiento de los equinodermos (Echinodermata) de la costa de Paraíba, noreste de Brasil

Resumen

Brasil dieron como resultado 74 especies. Nuestro estudio cualitativo incluyó registros actualizados con información sobre el hábitat y la presencia de las especies en unidades de conservación (UC). Aunque todos los registros están restringidos desde el intermareal hasta 35 m de profundidad, la diversidad de especies es alta en comparación con otras áreas, ya que corresponde a 21% de todas las especies brasileñas y a 16% de las especies conocidas del mar Caribe. Los principales hábitats utilizados por los equinodermos fueron los arrecifes y los mantos de rodolitos. Alrededor de 15% de las especies están en la Lista Roja brasileña. Un resultado positivo es que 67% de estas especies se encuentra dentro de las UC del estado. Con base en estos resultados, concluimos que la fauna de equinodermos de aguas someras está bien documentada en Paraíba. Finalmente, comentamos sobre el estado de conservación de las especies e indicamos direcciones futuras para el estudio del phylum Echinodermata.

Palabras clave: Bentos; Inventario; Arrecifes someros; Biodiversidad; Conservación; Atlántico sur

The littoral region of northeast Brazil (NE Brazil) extends for approximately 3,400 km, which corresponds to 42.5% of the Brazilian coastline (Gondim, Christoffersen et al., 2014). The area is unique, harbouring the largest and the richest reef strip of the Southwestern Atlantic (about 3,000 km) (Amaral & Jablonski, 2005; Leão et al., 2010). The region encompasses 9 coastal states: Maranhão (MA), Piauí (PI), Ceará (CE), Rio Grande do Norte (RN), Paraíba (PB), Pernambuco (PE), Alagoas (AL), Sergipe (SE), and Bahia (BA).

The littoral of the state of Paraíba is heterogeneous, with beaches, dunes, cliffs, restingas, bays, mangroves, and several reefs, that occur linearly along most of the coastline (Branner, 1904; Carvalho, 1982; Mendes & Pinheiro, 2019). The most common reef formations are of sandstone or biological origin (Carvalho, 1982), occurring as beachrocks, fringe reefs, barrier reefs, or permanently submerged reefs. For several years, the marine benthic fauna of this sector of the northeastern coastline remained unexplored. But knowledge has been growing exponentially throughout the last 2 decades (Brito et al., 2013; de Assis et al., 2007; de Assis, Alonso et al., 2012; Dias, 2009; Dias & Gondim, 2016; Dias et al., 2013; Duarte et al., 2014; Gama et al., 2006; Gondim et al., 2011; Lima et al., 2017; Lucena et al., 2017; Mota et al., 2020; Oliveira et al., 2014; Santos & Pinheiro, 2013, 2014; Santos et al., 2008, 2011, 2018). The southern coastline of the state (Pitimbu) was the first site impacted by the recent oil spill that affected the entire northeastern and part of the northern and southeastern coastline of Brazil in September 2019 (Soares, Teixeira, Bezerra, Paiva et al., 2020). This oil spill was considered the most extensive and severe environmental disaster ever recorded in Brazilian history, both for the South Atlantic Ocean basin and for tropical coastal regions worldwide (Soares, Teixeira, Bezerra, Rossi et al., 2020).

Knowledge of the echinoderm fauna in the state of Paraíba can be divided into 2 periods. The first period was characterized by naturalists and researchers, working at the benthic community level, only indirectly included echinoderms in their samples or studies. Much of this material has been deposited in scientific collections. The second period began in 2006, with the establishment of a research group on echinoderm taxonomy in the Invertebrate Laboratory Paulo Young (LIPY), at Universidade Federal da Paraíba (UFPB). This group, initially consisting of Anne Isabelley Gondim and Patrícia Lacouth, under the supervision of Carmen Alonso Samiguel, began their studies on echinoderm biodiversity along the Paraíba coastline based in the Invertebrate Collection Paulo Young (CIPY – UFPB).

Historically, the first records of echinoderms for the littoral of Paraíba were made by Rathbun (1879), based on material collected by J.C. Branner and other members of the Geological Commission of Brazil between 1875 and 1877. In that paper, Rathbun (1879) cited 6 species of echinoderms for Paraíba: 1 Crinoidea [Antedon sp., probably Comactinia echinoptera (Müller, 1840)], 1 Asteroidea [Echinaster (Othilia) echinophorus (Lamarck, 1816)], and 4 Ophiuroidea [Ophioderma cinereum Müller & Troschel, 1842 —as Ophiura cinérea; O. appressum (Say, 1825) —as Ophiura appressa, Ophiocoma echinata (Lamarck, 1816), and Ophiothrix (Ophiothrix) angulata (Say, 1825) —as Ophiothrix violacea]. Subsequently, echinoderms (mainly ophiurans) were cited only sporadically for the coast of Paraíba by Verrill (1899) (1 sp.), H.L. Clark (1915) (1 sp.), A.M. Clark (1953) (1 sp.), Laborel-Deguen (1963) (4 spp.), Tommasi (1965, 1970) (1 sp. and 5 spp., respectively), Thomas (1973) (1 sp.), Albuquerque (1986) (6 spp.), Young (1986) (7 spp.), and Albuquerque & Guille (1991) (3 spp.). A turning point in the systematic study of the group is provided by Gondim et al. (2008). The authors recorded 31 species of echinoderms for Cabo Branco beach (João Pessoa). Several inventories, new records, and new species have been published since then (Gondim et al., 2010, 2011, 2018; Gondim, Christoffersen et al., 2014; Prata & Christoffersen, 2017; Prata et al., 2014, 2017; Prata, Manso et al., 2020; Prata, Stevenson et al., 2020). Nevertheless, only 3 papers provide information on the ecology of the group along this coast (de Assis, Bezerra et al., 2012; Gondim, Dias et al., 2014; Lafite et al., 2021).

Among several types of research that provide data for the conservation and management of marine ecosystems, the inventory of biodiversity is a basic requirement (Sloan & Bartier, 2009). The first stage to conserve biodiversity is to identify, describe, map, and measure this diversity (Margules & Pressey, 2000). Under this view, regional evaluations contribute to the knowledge of biodiversity, uncover biogeographic patterns, and characterize ecosystems. Only then is it possible to establish public programs of conservation, especially in a megadiverse country of continental dimensions such as Brazil. Furthermore, qualitative inventories can be more expedient, more cost-effective, and of similar scientific validity to quantitative data for most conservation needs (Mikkelsen & Cracraft, 2001).

Herein, we present a diagnosis of the present status of knowledge of the Echinodermata for the coast of Paraíba. We provide an updated checklist of the echinoderm fauna, with notes on habitat and distribution along this coast. Likewise, we provide and discuss data of composition and similarity of the taxa in the Paraíba reefs, compare this diversity with other northeastern states and seek to answer the question: is the echinoderm fauna of Paraíba still poorly known? We conclude with comments on the state of conservation of species and recommendations for further research.

Materials and methods

Collection data on Echinodermata are based on literature surveys (published papers from 1879 to 2021) and examination of specimens deposited from the Invertebrate Collection Paulo Young (CIPY-UFPB), Marine Biology Laboratory of Estadual University of Paraíba (UEPB) (LBMar-UEPB), Federal University of Sergipe (LABIMAR-UFS), Museum of Zoology of the Federal University of Bahia (MZUFBA), Museum of Zoology of the University of São Paulo (MZUSP), National Museum of the Federal University of Rio de Janeiro (MNRJ). An extensive review of the literature and the database Brazilian Fauna Taxonomic Catalog-CTFB (Moura 2020), was also used to inventory the number of echinoderms from each northeastern state.

The taxonomic list is organized systematically, according to that contained in the specialized literature and the database World Register of Marine Species: WoRMS (2020), Asteroidea Database (Mah, 2020), Ophiuroidea Database (Stöhr et al., 2020), and Echinoidea Database (Kroh & Mooi, 2020). Santana et al. (2017) concluded that Ophiothrix (Ophiotrix) angulata does not occur in Brazil and proposed that Brazilian specimens corresponded to several new species. Only recently have these new species been described (Santana et al., 2020). Here, we adopted the name “Ophiothrix (Ophiothrix) angulata” or “O. (O.) angulata”, in reference to the study material that needs to be revised. In the similarity analysis, we used simply “O. (O.) angulata”, while records provided by Santana et al. (2020) were only considered when estimating the total number of species.

The coastline in Paraíba (6º29’S to 7º33’S) is 138 km long, extending from Barra de Camaratuba, in the north, to Acaú, in the south (Fig. 1). Several types of environments are found along this coast, such as mangroves, sandy beaches, and reefs. The subaquatic landscape includes the presence of seagrass, macroalgal banks, rhodolith beds, and patch reefs. To the south of João Pessoa, narrow beaches and small bays are found. The larger beaches occur along the northern sector of the state (Carvalho, 1982). The climate is tropical, warm, and humid, characterized by a dry period (between September and February) and a rainy season (from March to August). Along the coast, tides oscillate from 0.1 to 2.7 m (Souza & Furrier, 2015).

The continental shelf is narrow, shallow, and relatively flat, with a mean width of 30 km, becoming broader in a north-south direction; carbonatic sediments predominate (Barbosa, 1989; Feitosa et al., 2005). The beginning of the continental slope usually occurs between 50 and 60 m (Rocha et al., 1998). Canyons are observed at the outlets of the rivers Goiana, Paraíba, and Mamanguape, being presently disconnected from the continental shelf, but are visible beyond 15 m (Barbosa, 1989). The geomorphological characteristics of the continental shelf, slope, and abyssal plain are presented by Chaves (1979).

Reefs are quite common along the coast (Carvalho, 1982) (Figs. 1, 2). The greatest reef concentration may be observed between Baía da Traição and João Pessoa (Muniz et al., 2000). The width of the reef strip varies from a few meters to 150 m, with lengths of a few dozen meters to several kilometers. They reach depths greater than 60 m (Carvalho, 1982), but the large majority occur at depths of up to 40 m (Rocha et al., 1998). The northern coast, down to the Municipality of Cabedelo, is dominated by sandstone reefs (“arrecifes”), but beyond this region, the sandstone reefs become more patchy and co-occur with coral reefs (Laborel, 1970) (Fig. 2). Local reefs probably follow the structure common in northeastern Brazil, in which the base is arenitic, and the biogenic portion is formed by calcareous algae and vermetids (Melo, 2006). Around João Pessoa, the hermatypic corals are only scattered over the reef, whereas algae (e.g., Caulerpa, Halimeda) are predominant; therefore, the name “algal reef” would be more appropriate for these reefs (Guilcher, 1983, 1988). Many of these reef formations were intensely explored over many years to remove calcareous blocks for the construction of churches, monasteries, houses, and the production of lime (Branner, 1904). Branner (1904), Laborel (1970), and Carvalho (1982) provide a detailed characterization of the littoral of the state. Geological information may be obtained in Branner (1902).

Presently there are 6 Conservation Units (UCs) in the state of Paraíba: Parque Estadual Marinho de Areia Vermelha (PEMAV), Área de Proteção Ambiental Naufrágio Queimado (APANQ), Área de Proteção Ambiental da Praia de Jacarapé (APAPJ), Área de Proteção Ambiental de Tambaba (APAT), Área de Proteção Ambiental Barra do Rio Mamanguape (APABRM), and Reserva Extrativista Acaú-Goiana (Resex Acaú-Goiana). Only the first 2 are exclusively marine. These UCs cover 11% of the littoral area.

In order to describe ecological aspects of the inventoried species, point data extracted from their collection labels were analyzed. Graphs indicate habitats (hard and soft substrate, phytal, rhodolith beds, biological substrate, and artificial reefs), and depth ranges (0 to 10 meters; 11 to 29 m; 30 to 50 m) for each echinoderm class along the coast.

The similarity in species composition was analyzed at the local scale (coast of Paraíba) and a regional scale (northeast coast of Brazil). For the coast of Paraíba, the structure of the analyzed reefs was taken into account (type of reef/proximity to coast was used for 4 levels; Table 1). For the northeast coast, it was possible to compare the composition of the echinoderm fauna of the state of Paraíba with that of other states in the region. A presence/absence matrix was built with the species from the analyzed collections and the literature review. This matrix was subject to Euclidean Distance. The analyses were carried out considering a phylum and class approach; they were compared with cluster graphs and nMDS (non-metric multidimensional scaling). Statistical analyses were run in software Primer 6.0.

Results

We catalogued 74 species of echinoderms from Paraíba: Crinoidea (1 order, 2 families, 3 genera, and 3 species), Asteroidea (3 orders, 7 families, 7 genera, and 12 species), Ophiuroidea (2 orders, 9 families, 17 genera, and 30 species), Echinoidea (4 orders, 5 families, 8 genera, and 8 species), and Holothuroidea (3 orders, 7 families, 14 genera, and 21 species) (Table 2; Fig. 3). Two new records were added for the state: the feather star Comactinia echinoptera (Müller, 1840), and the brittle star Ophiocnida loveni (Ljungman, 1867).

In terms of number of species, Ophiuroidea and Holothuroidea were the most diverse classes. Within the first, Amphilepidida (21 spp.) was the order with the highest number of species, followed by Ophiacanthida (7 spp.). For Holothuroidea, Dendrochirotida (15 spp.) was the most diverse order, while Holothuriida (3 spp.) and Apodida (3 spp.) were less represented. Among the Asteroidea, Paxillosida (6 spp.) and Valvatida (4 spp.) were most represented, and Spinulosida (2 spp.) was less represented. All orders of Echinoidea were less diverse: Camarodonta and Clypeasteroida with 2 species each, and Cidaroida and Spatangoida with only 1 species each. As expected, Crinoidea was the least diverse class, represented by 3 species and 1 order (Comatulida) (Table 2).

Circa 82% (59 spp.) of the inventoried species occurred in isobaths below 10 m (Fig. 4a). This zone was the most diverse in number of species for all Echinodermata classes. The bathymetric range 11-29 m contained 39 species, compared to 20 species between 30 and 50 m. Regarding classes, Asteroidea and Ophiuroidea presented about the same number of species between 0-10 m and 11-29 m (Fig. 4b). Echinoidea diminished gradually in number of species along each depth range. On the other hand, 95% of Holothuroidea species occurred from the intertidal to 10 m (Fig. 4b). Only 6 sea cucumbers occurred below 10 m, and only 1 between 30 to 50 m (Holothuria [Cystipus] pseudofossor Deichmann, 1930). Species of Crinoidea come from shallow reefs up to 6 m deep. Considering all species with bathymetric data, 14 occurred in all evaluated depths: Linckia guildingi Gray, 1840, Oreaster reticulatus (Linnaeus, 1758), Ophiomyxa flaccida (Say, 1825), Ophiocoma echinata, Ophioderma appressum, Ophioderma cinereum, Ophiostigma isocanthum (Say, 1825), Ophiopsila hartmeyeri Koehler, 1913, “Ophiothrix (Ophoithrix) angulata”, Ophionereis reticulata (Say, 1825), Ophionereis squamulosa Koehler, 1914, Eucidaris tribuloides (Lamarck, 1816), Lytechinus variegatus (Lamarck, 1816), and Tripneustes ventricosus (Lamarck, 1816).

Hard substrates (sandstone and biological reefs) were the main habitat of echinoderms, followed by rhodolith beds and phytal (Fig. 4c). Ophiuroidea and Holothuroidea were the most diverse taxa in number of species in the first 2 substrate types. Biological substrates (sponges and corals) were also frequently used by these 2 classes. Except for Crinoidea, all the remaining classes were recorded on artificial reefs. Ophiuroidea was most diverse in such substrates, with 3 spp. in shipwrecks, followed by Asteroidea, Echinoidea, and Holothuroidea, all with 1 species from the Cabedelo breakwater. Crinoidea was not recorded in soft substrates (sand and mud bottoms). All remaining classes occurred in these substrates, but with a low diversity of species (Fig. 4c).

The similarity in species composition was only considered in relation to the phylum, and specifically for Ophiuroidea and Holothuroidea (Fig. 5). The remaining classes were not considered in this regard due to the small number of species. In general, the composition of the echinoderm fauna is more similar among reefs with similar structures. Most similar groups occur between patch or barrier reefs (Fig. 5a). Similarity increases in reefs of similar type and location, such as Coqueirinho and Carapibus reefs.

Ophiuroidea showed the same patterns of similarity as a function of the type of reef (Fig. 5b). Yet, the location of the reefs was not determinant for the formation of the most similar groups. For example, the reefs of Carapibus and Seixas were the most similar in terms of species composition; they are similar in type (patch reefs), but come from distinct locations (Fig. 5b). Class Holothuroidea was poorly recorded in barrier reefs (sandstone reefs), and thus could not be included in our analysis. The greatest similarity was seen between the reef fauna of Pitimbu and Jacumã, again a case of similar reef patch formations from distinct locations (Fig. 5c). No species of echinoderms occurred in all studied coastal reefs. The brittlestars Aphipholis squamata (Delle Chiaje, 1828) and “O. (O.) angulata”, and the sea urchin Echinometra lucunter (Linnaeus, 1758) were the most common species shared by these areas, occurring in 68%, 63% and 63% of the reefs, respectively. On the other hand, Tripneustes ventricosus, Holothuria (Thymiosycia) arenicola Semper, 1868, Ophiothrix brasiliensis Santana, Manso, Almeida & Alves, 2020, and Thyone pawsoni Tommasi, 1972 were the least common species, occurring in only 1 reef environment.

Table 1

Classification used for shallow reefs in Paraíba, Northeastern Brazil.

Classification	Description
Beach patch reef	Fringing reef, mainly beachrocks, located on intertidal zone and subject to exposure during low tides; with several natural pools of diverse sizes, shapes, and depths (Fig. 2a, e, g, h).
Beach barrier reef	Sandstone reefs, that begin at intertidal zone, but recede up to 1.67 km from the coast; subject to exposure during low tides, and may form small, shallow natural pools (Fig. 2b, c).
Offshore patch reef	Reef with high rates of coral-algae, distant between 0.1 and 1.5 km from coast; mostly submerged (Fig. 2d, f).
Offshore barrier reef	Sandstone reefs, that occur between 0.25 and 1.5 km from the beach; they are influenced by rivers, as evidenced by the turbidity of the water in some seasons of the year and the presence of fine muddy sediments covering the rocks; exposed during low tides; shallow natural pools may be present (Fig. 2i).

Table 2

Taxonomic list of species of echinoderms from Paraíba, with data on occurrence, habitat, and voucher. Localities: AC (Acaú Beach), AT (Atolzinho reef), AVR (Areia Vermelha reef), BC (Barra de Camaratuba beach), BM (Barra de Mamanguape beach), BT (Baía da Traição beach), BB (Bessa Beach), CA (Carapibus Beach), CB (Cabo Branco beach), CBD (Cabedelo beaches), CQ (Coqueirinho beach), JC (Jacarapé beach), JM (Jacumã beach), LC (Lucena beaches), MNB (Manaíra beach), MRE (Mamanguape River Estuary), PC (Picãozinho reef), PCP (Ponta de Campina beach), PH (Penha beach), PNR (Paraíba do Norte River Estuary), PTB (Pitimbú beaches), PS (Pomar das esponjas reef), PTC (Port of Cabedelo), QCB (Breakwater of Cabedelo), QQ (Quebra-Quilha reef), RG (Galé reefs), RS (Seixas reefs), SG (São Gonçalo reef), TB (Tambaú beach), TBB (Tambaba beach), TG (Tabatinga beach). Substrate and habitat: adc (associated with different coral species); atr (artificial reefs – shipwrecks and breakwater); csh (continental shelf between 10 to 35 m); phy (phytal of some algae); rhb (rhodolith beds); sr (submerse reef), srf (shallow coastal reef); sd (sand substrate); sdw (sponge-dwelling); md (mud sediment). Conservation Units of Paraíba littoral: APABRM (APA Barra do Rio Mamanguape), APANQ (APA Naufrágio Queimado), APAT (APA Tambaba), and PEMAV (Parque Estadual Marinho de Areia Vermelha). *Occurrence extracted from Tommasi (1965). **Specimens that need reviewed. ***Occurrence extracted from Santana et al. (2020).

Taxon	Ocurrence	Ocurrence in Conservation Units	Habitat	Voucher
Crinoidea Miller, 1821
Comatulidae Fleming, 1828
Comactinia echinoptera (Müller, 1840)	PC, QQ, SG	APANQ	phy, scr	UFPB.ECH.49
Davidaster rubiginosus (Pourtalès, 1869)*	—	—	—	—
Tropiometridae A.H. Clark, 1908
Tropiometra carinata (Lamarck, 1816)	BM, BT, CB, PC, QQ, PS, RG	APABRM, APANQ	scr	UFPB.ECH.1014
Asteroidea de Blainville, 1830
Astropectinidae Gray, 1840
Astropecten alligator Perrier, 1881	PCP	APANQ	csh	UFPB.ECH.881
Astropecten marginatus Gray, 1840	CBD, TB	APABRM, APANQ	sd	UFPB.ECH.864
Luidiidae Sladen, 1889
Luidia alternata alternata (Say, 1825)	BM, PCP, BB	APANQ	csh	UFPB.ECH.876
Luidia clathrata (Say, 1825)	CBD	APANQ	csh	UFPB.ECH.875
Luidia ludwigi scotti Bell, 1917	BT	—	csh	UFPB.ECH.878
Luidia senegalensis (Lamarck, 1816)	CBD, LC, PNRE	—	sd	UFPB.ECH.1865
Echinasteridae Verrill, 1867
Echinaster (Othilia) brasiliensis Müller & Troschel, 1842	AVR, BB, CB, RS	APANQ, PEMAV	rhb, scr	UFPB.ECH.138
Echinaster (Othilia) echinophorus (Lamarck, 1816)	AVR, BB, CB, LC, PC, PCP, RS	APANQ, PEMAV	rhb, scr	UFPB.ECH.568
Asterinidae Gray, 1840
Asterinides folium (Lütken, 1860)	CBD	—	rhb	UFPB.ECH.572
Mithrodiidae Viguier, 1878
Mithrodia clavigera (Lamarck, 1816)	BB	—	csh	UFPB.ECH.880
Ophidiasteridae Verrill, 1870
Linckia guildingi Gray, 1840	BB, BC, CB, CBD, JC, PCP, PTB	APANQ	csh, scr	UFPB.ECH.1159

Table 2. Continued.
Taxon	Ocurrence	Ocurrence in Conservation Units	Habitat	Voucher
Oreasteridae Fisher, 1908
Oreaster reticulatus (Linnaeus, 1758)	AC, BT, CBD, JC, LC, PCP, PH, QCB, TB	APANQ	csh, rhb	UFPB.ECH.1251
Ophiuroidea Gray, 1840
Ophiomyxidae Ljungman, 1867
Ophiomyxa flaccida (Say, 1825)	AC, AVR, BC, CB, LC	APANQ, PEMAV	csh, phy, rhb, scr	UFPB.ECH.64
Ophiocomidae Ljungman, 1867
Ophiocoma echinata (Lamarck, 1816)	AVR, CBD, PCP	APANQ, PEMAV	csh, rhb, scr	UFPB.ECH.216
Ophiomastix wendtii (Müller & Troschel, 1842)	BC, BM, CBD, LC, PTB	APANQ	atr, csh	UFPB.ECH.397
Ophiocomella ophiactoides (H.L. Clark, 1900)	AT, BB, PC, PTB, RS, SG	APANQ	phy, rhb, scr	UFPB.ECH.34
Ophiodermatidae Ljungman, 1867
Ophioderma appressum (Say, 1825)	AVR, BC, BM, BT, CA, CB, CBD, CQ, JM, PTB, RG, RS, TBB	APABRM, APANQ, APAT, PEMAV	csh, scr, rhb	UFPB.ECH.296
Ophioderma cinereum Müller & Troschel, 1842	AVR, CA, CB, CBD, CQ, JM, RG, RS	PEMAV	csh, scr	UFPB.ECH.116
Ophioderma januarii Lütken, 1856	BC, BT, CB, CBD, PTC, TB	APANQ	csh, scr	UFPB.ECH.271
Amphiuridae Ljungman, 1867
Amphiura stimpsonii Lütken, 1859	BM, PC, PTB, QQ	APANQ	adc, csh, scr	UFPB.ECH.42
Amphipholis januarii Ljungman, 1866	AVR, BB, BM, BT, CA, CB, CBD, CQ, PS, PTB, PTC, QQ, RG, RS, TBB	APABRM, APANQ, APAT, PEMAV	adc, atr, csh, phy, scr, sr, rhb	UFPB.ECH.50
Amphipholis squamata (Delle Chiaje, 1828)	BB, BC, BM, BT, CA, CB, CBD, CQ, RG, RS, SG, PC, PS, PTB, QQ, TBB, TG	APABRM, APANQ, APAT	adc, csh, phy, rhb, scr, sr	UFPB.ECH.43
Ophiostigma isocanthum (Say, 1825)	BB, BC, BT, CBD, JC, JM, LC, MNB, PTB	—	csh, rhb	UFPB.ECH.173
Ophiocnida scabriuscula (Lütken, 1859)	AVR, BB, BT, CA, CB, CBD, CQ, JM, LC, PCP, RG, RS	APANQ, PEMAV	csh, rhb, scr	UFPB.ECH.174
Ophiocnida loveni (Ljungman, 1867)	—	—	sch	—
Microphiopholis atra (Stimpson, 1852)	CB, MRE	APANQ	csh, rhb, sd	UFPB.ECH.2183
Microphiopholis gracillima (Stimpson, 1854)	BB, RS	APANQ	phy, rhb	UFPB.ECH.2202
Amphiodia planispina (v. Martens, 1867)	BB, CB, CBD, LC, MNB, PCP, PH, PTB	APANQ	csh, rhb, scr	UFPB.ECH.227
Amphiodia riisei (Lütken, 1859)	CB	—	csh	UFPB.ECH.931
Ophiophragmus luetkeni (Ljungman, 1872)	BM	APABRM	scr	UFPB.ECH.2279
Ophiophragmus pulcher H.L. Clark, 1918	RS	—	csh, rhb	UFPB.ECH.2231
Ophiopsilidae Matsumoto, 1915
Ophiopsila hartmeyeri Koehler, 1913	BB, CB, CBD, JC, JM, LC, PH, PTB	—	csh	UFPB.ECH.323
Ophiactidae Matsumoto, 1915
Ophiactis lymani Ljungman, 1872	BB, BT, CB, PC, PS, PTB, QQ, RG, RS, TBB	APANQ, APAT	adc, phy, scr, sr	UFPB.ECH.58
Ophiactis quinqueradia Ljungman, 1872	BC, BT, CB, CBD, JC, LC, PTB	—	csh, scr, sdw	UFPB.ECH.288
Ophiactis savignyi (Müller & Troschel, 1842)	BB, BM, BT, CA, CB, CQ, PC, PS, PTB, QQ, RG, RS, SG	APABRM, APANQ	adc, atr, phy, rhb, scr, sdw, sr	UFPB.ECH.39
Ophiotrichidae Ljungman, 1867
Ophiothix (Ophiothrix) angulata (Say, 1825)**	AVR, BB, BC, BM, BT, CA, CB, CBD, CQ, JC, JM, LC, RS, RG, PCP, PS, PH, PTB, QQ, TB, TBB, TG	APABRM, APANQ, APAT, PEMAV	adc, atr, csh, rhb, scr, sr	UFPB.ECH.78
Ophiothrix brasiliensis Santana, Manso, Almeida & Alves, 2020***	—	—	—	—
Ophiothrix tommasii Santana, Manso, Almeida & Alves, 2020***	—	—	—	—
Ophionereididae Ljungman, 1867
Ophionereis dolabriformis John & A.M. Clark, 1954	BB, CBD, CQ, LC, PTB, TBB	—	csh	UFPB.ECH.749
Ophionereis reticulata (Say, 1825)	AVR, CA, BC, BM, BT, CB, CQ, JM, PS, RG, RS, TBB	APANQ, APAT, PEVAV	scr	UFPB.ECH.1139
Ophionereis squamulosa Koehler, 1914	BB, BC, CBD, CQ, JC, LC, PH, PTB, TB	—	rhd	UFPB.ECH.584
Ophiolepididae Ljungman, 1867
Ophiolepis impressa Lütken, 1859	BC, JM, LC, TB	—	csh	UFPB.ECH.490
Ophiolepis paucispina (Say, 1825)	BB, PTB	—	csh, phy, scr	UFPB.ECH.172
Echinoidea Leske, 1778
Cidaridae Gray, 1825
Eucidaris tribuloides (Lamarck, 1816)	BB, BC, BM, BT, CBD, CQ, JC, JM, LC, PH, PTB, TB	—	csh	UFPB.ECH.1620
Echinometridae Gray, 1855
Echinometra lucunter (Linnaeus, 1758)	AVR, BC, BM, BT, CA, CB, CBD, CQ, JM, PCB, PCP, PTB, RG, RS, TBB, TG	APABRM, APANQ, APAT, PEMAV	scr, phy, rhb	UFPB.ECH.01
Toxopneustidae Troschel, 1872
Lytechinus variegatus (Lamarck, 1816)	BB, BC, BM, BT, CB, CBD, JC, JM, LC, PH, PTB, RG, TB	APANQ	csh, phy, rhb, scr	UFPB.ECH.1158
Tripneustes ventricosus (Lamarck, 1816)	BB, BT, PTB	APANQ	csh, scr	UFPB.ECH.1361
Mellitidae Stephanini, 1912
Mellita aff. quinquesperforata (Leske, 1778)	BB, BM, BT, CA, CB, CBD, CQ, JM, LC, PCP	APABRM, APANQ	sd	UFPB.ECH.350
Leodia sexiesperforata (Leske, 1778)	BT, PCP, PTC	APANQ	sd	UFPB.ECH.1013
Encope emarginata (Leske, 1778)	AVR, BM, CB, CBD, LC, PCP, PTC	APABRM, APANQ, PEMAV	sd	UFPB.ECH.615
Brissidae Gray, 1855
Brissopsis sp.	CBD	—	csh	UFPB.ECH.1646
Holothuroidea (Blainville, 1834)
Chiridotidae Östergren, 1898
Chiridota rotifera (Pourtalès, 1851)	AVR, BB, BC, CA, CB, CBD, JM, PH, PS, PTB, RS, TBB	APANQ, APAT, PEMAV	csh, scr, phy, rhb	UFPB.ECH.187
Synaptidae Burmeister, 1837
Synaptula hydriformis (Lesueur, 1824)	BB, CB, PC, RS, SG	APANQ	phy, rhb, scr	UFPB.ECH.161
Protankyra ramiurna Heding, 1928	PTC	—	—	UFPB.ECH.2125
Holothuriidae Burmeister, 1837
Holothuria (Cystipus) pseudofossor Deichmann, 1930	CBD	—	csh	UFPB.ECH.2070
Holothuria (Halodeima) grisea Selenka, 1867	BC, BM, BT, CA, CB, CBD, CQ, JM, PCB, PH, SG, TG	APABRM, APANQ	scr	UFPB.ECH.316
Holothuria (Thymiosycia) arenicola Semper, 1868	CB	APANQ	scr	UFPB.ECH.1480
Cucumariidae Ludwig, 1894
Thyonidium seguroensis (Deichmann, 1930)	AVR, BB, BC, CB, CBD, PC, PTB, RS, TB	APANQ, PEMAV	rhb, scr	UFPB.ECH.1553
Parathyone suspecta (Ludwig, 1875)	AVR, BB, CB, PTB	PEMAV	csh, scr	UFPB.ECH.1216
Ocnus braziliensis (Verrill, 1868)	CB	APANQ	scr	UFPB.ECH.1063
Phyllophoridae Östergren, 1907
Pentamera paraibanensis Prata & Christoffersen, 2016	BB, CB, CBD, CQ, PC, TB	APANQ	phy, rhb, scr	UFPB.ECH.141
Pentamera pulcherrima Ayres, 1852	CBD	—	rhb	UFPB.ECH-2147
Stolus cognatus (Lampert, 1885)	AVR, BB, BC, CB, CBD, PCP, RS, TB	APANQ, PEMAV	rhb	UFPB.ECH.854
Thyone brasiliana Prata, Manso & Christoffersen, 2020	BB	—	rhb	UFPB.ECH.2121
Thyone crassidisca Miller & Pawson, 1981	CBD	—	csh, rhb	UFPB.ECH.2113
Thyone pawsoni Tommasi, 1972	RS	APANQ	rhb, scr	UFPB.ECH.1992
Thyone pseudofusus Deichmann, 1930	BB, CBD	—	rhb	UFPB.ECH.2116
Psolidae Burmeister, 1837
Lissothuria braziliensis (Théel, 1886)	CB, RS	APANQ	scr, rhb	UFPB.ECH.1292
Sclerodactylidae Panning, 1949
Pseudothyone belli (Ludwig, 1886)	AT, BB, CB, CBD, TB	APANQ	phy, rhb	UFPB.ECH.146
Coronatum baiensis Martins & Souto in Martins, Souto & Menegola, 2012	BB, CBD, TB	—	rhb	UFPB.ECH.2155
Euthyonidiella occidentalis (Ludwig, 1875)	AVR, BB, BC, CB, CBD, JM, PCP, PH, PTB, RS, TB	APANQ, PEMAV	rhb, scr	UFPB.ECH.2110
Euthyonidiella trita (Sluiter, 1910)	BB	—	rhb	UFPB.ECH.2124

The number of echinoderm species recorded in Paraíba (74 spp.) corresponds to 39% of the total number of species known for the entire northeastern region of Brazil, where 191 species are recorded (Table 3). The state of Bahia has the largest number of recorded species, 131 (69% of the total species), followed by Alagoas, with 75 spp. (39%). On the other hand, the smallest species diversity is recorded for the states of Piauí and Sergipe, with 8 and 11 species, respectively.

A dendrogram indicates that the state of Bahia separates from the remaining northeastern states (Fig. 6a-f), except for Crinoidea, in which Bahia groups with others 5 states (Rio Grande do Norte, Sergipe, Paraíba, Alagoas and Ceará), due to their sharing a low number of species (Fig. 6b). Groupings by nMDS share the states of Bahia, Paraíba, Pernambuco, Rio Grande do Norte, Alagoas, and Ceará, based on the composition of echinoderm faunas (Fig. 7a-f).

Uses, impacts and threats. From the literature and in situ observations, it has been possible to record different uses and moderate populational pressure on echinoderms throughout the state. Basically, echinoderms (mainly Asteroidea and Echinoidea) are used as souvenirs in the confection of zoological artisanal artifacts (Fig. 8). The main threats to this fauna lie in the unplanned use of reef environments, causing alterations or destruction of these habitats, in pollution, and accidental capture during fishing with trawling nets. 

Within the phylum, Asteroidea is the group that suffers the greatest threats in the state. It is common to observe the selling of dried specimens of Oreaster reticulatus and Astropecten spp., that serve as decoration items in shops, hotels, and bars. Young specimens of Astropecten spp. are commonly used in the confection of costume jewelry (Fig. 8). Luidia senegalensis (Lamarck, 1816) and Astropecten marginatus Gray, 1840 are frequently found as part of the bycatch of net trawlings along the beaches. Although accidental captures are common, the number of individuals in these events is low.

Direct pressures are low for class Echinoidea. Yet, echinoid tests are used as decorative items. These animals are also used asexperimental models in scientific research. However, no significant captures or threats were detected for the remaining species in our state. There are no records of uses in the aquarium trade, nor of the fishing of sea urchins and sea cucumbers for local consumption or to supply external markets.

Discussion

Description and cataloguing of the biodiversity is a continuous process. Based on present results, we may consider that the biodiversity of shallow-water echinoderms in Paraíba is well documented. Further, considering the large dimensions of Brazil, and the comparatively short extension of the Paraíba coast, the third smallest in the country, the diversity from the area is high. These species represent 39% of those known for northeastern Brazil, 21% of those known for the country (339 spp.), 16% of the Caribbean fauna (433 spp.; Alvarado, 2011), 11% of the Atlantic sector of South America (627 spp.; Pérez-Ruzafa et al., 2013), and 4.8% of Latin America (1,539 spp.; Alvarado & Solís-Marín, 2013). Considering biodiversity, 39% of the species of Ophiuroidea from Northeastern Brazil are compiled, 21% of the Brazilian fauna (134 spp.), and 20% of the species known from the Caribbean Sea (148 spp.; Alvarado, 2011). For Holothuroidea, these numbers are 52%, 30% (69 spp.), and 33% (63 spp.; Alvarado, 2011), respectively. Two species are endemic to the state: Parathyone paraibanensis Prata & Christoffersen, 2016 and Thyone brasiliana Prata, Manso & Christoffersen, 2020.

Table 3

Number of species of echinoderms arranged by class for each state in Northeast Brazil.

States	Number of species for taxon	Total
	Crinoidea	Asteroidea	Ophiuroidea	Echinoidea	Holothuroidea
Maranhão	8	3	16	3	0	30
Piauí	0	2	2	2	2	8
Ceará	6	7	25	7	4	49
Rio Grande do Norte	1	7	18	8	11	45
Paraíba	3	12	20	8	21	74
Pernambuco	7	12	25	9	9	62
Alagoas	4	8	27	17	19	75
Sergipe	1	1	5	4	0	11
Bahia	6	18	60	21	26	131
NE Brazilian coast	17	28	74	31	40	191

 

These numbers are relevant when compared to the more diverse areas in the tropical Atlantic Ocean, where intensive sampling has been conducted, such as the Gulf of Mexico (522 species; Pawson et al., 2009) and Caribbean Sea (Alvarado, 2011). The fauna recorded in Paraíba refers mainly to hard substrates (reefs) and rhodolith beds in shallow water, from the intertidal to 35 m in depth. When greater depths and new habitats become better explored, these numbers should increase substantially. 

Considering only the composition of echinoderms from shallow reefs in Paraíba, the most common species were Aphipholis squamata, “Ophiothrix (O.) angulata”, Ophionereis reticulata, Ophiactis savignyi (Müller & Troschel, 1842), Ophiocnida scabriuscula (Lütken, 1859), Echinometra lucunter, and Holothuria (Halodeima) grisea Selenka, 1867. These are generally also the most common reef species in other localities of northeastern Brazil, with a few additions (Alves & Cerqueira, 2000; Gondim & Giacometti, 2010; Lima-Verde, 1969; Martins & Martins de Queiroz, 2006; Miranda et al., 2012). It is noteworthy that some species found in the shallow reefs between Pernambuco and Bahia are not found in the coastal reefs of Paraíba. For example, Eucidaris tribuloides, a common species in the intertidal zone along the coasts of Pernambuco, Alagoas and Bahia, occurs in Paraíba, restricted to depths greater than 10 m (Gondim et al., 2018). Furthermore, the records of E. tribuloides in Paraíba are from 1981, there being no recent records and information on the status of the local populations.

In terms of similarity of the echinoderm fauna from Paraíba reefs, a cluster was observed among areas with similar topological and environmental characteristics. Those areas with similar types of reefs are the most similar in echinoderm composition. A cluster is formed by Barra de Mamanguape, Baía da Traição, and Pedra da Galé, which are very similar regarding topography, biogenic constitution, and availability of microhabitats. However, we believe that these results are due mainly to the availability of microhabitats provided by different types of reefs. The reefs here classified as “barrier reefs” are less complex environments, with few tide pools, and low algal and coralline covering. It is well known that structurally more complex environments offer more habitats and niches, permitting the coexistence of several species and promoting a higher diversity (Beck, 2000; Kerr, 2001; Kostylev et al., 2005; Kovalenko et al., 2012; Matias et al., 2010). However, it is necessary to look at these results with care, because in some cases they could reflect different sampling efforts between areas over time, particularly when we consider the echinoderm classes.

The dendrogram of records in each state in northeast Brazil showed groups shared between closer states that share more similar coastal characteristics. Yet, when each class is considered separately, the groups tend to reflect sampling procedures, and thus are related to the degree of local knowledge of the fauna. Pérez-Ruzafa et al. (2013) analysed biogeographical patterns of echinoderms in Latin America, concluding that similarity between country faunas depends on climatic and trophic conditions and geographical proximity, and that the number of species is highly dependent of the length of the coast. From such a premise, one could expect that the states with highest diversity would be Bahia, Maranhão, Ceará, and Rio Grande do Norte, respectively. When mapping the species every 10 km, Paraíba recorded the highest value (5.1), followed by Alagoas (3.2), Pernambuco (3.2), Bahia (1.4), Piauí (1.1), Rio Grande do Norte (1.0), Sergipe (0.6), and Maranhão (0.4). Thus, the patterns found by Pérez-Ruzafa et al. (2013) are only applicable in part to the northeastern states. The disparity in sampling efforts is an important factor that can influence the interpretation of geographic patterns (Price et al., 1999), species richness, and species similarity. Furthermore, the results generated by the dendrogram and nMDS may be related to sampling efforts in each area, lack of taxonomic expertise, limited funding for research, and limited access to sampling in some area. Local environmental conditions and anthropogenic interference in each sector of the littoral may also influence results.

Throughout the years studying echinoderms, we have noticed reductions in some populations in shallow reefs, and a moderate loss of diversity in these environments. For example, the reef at Cabo Branco, where 31 species of echinoderms have been recorded, displayed an exuberant and diverse fauna up to the middle of 2010 (Dias, 2009; Duarte et al., 2014; Gama et al., 2006; Gondim et al., 2008; Leonel et al., 2012; Lomônaco et al., 2011; Riul et al., 2008; Rosa et al., 1997), with several endemic species (e.g., Siderastrea stellata Verrill, 1868, Voluta ebraea Linnaeus, 1758). Today, the area is visibly impoverished. 

Common species in the area, such as Echinometra lucunter, Ophioderma cinereum, Echinaster (O.) echinophorus, and Linckia guildingi are presently rarely observed. Although Cabo Branco reef is a naturally dynamic reef, the erosion of the adjoining cliff has gradually buried a large part of the reef. This process of erosion has been accelerated by increasing constructions in the area, with inadequate use of the soil, deforestation, inadequate maintenance of soil drainage, and circulation of vehicles close to the shoreline at the edge of the cliff (Pinto et al., 2017). Further, the natural pools during low tides are increasingly used for bathing and subsistence fishermen. Only recently (Dec. 28, 2018) this reef has been included in a UC (APANQ).

Cabo Branco is an example of the gradual loss of diversity in recent years. Unfortunately, it is difficult to pinpoint particular culprits. Local stressors (e.g., pollution, coastal acidification) may be responsible, direct anthropic actions (e.g., change or loss of habitats), the activity of pathogens on the populations, or even to anomalous temperatures in sea surface water recorded in the area during the last decade. Ocean warming and ocean acidification are amply recognized stress factors because they affect the physiology, biology, and behavior of echinoderms across life-history stages (Bellucci & Smith, 2019; Brennand et al., 2010; Byrne & Hernández, 2020; Gooding et al., 2009; Wood et al., 2008; Yuan et al., 2016). When associated with a recent case of oil spilling that has affected several beaches in Paraíba, the situation becomes worrisome. Monitoring studies are essential to an understanding of the factors affecting the local echinoderm populations. Echinoderms participate, for example, in the carbon cycle, producing and winnowing vast quantities of the world’s seafloor sediments, enhancing the productivity of the benthic biota, through metabolites and their excreta, and acting to increase seawater alkalinity, which contributes to local buffering of ocean acidification (Guillén et al., 2008; Hendler et al., 1995; Lebrato et al., 2010; Purcell et al., 2016).

On the positive side, about 67% of the species recorded in this study occur in UCs in the state. Yet, they all represent Sustainable Use Units (SNUC, 2002), many with intense touristic exploitation, where surveillance is mostly lacking. Considering that we are beginning a United Nations Decade of Ocean Science for Sustainable Development (2021-2030) (ONU, 2019), geo-referenced historical (literature and collections-based) invertebrate species inventories can be a useful early step in biodiversity knowledge-gathering towards marine area conservation (Sloan & Bartier, 2009).

Conservation. Brazil is conservatively estimated to contain more than 13% of the world’s biota (Brandon et al., 2005). A large part of this biodiversity is located in marine environments (e.g., mangroves, reefs, rhodolith beds). Such environments are of great biological importance, representing important oases of biodiversity, and functioning as nursery grounds (Donato et al., 2011; Horta et al., 2016; Leão et al., 2016; Schaeffer-Novelli et al., 2000). Yet, these environments, and consequently their flora and fauna, suffer increasing pressure from human activities (e.g., real estate speculation, tourism, pollution, global warming, etc.).

According to the Instituto Chico Mendes de Conservação da Biodiversidade – ICMBIO (2018), the capture of marine invertebrates, directed to consumption, to aquarium trade, or used as bait, are the main threat to this fauna in coastal waters in Brazil. They are followed in importance by pollution of the coastal and marine environment. Presently, 657 species of marine invertebrates are listed in the Brazilian Red List (BRL), of which 38 are echinoderms. Among the categories of threat included in IUCN (The International Union for Conservation of Nature), the species of echinoderms present in the BRL are classified as critically endangered (CR = 1 sp.), endangered (EN = 1 sp.), vulnerable (VU = 8 spp.), and of least concern (LC = 28 spp.).

There have been no specific studies with the objective of evaluating the conservation status of echinoderms in Brazil (Gondim et al., 2018). Data on the conservation status of species may be found in Machado et al. (2008), Ventura et al. (2013, 2018), and Gondim et al. (2018). In Paraíba, Gondim, Dias et al. (2014) pointed out the importance of conserving rhodolith beds for the echinoderm fauna.

In general, data on the status of populations of echinoderms in Paraíba are practically non-existent. Consequently, it is difficult to establish the threatened status over this fauna. As previously mentioned, observations in situ and observations of traditional local communities have recorded reductions in the sizes of these populations. Recently, Gondim et al. (2018) recorded a reduction in the populations of Echinometra lucunter and Lytechinus variegatus in several areas of Paraíba (e.g., beaches of Cabo Branco, Seixas, Camboinha, Formosa, Jacarapé, among others). This same situation applies to Ophioderma appressum and O. cinereum, previously common species that are now not often observed on several reefs in our state.

Interestingly all species of Asteroidea recorded in this study are in the BRL. Excepting Luidia senegalensis, Astropecten marginatus, and Linckia guildingi, the remaining occurrences of sea stars throughout the Paraíba state are historical records (with more than 10 years). For example, the most recent record of Oreaster reticulatus is from rhodolith beds at a depth of 6 m in 2005 (UFPB.ECH.1871). Since then, the species has not been observed in situ. This information is worrisome because the species suffers from the illegal collecting by the aquarium trade (Gasparini et al., 2005; Lunn et al., 2008). When dried they are used in traditional folk medicine, in magicreligious rituals, and are sold, in the hundreds, as a decorative piece (Alves & Dias, 2010; Alves et al., 2006, 2018; Machado et al., 2008; Ferreira et al., 2012, 2013). In the northeast, Dias et al. (2017) recorded several dry specimens of O. reticulatus for sale in a beach tent in Coqueirinho beach (Paraíba). Alves et al. (2006) recorded the sale of several dried individuals in the city of Recife (Pernambuco). Martins et al. (2012) recorded the capture of 142 specimens in Bahía de Todos os Santos (Bahia), between 1996 and 2005, for the aquarium trade. In the southeast, Pinheiro et al. (2018) recorded the daily capture of 24 individuals of the species, also to replenish the aquarium trade in Espírito Santo. According to Ventura et al. (2018), populations of O. reticulatus are suffering a strong decrease, less than 2,500 adult individuals being estimated as extant. These authors further estimate that a reduction in the order of 30% has occurred in populations from the northeast, where smaller and smaller individuals are being commercialized. The capture of O. reticulatus has been prohibited along the Brazilian littoral since 2004, except for scientific purposes (Normative Instruction nº 05/2004 of Ministry of Environment) (Ventura et al., 2018).

Echinaster (O.) echinophorus was one of the commonest species of sea stars in shallow reefs of Paraíba. Presently it is observed only sporadically in situ, suggesting a reduction in local populations. This is a widely used species by aquarium enthusiasts, in zoological costume jewelry, and traditional folk medicine (Alves & Dias, 2010; Ferreira et al., 2012; Gurjão & Lotufo, 2018; Gurjão et al., 2018; Machado et al., 2008). Ferreira et al. (2013) recorded that E. (O.) echinophorus and other species of echinoderms are being sold for medicinal purposes in cities far removed from the coast, such as Juazeiro do Norte (Ceará), Caruaru and Santa Cruz do Capibaribe (Pernambuco). This demonstrates that the commercial demand for these organisms is not restricted to coastal cities. Among the reefs in Paraíba, L. guildingi is observed in few areas and only sporadically. This species characteristically forms populations with low densities. It is estimated that populations along the Brazilian coast have less than 10,000 adult individuals. Although the capture of this species is rarely documented, their populations are decreasing strongly (Machado et al., 2008). Martins et al. (2012) recorded the collection of L. guildingi (437 specimens; a mean of 50 specimens per year) for aquarium trade along the coast of Bahia. The capture of Echinaster spp. and L. guildingi are also prohibited.

Species of Astropecten and Luidia suffer mainly from accidental capture in trawling fisheries. Although populational data for the species of these genera are not available, it has been estimated that their populations suffered a reduction of 30% in their area of occurrence (Ventura et al., 2018). Like other sea stars, the capture of both genera is prohibited in Brazil, yet swimmers are very commonly observed capturing specimens of L. senegalensis and A. marginatus. These individuals sometimes are returned to the sea, but often they are taken home to serve as objects of decoration.

Only 2 species of Holothuroidea [Synaptula secreta Ancona Lopez, 1957, endemic to São Paulo, and Isostichopus badionotus (Selenka, 1867) —with a record for the northeast] are in BRL. There are no official records of holothurian fisheries in Brazil, but in 2001 about 0.45 tons of dry sea cucumbers were exported to Hong Kong (Machado et al., 2008). In recent years the media has been announcing the apprehension of several kilograms of sea cucumbers in the southeast (e.g., in 2018, 200 kg of sea cucumbers were seized in Angra dos Reis, Rio de Janeiro; in January 2019, fishermen denounced contracts for collecting these animals in Ilha Grande – RJ, that would later be sold in the international trade). In the northeast, Ponte (2017) recorded the fishing of about 200 thousand specimens of Holothuria (H.) grisea on the coast of Ceará during 1 year. Many of these individuals (66.5%) had not attained first sexual maturity (less than 13 cm) and only 33.5% (≥ 13.00 cm) had already reproduced at least once (Ponte & Feitosa, 2019). According to Souza Jr. et al. (2017), sea cucumber collection in Ceará started about 20 years ago, but intensified rapidly over the last 11 years, as a complementary income activity of traditional fisheries. Along the coast of Bahia, approximately 1,300 specimens of H. (H.) grisea were collected during 10 years for the aquarium trade (mean of 144 individuals annually) (Martins et al., 2012). Although no population data are available for H. (H.) grisea, in a locality in Ceará (a beach close to the village of Bitupitá) a population decline of 98.7% over a period of 4 years has been estimated (Souza Jr. et al., 2017). Gurjão and Lotufo (2018) recorded the illegal selling of holothurians in discussion forums, under the common names “giant sea cucumber”, “detritivorous sea cucumber” and “burrowing sea cucumber”. So far, there is no record of the capture of these animals along the coast of Paraíba for any purpose. Although H. (H.) grisea is a common species, it does not form dense populations in the study area.

No one species of Crinoidea is considered threatened in Brazil. However Tropiometra carinata was the third most captured echinoderm for the aquarium trade in Baía de Todos os Santos (Bahia) between 1996 and 2005. During this period, about 190 specimens were captured annually (Martins et al., 2012). Hadel et al. (1999) cited a significant reduction in the populations of this species in the coast of São Paulo (southeastern of Brazil). Along the coast of Paraíba, the 3 recorded species are not common, and occur in areas abundantly used for touristic activities.

Although the capture of several echinoderms is prohibited in Brazil, there is no inspection and a majority of the population ignores such prohibitions. Artisanal markets commercializing these animals are quite common. Species of sea stars and sea urchins are the main representatives sold in the curiosity trade around the world, being used for decoration or for the confection of artisanal craft in general (Alves et al., 2018). Education programs on the importance of these animals and on the current legislation are fundamental to avoid the withdrawal of these animals from nature.

The largest obstacle for conservation strategies is the lack of information on the status of specific populations. The necessity for research on the biology and ecology of marine organisms is thus essential to reduce the anthropic impacts on echinoderms along our coast. 

General guidelines for the future

Circa 81% of the species of echinoderms recorded for the coast of Paraíba is concentrated in shallow reefs down to 10 m. Below this depth, there are a few historical records dating mainly from 1981. Records refer basically to Ophiuroidea, Asteroidea, and Echinoidea. There is a complete lack of knowledge of the entire echinoderm fauna from the lower continental shelf, from bathyal and from abyssal waters. Inventories are thus necessary from depths below 10 m. More funds are needed for sampling and for maintaining scientific collections. A continuous formation of new specialists for the study of the group should be forthcoming.

A relevant point is that 99% of the ongoing studies developed along the coast of the State of Paraíba are taxonomical (inventories, new records, and new species descriptions). Biological, ecological and populational studies are virtually nonexistent. Recently, with the joining of the first author to the Postgraduate Program in Conservation and Ecology as a professor (PPGEC-UEPB), the development of research on biology and reproductive ecology of echinoderm species has started in our state (e.g., Cerqueira 2020). Such research is still incipient and needs to be complemented with further studies on the status of these populations.

We know that the incidental capture of echinoderms in trawling nets is common. However, information on the impacts of this activity on echinoderm populations is limited. Another important factor is that during trawling activities, it is common for fishermen to discard captured specimens. Even though many specimens end up returned to the sea, many of them are already dead after long exposure out of the water. Along the coast of Santa Catarina (southern Brazil), for example, Branco et al. (2015) recorded 11 species of echinoderms in the bycatch of seabob shrimp trawl fisheries. These captured species belonged to the sea stars Astropecten brasiliensis Müller and Troschel, 1842, A. marginatus, Luidia clathrata (Say, 1825), Luidia senegalensis, Asterina stellifera (Möbius, 1859), Echinaster (O.) brasiliensis, 3 echinoids, Arbacia lixula (Linnaeus, 1758), L. variegatus, Mellita quinquiesperforata (Leske, 1778), and 2 brittle stars, Microphiopholis atra (Stimpson, 1852) and Hemipholis cordifera (Bosc, 1802). Data such as these are not available for the coastline in northeastern Brazil. Studies evaluating the impact of fishing activities on echinoderms are needed along the entire coastline of Brazil.

In short, the most critical points highlighted by our results are: 1) little knowledge of the fauna below the depth of 10 meters; 2) the necessity of ecological studies and on monitoring the fauna; 3) lack of evaluation of the impact of commercial activities (e.g., bycatch and captures for the aquarium trade, for medicinal use, and for use in handicrafts). The database, however, is already constructed (inventories and taxonomical studies). New strategies can now be planned according to local demands and following the recommendations of the scientific community. All research lines indicated herein are indispensable for the attainment of efficient public policies aimed at the conservation of these animals. We stress that in order to close the gaps highlighted herein, there is a demand for organization and financial support.

Acknowledgements

This paper is dedicated to Carmen Alonso and Cynthia Lara de Castro Manso (UFS), who inspired the first author to study echinoderms. We thank Rafael B. de Moura (UFRJ) for valuable discussions and suggestions during the elaboration of this text. We would also like to thank all researchers that deposited specimens of echinoderms in CIPY, thus contributing to this study. Anne I. Gondim was supported by CNPq through a postdoctoral scholarship (process number: 150070/2018-7), and Martin L. Christoffersen was supported by a CNPq productivity research grant (process number: 301288/2018-6). 

References

Albuquerque, M. N. (1986). Ophiuroidea Gray, 1840 (Echinodermata) da plataforma continental do norte e nordeste brasileiro (Ph.D. Thesis). Universidad de São Paulo, São Paulo, Brasil.

Albuquerque, M. N., & Guille, A. (1991). Ophiuroidea (Echinodermata) ao largo do Brasil: Banco dos Abrolhos, Cadeia Submarina Vitória-Trindade e plataforma continental adjacente. Boletim do Museu Nacional, 353, 1–29.

Alvarado, J. J. (2011). Echinoderm diversity in the Caribbean Sea. Marine Biodiversity, 41, 261–285. http://dx.doi.org/10.1007/s12526-010-0053-0 

Alvarado, J. J., & Solís-Marín, F. A. (2013). Echinoderm research and diversity in Latin America. In J. J. Alvarado & F. A. Solís-Marín (Eds.), Echinoderm research and diversity in Latin America (pp. 1–9). Springer-Verlag Berlin Heidelberg. http://dx.doi.org/10.1007/978-3-642-20051-9_1 

Alves, O. F. S., & Cerqueira, W. R. P. (2000). Echinodermata das praias de Salvador (Bahia, Brasil). Revista Brasileira de Zoologia, 17, 543–553.

Alves, R. R. N., & Dias, T. L. P. (2010). Usos de invertebrados na medicina popular no Brasil e suas implicações para conservação. Tropical Conservation Science, 3, 159–174.

Alves, R. R. N., Mota, E. L. S., & Dias, T. L. P. (2018). Use and commercialization of animals as decoration. In R. R. N. Alves & U. P. Albuquerque (Eds.), Ethnozoology: animals in our lives (pp. 261–275). Springer, Switzerland. http://dx.doi.org/10.1016/B978-0-12-809913-1.00014-4 

Alves, M. S., Silva, M. A., Júnior, M. M., Paranaguá, M. N., & Pinto, S. L. (2006). Zooartesanato comercializado em Recife, Pernambuco, Brasil. Revista Brasileira de Zoociências, 8, 99–109.

Amaral, A. C. Z., & Jablonski, S. (2005). Conservation of marine and coastal biodiversity in Brazil. Conservation Biology, 19, 625–631. https://doi.org/10.1111/j.1523-1739.2005.00692.x 

Barbosa, C. M. B. M. (1989). Sedimentos carbonáticos da plataforma continental do estado da Paraíba. Tropical Oceanography, 20, 125–134. https://doi.org/10.5914/tropocean.v20i1.2628 

Beck, M. W. (2000). Separating the elements of habitat structure: independent effects of habitat complexity and structural components on rocky intertidal gastropods. Journal of Experimental Marine Biology and Ecology, 249, 29–49. https://doi.org/10.1016/S0022-0981(00)00171-4 

Bellucci, L. M. A., & Smith, N. F. (2019). Crawling and righting behavior of the subtropical sea star Echinaster (Othilia) graminicola: effects of elevated temperature. Marine Biology, 166, 138. https://doi.org/10.1007/s00227-019-3591-4 

Branco, J. O., Júnior, F. F., & Christoffersen, M. L. (2015). Bycatch fauna of seabob shrimp trawl fisheries from Santa Catarina State, southern Brazil. Biota Neotropica, 15, 1–14. http://dx.doi.org/10.1590/1676-06032015014314 

Brandon, K., Fonseca, G. A. B., Rylands, A. B., & Silva, J. M. C. (2005). Brazilian Conservation: Challenges and Opportunities. Conservation Biology, 19, 595–600. https://www.jstor.org/stable/3591041 

Branner, J. C. (1902). Geology of the Northeast coast of Brazil. Bulletin of the Geological Society of America, 13, 41–98.

Branner, J. C. (1904). The stone reefs of Brazil, their geological and geographical relations, with a chapter on the coral reefs. Bulletin of the Museum of Comparative Zoology at Harvard College, 44. Cambridge, Mass.: Harvard College.

Brennand, H. S., Soars, N., Dworjanyn, S. A., Davis, A. R., & Byrne, M. (2010). Impact of Ocean warming and Ocean acidification on larval development and calcification in the sea urchin Tripneustes gratilla. Plos One, 5, e11372. https://doi.org/10.1371/journal.pone.0011372 

Brito, R. J., de Assis, J. E., & Christoffersen, M. L. (2013). First record of Chaetacanthus magnificus (Polychaeta: Polynoidae) from the northeast coast of Brazil, with an overview of its taxonomic history. Cuadernos de Investigación UNED, 5, 25–32. https://doi.org/10.22458/urj.v5i1.190 

Byrne, M., & Hernández, J. C. (2020). Sea urchins in a high CO2 world: impacts of climate warming and ocean acidification across life history stages. In J. M. Lawrence (Ed.), Sea urchins: Biology and Ecology, 4th Edition (pp. 281–297). London: Elsevier. http://dx.doi.org/10.1016/B978-0-12-819570-3.00016-0 

Carvalho, M. G. R. F. (1982). Estado da Paraíba. Classificação geomorfológica. Paraíba: Editora Universitária/ Universidade Federal da Paraíba, João Pessoa.

Cerqueira, N. F. L. (2020). Dinâmica populacional, micro-hábitat, biologia alimentar e reprodutiva de Ophioderma appressum (Say, 1825) (Ophiodermatidae, Ophiuroidea, Echinodermata) em recifes costeiros da Paraíba, Brasil (Master Thesis). Universidade Estadual da Paraíba, Paraíba, Brasil.

Chaves, H. A. F. (1979). Geomorfologia da margem continental brasileira e das áreas oceânicas adjacentes. Série Projeto REMAC 7. Petrobras, DNPM, CPRM, DHN, CNPq.

Clark, A. M. (1953). A revision of the genus Ophionereis (Echinodermata, Ophiuroidea). Proceedings of the Zoological Society of London, 123, 65–94. https://doi.org/10.1111/j.1096-3642.1953.tb00157.x

Clark, H. L. (1915). Catalogue of recent Ophiurans: based on the collection of the Museum of Comparative Zoology. Bulletin of the Museum of Comparative Zoology at Harvard College, 25, 165–376. https://doi.org/10.5962/bhl.title.48598

de Assis, J. E., Alonso, C., Brito, R. J., Santos, A. S., & Christoffersen, M. L. (2012). Polychaetous annelids from the coast of Paraíba State, Brazil. Revista Nordestina de Biologia, 21, 3–45.

de Assis, J. E., Alonso, C. S., & Christoffersen, M. L. (2007). Two new species of Nicomache (Polychaeta: Maldanidae) from the Southwest Atlantic. Zootaxa, 1454, 27–37. https://doi.org/10.11646/zootaxa.1454.1.2 

de Assis, J. E., Bezerra, E. A. S., Brito, R. J., Gondim, A. I., & Christoffersen, M. L. (2012). An Association between Hesione picta (Polychaeta: Hesionidae) and Ophionereis reticulata (Ophiuroidea: Ophionereididae) from the Brazilian Coast. Zoological Studies, 51, 762–767.

Dias, T. L. P. (2009). First field study of the Brazilian endemic marine gastropod Voluta ebraea Linnaeus, 1758 (Mollusca: Volutidae). Marine Biodiversity Records, 2, e10. https://doi.org/10.1017/S1755267208000109 

Dias, T. L. P., & Gondim, A. I. (2016). Bleaching in scleractinians, hydrocorals, and octocorals during thermal stress in a northeastern Brazilian reef. Marine Biodiversity, 46, 303–307. https://doi.org/10.1007/s12526-015-0342-8 

Dias, T. L. P., Mota, E. L. S., Duarte, R. C. S., & Alves, R. R. N. (2017). What do we know about Cassis tuberosa (Mollusca: Cassidae), a heavily exploited marine gastropod? Ethnobiology and Conservation, 6, 16.

Dias, T. L. P., Mota, E. L. S., Gondim, A. I., Oliveira, J. M., Rabelo, E. F., Almeida, S. M., & Christoffersen, M. L. (2013). Isognomon bicolor (C. B. Adams, 1845) (Mollusca: Bivalvia): first record of this invasive species for the States of Paraíba and Alagoas and new records for other localities of Northeastern Brazil. Check List, 9, 157–161. http://dx.doi.org/10.15560/9.1.157 

Donato, D. C., Kauffman, J. B., Murdiyarso, D., Kurnianto, S., Stidham, M., & Kanninen, M. (2011). Mangroves among the most carbon-rich forests in the tropics. Nature Geoscience, 4, 293–297. https://doi.org/10.1038/ngeo1123 

Duarte, R. C. S., Mota, E. L. S., & Dias, T. L. P. (2014). Mollusk fauna from shallow-water back reef habitats of Paraíba coast, northeastern Brazil. Strombus, 21, 15–29.

Feitosa, B. M., Rosa, R. S., & Rocha, L. A. (2005). Ecology and zoogeography of deep reef fishes in northeastern Brazil. Bulletin of Marine Science, 76, 725–742.

Ferreira, F. S., Albuquerque, U. P., Coutinho, H. D. M., Almeida, W. O., & Alves, R. R. N. (2012). The Trade in medicinal animals in Northeastern Brazil. Evidence-Based Complementary and Alternative Medicine, 2012, 126938. https://doi.org/10.1155/2012/126938 

Ferreira, F. S., Fernandes-Ferreira, H., Neto, N. A. L., Brito, S. V., & Alves, R. R. N. (2013). The trade of medicinal animals in Brazil: current status and perspectives. Biodiversity and Conservation, 22, 839–870. https://doi.org/10.1007/s10531-013-0475-7 

Gama, P. B., Leonel, R. M. V., Hernández, M. I. M., & Mothes, B. (2006). Recruitment and colonization of colonial ascidians (Tunicata: Ascidiacea) on intertidal rocks in Northeastern Brazil. Iheringia, 96, 165–172. https://doi.org/10.1590/S0073-47212006000200005

Gasparine, J. L., Floeter, S. R., Ferreira, C. E. L., & Sazima, I. (2005). Marine Ornamental Trade in Brazil. Biodiversity and Conservation, 14, 2883–2899. https://doi.org/10.1007/s10531-004-0222-1 

Gondim, A. I., Christoffersen, M. L., & Dias, T. L. P. (2014). Taxonomic guide and historical review of starfishes in northeastern Brazil (Echinodermata, Asteroidea). Zookeys, 449, 1–56. https://doi.org/10.3897/zookeys.449.6813 

Gondim, A. I., Dias, T. L. P., Campos, F. F., Alonso, C., & Christoffersen, M. L. (2011). Macrofauna bêntica do Parque Estadual Marinho de Areia Vermelha, Cabedelo, Paraíba, Brasil. Biota Neotropica, 11, 75–86. https://doi.org/10.1590/S1676-06032011000200009 

Gondim, A. I., Dias, T. L. P., Duarte, R. C. S., Riul, P., Lacouth, P., & Christoffersen, M. L. (2014). Filling a knowledge gap on the biodiversity of rhodolith-associated Echinodermata from northeastern Brazil. Tropical Conservation Science, 7, 87–99.

Gondim, A. I., & Giacometti, A. C. M. (2010). Equinodermos. In A. C. M. Giacometti & D. Loebmann (Orgs.), Biodiversidade do litoral do Piauí (pp. 129–133). Gráfica e Editora Paratodos Sorocaba Ltda, Sorocaba, Brasil.

Gondim, A. I., Lacouth, P., Alonso, C., & Manso, C. L. C. (2008). Echinodermata da praia do Cabo Branco, João Pessoa, Paraíba, Brasil. Biota Neotropica, 8, 151–159. https://doi.org/10.1590/S1676-06032008000200016 

Gondim, A. I., Manso, C. L. C., & Alonso, C. (2010). First record of Ophionereis dolabriformis (Echinodermata: Ophiuroidea: Ophionereididae) for the Brazilian coast. Marine Biodiversity Records, 3, e34. https://doi.org/10.1017/S1755267210000096 

Gondim, A. I., Moura, R. B., Christoffersen, M. L., & Dias, T. L. P. (2018). Taxonomic guide and historical review of echinoids (Echinodermata: Echinoidea) from northeastern Brazil. Zootaxa, 4529, 001–072. https://doi.org/10.11646/zootaxa.4529.1.1 

Gooding, R. A., Harley, C. D. G., & Tang, E. (2009). Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. PNAS, 106, 9316–9321. https://doi.org/10.1073/pnas.0811143106 

Guilcher, A. (1983). Gèomorphologie et utilisation de la côte de la Paraiba (Brésil). In Geographie et écologie de la Paraibá (Brésil), Vol II. Travaux et Documents de Gérographie Tropicale, Bordeaux-Talence, CEGET, 50, 373–425.

Guilcher, A. (1988). Coral reef geomorphology. John Wiley, New York.

Guillén, J., Soriano, S., Demestre, M., Falqués, A., Palanques, A., & Puig, P. (2008). Alteration of bottom roughness by benthic organisms in a sandy coastal environment. Continental Shelf Research, 28, 2382–2392. https://doi.org/10.1016/j.csr.2008.05.003

Gurjão, L. M., & Lotufo, T. M. C. (2018). Native species exploited by marine aquarium trade in Brazil. Biota Neotropica, 18, e20170387. http://dx.doi.org/10.1590/1676-0611-BN-2017-0387 

Gurjão, L. M., Barros, G. M. L., Lopes, D. P., Machado, D. A. N., & Lotufo, T. M. C. (2018). Illegal trade of aquarium species through the Brazilian postal service in Ceará State. Marine and Freshwater Research, 69, 178–185. https://doi.org/10.1071/MF16257 

Hadel, V. F., Monteiro, A. M. G., Ditadi, A. S. F., Thiago, C. G., & Tommasi, L. R. (1999). Echinodermata. In A. C. Migotto & C. G. Thiago (Eds), Biodiversidade do Estado de São Paulo, Brasil: Síntese do Conhecimento ao Final do Século XX, 3: Invertebrados Marinhos (pp. 260–271). FAPESP, São Paulo.

Hendler, G., Miller, J. E., Pawson, D. L., & Kier, P. M. (1995). Sea stars, sea urchins and allies: echinoderms of Florida and the Caribbean. Washington, D.C.:Smithsonian Institution Press. 

Horta, P. A., Riul, P., Amado-Filho, G. M., Gurgel, C. F. D., Berchez, F., Nunes, J. M. C. et al. (2016). Rhodoliths in Brazil: current knowledge and potential impacts of climate change. Brazilian Journal of Oceanography, 64, 117–136. http://dx.doi.org/10.1590/S1679-875920160870064sp2 

Instituto Chico Mendes de Conservação da Biodiversidade. (2018). Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. Volume VII – Invertebrados. In Instituto Chico Mendes de Conservação da Biodiversidade (Org.), Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. Brasília: ICMBio.

Kerr, J. (2001). Global biodiversity patterns: from description to understanding. Trends Ecology and Evolution, 16, 424–425. https://doi.org/10.1016/S0169-5347(01)02226-1 

Kostylev, V. E., Erlandsson, J., Ming, M. Y., & Williams, G. A. (2005). The relative importance of habitat complexity and surface area in assessing biodiversity: Fractal application on rocky shores. Ecological Complexity, 2, 272–286. https://doi.org/10.1016/j.ecocom.2005.04.002 

Kovalenko, K. E., Thomaz, S. M., & Warfe, D. M. (2012). Habitat complexity: approaches and future directions. Hydrobiologia, 685, 1–17. https://doi.org/10.1007/s10750-011-0974-z 

Kroh, A., & Mooi, R. (2020). World Echinoidea Database. Recuperado el 08 junio, 2020 de: http://www.marinespecies.org/echinoidea 

Laborel-Deguen, F. (1963). Nota preliminar sobre a ecologia das pradarias de fanerógamas marinhas nas costas dos estados de Pernambuco e Paraíba. Trabalhos do Instituto Oceanográfico, 3, 39–50. https://doi.org/10.5914/tropocean.v3i1.2481 

Laborel, J. (1970). Les peuplements de madréporaires des côtes tropicales du Brésil. Annales de l’Université d’Abidjan, 2, 1–260.

Lafite, N. F., Christoffersen, M. L., & Gondim, A. I. (2021). Feeding biology of the brittlestar Ophioderma appressum (Say, 1825) (Echinodermata, Ophiuroidea) in a tropical shallow reef from the Brazilian coast. Marine Biology Research, 17, 286–294. http://dx.doi.org/10.1080/17451000.2021.1943753 

Leão, Z. M. A. N., Kikuchi, R. K., Oliveira, M. D. M., & Vasconcellos, V. (2010). Status of Eastern Brazilian coral reefs in time of climate changes. Panamjas, 5, 52–63.

Leão, Z. M. A. N., Kikuchi, R. K., Ferreira, B. P., Neves, E. G., Sovierzoski, H. H., Oliveira, M. D. M. et al. (2016). Brazilian coral reefs in a period of global change: a synthesis. Brazilian Journal of Oceanography, 64, 97–116. http://dx.doi.org/10.1590/S1679-875920160916064sp2 

Leonel, R. M. V., Mothes, B., Lerner, C., Gama, P. B., & Campos, M. A. (2012). Guia ilustrado dos invertebrados da Praia do Cabo Branco. Esponjas. Holos, Ribeirão Preto.

Lebrato, M., Iglesias-Rodriguez, D., Feely, R. A., Greeley, D., Jones, D. O. B., Suarez-Bosche, N. et al. (2010). Global contribution of echinoderms to the marine carbon cycle: CaCO3 budget and benthic compartments. Ecological Monographs, 80, 441–467. https://doi.org/10.1890/09-0553.1 

Lima, S. F. B., Lucena, R. A., Santos, G. M., Souza, J. W., Christoffersen, M. L., Guimarães, C. R. et al. (2017). Inventory of mollusks from the estuary of the Paraíba River in northeastern Brazil. Biota Neotropica, 17, e20160239. https://doi.org/10.1590/1676-0611-bn-2016-0239 

Lima-Verde, J. S. (1969). Primeira contribuição ao inventário dos Echinodermas do nordeste Brasileiro. Arquivos de Ciencias do Mar, 9, 9–13.

Lomônaco, C., Santos, A. S., & Christoffersen, M. L. (2011). Effects of local hydrodynamic regime on the individual’s size in intertidal Sabellaria (Annelida: Polychaeta: Sabellariidae) and associated fauna at Cabo Branco beach, north-east Brazil. Marine Biodiversity Records, 4, e76. https://doi.org/10.1017/S1755267211000807 

Lucena, R. A., Lima, S. F. B., & Christoffersen, M. L. (2017). First record of Pallenopsis fluminensis (Krøyer, 1844) (Pycnogonida: Pallenopsidae) for the coast of the state of Paraíba (northeastern Brazil). Pesquisa e Ensino em Ciências Exatas e da Natureza, 1, 19–27. https://doi.org/10.29215/pecen.v1i1.164 

Lunn, K. E., Noriega, M. J. V., & Vincent, A. C. J. (2008). Souvenirs from the sea: an investigation into the curio trade in echinoderms from Mexico. Traffic Bulletin, 22, 19–32.

Machado, A. B. M., Drummond, G. M., & Paglia, A. P. (2008). Livro vermelho da fauna brasileira ameaçada de extinção. Ministério do Meio Ambiente, Brasília. Série Biodiversidade 19.

Mah, C. L. (2020). World Asteroidea Database. Retrieved March 1st., 2020, from: http://www.marinespecies.org/asteroidea 

Maresia. Retrieved June 14th., 2020 de: http://www.maresiatour.com.br/picaozinho-piscinas-naturais.php 

Margules, C. R., & Pressey, R. L. (2000). Systematic conservation planning. Nature, 405, 243–253. http://dx.doi.org/10.1038/35012251 

Martins, I. X., & Martins de Queiroz, A. C. (2006). Echinodermos do litoral do Estado do Ceará. In H. Matthews-Cascon & T. M. C. Lotufo (Eds.), Biota Marinha da Costa Oeste do Ceará (pp. 199–220). Brasília: Ministério do Meio Ambient.

Martins, L., Souto, C., Magalhães, W. F., Alves, O. F. S., Rosa, I. L., & Sampaio, C. L. S. (2012). Echinoderm harvesting in Todosos-Santos Bay, Bahia State, Brazil: the aquarium trade. Sitientibus, Série Ciências Biológicas, 12, 53–59. http://dx.doi.org/10.13102/scb123 

Matias, M. G., Underwood, A. J., Hochuli, D. F., & Coleman, R. A. (2010). Independent effects of patch size and structural complexity on diversity of benthic invertebrates. Ecology, 91, 1908–1915. https://doi.org/10.1890/09-1083.1 

Melo, R. S. (2006). Planejamento turístico-recreativo dos ambientes recifais das praias do Seixas, Penha e Arraial (Master Thesis). Universidade Federal da Paraíba, João Pessoa, Brasil.

Mendes, L. F., & Pinheiro, A. C. M. (2019). Recifes e/ou ambientes coralíneos de Pirangi (RN) a João Pessoa (PB). In F. Laborel-Deguen, C. B. Castro, F. D. Nunes, & D. O. Pires (Eds.), Recifes brasileiros: o legado de Laborel (pp. 92–93). Série Livros, 64, Rio de Janeiro: Museu Nacional. http://coralvivo.org.br/pesquisa-e-educacao/publicacoes 

Mikkelsen, P. M., & Cracraft, J. (2001). Marine biodiversity and the need for systematic inventories. Bulletin of Marine Science, 69, 525–534.

Miranda, A. L. S., Lima, M. L. F., Sovierzoski, H. H., & Correia, M. D. (2012). Inventory of the Echinodermata collection from the Universidade Federal de Alagoas. Biota Neotropica, 12, 135–146. https://doi.org/10.1590/S1676-06032012000200014 

Mota, E. L. S., Alves, R. R. N., & Dias, T. L. P. (2020). Fishing, trade, and local ecological knowledge of the marine gastropod, Cassis tuberosa – a target species of the international shell trade. Ethnobiology and Conservation, 9, 23. https://doi.org/10.15451/ec2020-06-9.23-1-11 

Moura, R. B. (2020). Echinodermata in Catálogo taxonômico da fauna do Brasil. PNUD. Recuperado el 21 marzo, 2020 de: http://fauna.jbrj.gov.br/fauna/faunadobrasil/8 

Muniz, M. P. A., Oliveira, M. M., & Batalla, J. F. (2000). Gastrópodes e bivalves bentónicos do infralitoral do Estado da Paraíba, Brasil. Revista Nordestina de Biologia, 14, 39–49.

Oliveira, L. M., Gamba, G. A., & Rocha, R. M. (2014). Eudistoma (Ascidiacea: Polycitoridae) from tropical Brazil. Zoologia, 31, 195–208. http://dx.doi.org/10.1590/S1984-46702014000200011 

ONU (Assembleia Geral das Nações Unidas). (2019). A Ciência que precisamos para o oceano que queremos: Década das Nações Unidas da Ciência Oceânica para o Desenvolvimento Sustentável (2021-2030). Retrieved on June 08, 2020 from: https://unesdoc.unesco.org/ark:/48223/pf0000265198_por 

Pawson, D. L., Vance, D. J., Messing, C. G., Solís-Marín, F. A., & Mah, C. L. (2009). Echinodermata of the Gulf of Mexico. In D. L. Felder & D. K. Camp (Eds), Gulf of Mexico: origin, waters, and biota (pp. 1177–1204). College Station: Texas A & M University Press.

Pérez-Ruzafa, A., Alvarado, J. J., Solís-Marín, F. A., Hernández, J. C., Morata, A., Marcos, C. et al. (2013). Latin America Echinoderm biodiversity and biogeography: patterns and affinities. In J. J. Alvarado, & F. A. Solís-Marín (Eds.), Echinoderm research and diversity in Latin America (pp. 1–9). Berlin, Heidelberg: Springer-Verlag. http://dx.doi.org/10.1007/978-3-642-20051-9_1 

Pinheiro, F. C. F., Pinheiro, H. T., Costa, T. J. F., Teixeira, J. B., Gasparini, J. L., Jean-Joyeux, J. C. et al. (2018). Harvest of endangered marine invertebrates in a priority area for conservation in Brazil. Nature Conservation Research, 3, 78–81. http://dx.doi.org/10.24189/ncr.2018.050 

Pinto, A. L. M. S., Fonseca, M. B., & Araújo, A. F. V. (2017). Percepção ambiental e valoração ambiental: o caso da Barreira do Cabo Branco em João Pessoa – PB. Reflexões Econômicas, 3, 57–77.

Prata, J., & Christoffersen, M. L. (2017). Checklist of the Holothuroidea (Echinodermata) from the State of Paraíba, Brazil. Pesquisa e Ensino em Ciências Exatas e da Natureza, 1, 45–59.

Prata, J., Costa, D. A., Manso, C. L. C., Crispim, M. C., & Christoffersen, M. L. (2017). Echinodermata associated to rhodoliths from Seixas Beach, State of Paraíba, Northeast Brazil. Biota Neotropica, 17, e20170363. http://dx.doi.org/10.1590/1676-0611-BN-2017-0363 

Prata, J., Manso, C. L. C., & Christoffersen, M. L. (2014). Aspidochirotida (Echinodermata: Holothuroidea) from the northeast coast of Brazil. Zootaxa, 3889, 127–150. http://dx.doi.org/10.11646/zootaxa.3889.1.8 

Prata, J., Manso, C. L. C., & Christoffersen, M. L. (2020). Dendrochirotida (Echinodermata: Holothuroidea) from the northeastern coast of Brazil. Zootaxa, 4755, 401–453. https://doi.org/10.11646/zootaxa.4755.3.1 

Prata, J., Stevenson, V., Silva, J., Lima, S. F. B., & Christoffersen, M. L. (2020). Echinodermata from Barra de Mamanguape, Northeast of Brazil, Tropical Southwestern Atlantic. Thalassas: An International Journal of Marine Sciences, 36, 273–289. https://doi.org/10.1007/s41208-020-00214-y 

Ponte, I. A. R. (2017). A pesca, processamento artesanal e qualidade microbiológica do produto final do pepino do mar Holothuria grisea Selenka, 1867 (Echinodermata: Holothuroidea) no extremo litoral oeste do Ceará (Tesis de maestria). Universidad Federal de Ceará, Ceará, Brasil.

Ponte, I. A. R., & Feitosa, C. V. (2019). Evaluation of an unreported and unregulated sea cucumber fishery in eastern Brazil. Ocean & Coastal Management, 167, 1–8. https://doi.org/10.1016/j.ocecoaman.2018.09.016

Price, A. R. G., Keeeling, M. J., & O’Callaghan, C. J. (1999). Ocean-scale patterns of ‘biodiversity’ of Atlantic asteroids determined from taxonomic distinctness and other measures. Biological Journal of the Linnean Society, 66, 187–203. https://doi.org/10.1006/bijl.1998.0275 

Purcell, S. W., Conand, C., Uthicke, S., & Byrne, M. (2016). Ecological roles of exploited sea cucumbers. Oceanography and Marine Biology: An Annual Review, 54, 367–386.

Rathbun, R. (1879). A list of the Brazilian echinoderms, with notes on their distribution, etc. Transactions of the Connecticut Academy of Arts and Sciences, 5, 139–151. https://doi.org/10.5962/bhl.title.16126 

Riul, P., Rodrigues, F. M. A., Xavier-Filho, E. S., Santos, R. G., Leonel, R. M. V., & Christoffersen, M. L. (2008). Macrocrustaceans from Ponta do Cabo Branco, João Pessoa, Paraíba, Brazil, the easternmost point of South America. Revista Nordestina de Biologia, 19, 3–13.

Rocha, L. A., Rosa, I. L., & Rosa, R. S. (1998). Peixes recifais da costa da Paraíba, Brasil. Revista Brasileira de Zoologia, 15, 553–566. https://doi.org/10.1590/S0101-81751998000200017 

Rosa, R. S., Rosa, I. L., & Rocha, L. A. (1997). Diversidade da ictiofauna de poças de maré da praia do Cabo Branco, João Pessoa, Paraíba, Brasil. Revista Brasileira de Zoologia, 14, 201–212. https://doi.org/10.1590/S0101-81751997000100019 

Santana, A., Manso, C. L. C., Almeida, A. C. S., & Alves, O. F. S. (2017). Redescription and designation of a neotype for Ophiothrix angulata (Say, 1825) (Echinodermata: Ophiuroidea: Ophiotrichidae). Zootaxa, 4344, 291–307. https://doi.org/10.11646/zootaxa.4344.2.5 

Santana, A., Manso, C. L. C., Almeida, A. C. S., & Alves, O. F. S. (2020). Taxonomic review of Ophiothrix Müller & Troschel, 1840 (Echinodermata: Ophiuroidea) from Brazil, with the description of four new species. Zootaxa, 4808, 051–078. https://doi.org/10.11646/zootaxa.4808.1.3 

Santos, A. S., Costa, D. A., & Christoffersen, M. L. (2008). First record of Scolelepis (Scolelepis) lighti along the Brazilian coast. Marine Biodiversity Records, 2, e39. https://doi.org/10.1017/S1755267208000183 

Santos, G. G., Nascimento, E., & Pinheiro, U. (2018). Halichondriidae Gray, 1867 from the Northeastern Brazil with description of a new species. Zootaxa, 4379, 556–566. https://doi.org/10.11646/zootaxa.4379.4.7 

Santos, G. G., & Pinheiro, U. (2013). First record of Damiria Keller, 1891 from Brazil, with the description of a new species (Poecilosclerida; Demospongiae; Porifera). Zootaxa, 3700, 597–600. http://dx.doi.org/10.11646/zootaxa.3700.4.9 

Santos, G. G., & Pinheiro, U. (2014). Two new cleistocheliferous species of Clathria of sciophilous habitats from Northeastern Brazil (Poecilosclerida: Demospongiae: Porifera). Zootaxa, 3900, 107–116. http://dx.doi.org/10.11646/zootaxa.3900.1.6 

Santos, A. S., Riul, P., Brasil, A. C. S., & Christoffersen, M. L. (2011). Encrusting Sabellariidae (Annelida: Polychaeta) in rhodolith beds, with description of a new species of Sabellaria from Brazilian coast. Journal of the Marine Biological Association of the United Kingdom, 91, 425–438. https://doi.org/10.1017/S0025315410000780 

Schaeffer-Novelli, Y., Cintrón-Molero, G., Soaresc, M. L. G., & De-Rosa, T. (2000). Brazilian mangroves. Aquatic Ecosystem Health & Management, 3, 561–570. https://doi.org/10.1080/14634980008650693 

Sloan, N. A., & Bartier, P. M. (2009). Historic marine invertebrate species inventory: case study of a science baseline towards establishing a marine conservation area. Aquatic Conservation: Marine and Freshwater Ecosystems, 19, 827–837. https://doi.org/10.1002/aqc.1019 

SNUC (Sistema Nacional de Unidades de Conservação da Natureza). (2002). Lei Nº 9.985, de 18 de julho de 2000; Decreto Nº 4.340, de 22 de agosto de 2002. 2 ed. Brasília: Ministério do Meio Ambiente – MMA/SBF.

Soares, M. O., Teixeira, C. E. P., Bezerra, L. E. A., Paiva, S. V., Tavares, T. C. L., Garcia, T. M. et al. (2020). Oil spill in South Atlantic (Brazil): Environmental and governmental disaster. Marine Policy, 115, 103879. https://doi.org/10.1016/j.marpol.2020.103879 

Soares, M. O., Teixeira, C. E. P., Bezerra, L. E. A., Rossi, S., Tavares, T. C. L., & Cavalcante, R. M. (2020). Brazil oil spill response: Time for coordination. Science, 367, 155. https://doi.org/10.1126/science.aaz9993

Souza, A. S., & Furrier, M. (2015). Caracterização geomorfológica e ocupação antrópica de zonas costeiras: o caso da Ponta do Seixas, litoral da Paraíba, Brasil. Revista do Departamento de Geografia, 30, 166–178.

Souza Junior, J., Ponte, I., Coe, C. M., Farias, W. R. L., Feitosa, C. V., Hamel, J. F. et al. (2017). Sea cucumber fisheries in Northeast Brazil. SPC Beche-de-mer Information Bulletin, 37, 43–47.

Stöhr, S., O’Hara, T., & Thuy, B. (2020). World Ophiuroidea Database. Retrieved march 5th., 2020 from: http://www.marinespecies.org/ophiuroidea; https://doi.org/10.14284/358 

Thomas, L. P. (1973). Western Atlantic brittlestars of the genus Ophionereis. Bulletin of Marine Science, 23, 585–599.

Tommasi, L. R. (1965). Lista dos Crinoides recentes do Brasil. Contribuições do Instuto Oceanográfico da Universidade de São Paulo, 9, 1–33.

Tommasi, L. R. (1970). Os ofiuróides recentes do Brasil e de regiões vizinhas. Contribuições do Instuto Oceanográfico da Universidade de São Paulo, 20, 1–146.

Ventura, C. R. R., Borges, M., Campos, L. S., Costa-Lotufo, L. V., Freire, C. A., Hadel, V. F. et al. (2013). Echinoderms from Brazil: historical research and the current state of biodiversity knowledge. In J. J. Alvarado, & F. A. Solís-Marín (Eds.), Echinoderm research and diversity in Latin America (pp. 301–344). Berlin, Heidelberg: Springer. https://doi.org/10.1007/978-3-642-20051-9_9 

Ventura, C. R. R., Tiago, C. G., Cerqueira, W. R. P., & Borges, M. (2018). Echinodermata. In Instituto Chico Mendes de Conservação da Biodiversidade (Org.), Livro Vermelho da Fauna Brasileira Ameaçada de Extinção, V. 7, Invertebrados (pp. 26–48). Brasília: ICMBio.

Verrill, A. E. (1899). Report on the Ophiuroidea collected by the Bahama Expedition from the University of Iowa in 1893. Bulletin from the laboratories of natural history of the State University of Iowa, 5, 1–86. https://www.biodiversitylibrary.org/page/15418571#page/13/mode/1up 

Wood, H. L., Spicer, J. I., & Widdicombe, S. (2008). Ocean acidification may increase calcification rates, but at a cost. Proceedings of the Royal Society B: Biological Sciences, 275, 1767–1773. https://doi.org/10.1098/rspb.2008.0343 

WoRMS Editorial Board. (2020). World Register of Marine Species. Recuperado el 04 marzo, 2020 de: http://www.marinespecies.org

Young, P.S. (1986). Análise qualitativa e quantitativa da fauna associada a corais hermatípicos (Coelenterata, Scleractinia) nos recifes de João Pessoa, PB. Revista Brasiliera de Biologia, 46, 99–126.

Yuan, X., Shao, S., Yang, X., Yang, D., Xu, Q., Zong, H. et al. (2016). Bioenergetic trade-offs in the sea cucumber Apostichopus japonicus (Echinodermata: Holothuroidea) in response to CO2-driven ocean acidification. Environmental Science and Pollution Research, 23, 8453–8461. https://doi.org/10.1007/s11356-016-6071-0