Echinoderms from Santa Catarina, southern Brazil: an update on biodiversity and distribution

1 Universidade Federal do Rio de Janeiro (UFRJ), Museu Nacional (MN), Programa de Pós-Graduação em Zoologia. Rio de Janeiro, RJ, Brasil. ORCID: https://orcid.org/0000-0001-6109-5697. E-mail: nataly.slivak@gmail.com (corresponding author) 2 Universidade Federal de Santa Catarina (UFSC), Departamento de Ecologia e Zoologia (ECZ). Florianópolis, SC, Brasil. ORCID: https://orcid.org/0000-0003-3288-0885. E-mail: alberto.lindner@ufsc.br 3 Universidade Federal do Rio Grande do Sul (UFRGS), Instituto de Biociências (IBIO), Departamento de Zoologia. Porto Alegre, RS, Brasil. ORCID: https://orcid.org/0000-0001-8342-4607. E-mail: hpromano@ufrgs.br


INTRODUCTION
There are about 7,000 echinoderm species worldwide, of which 347 have been reported in Brazil (Ventura et al., 2006. The group is represented by sea stars (Asteroidea), sea urchins (Echinoidea), sea cucumbers (Holothuroidea), sea lilies and feather stars (Crinoidea), and brittle stars (Ophiuroidea). Echinoderms, such as starfishes and sea urchins, are important predators and herders that play key roles in the functioning of shallow-water marine ecosystems (Paine, 1966;Lessios, 1988;Birkeland, 1989). Over the years, echinoderms became targets of anthropic action. Sea urchins and sea cucumbers, for instance, are commercially popular in several regions for human consumption and supposed medicinal properties (Pangestuti & Arifin, 2017). In Brazil, these organisms are also collected and sold as a decorative artifact, such as the starfish Oreaster reticulatus (Linnaeus, 1758) Martins et al., 2012c;Alves et al., 2018), currently in vulnerable status in the endangered species book (ICMBio, 2018).
The history of studies on echinoderms in Brazil goes back to the first report of echinoderms in 1648 (see Marcgrave, 1942;Ventura et al., 2013). The following records were those of Verrill (1868), Rathbun (1879), Ludwig (1882), and those from the southern coast of Brazil by Müller (1898) (Tiago, 1998;Hadel et al., 1999;

RESULTS
The echinoderm species search resulted in 444 records for the state of Santa Catarina. One hundred and fifty one records are in scientific manuscripts, 90 in master thesis, PhD thesis and undergraduate thesis, 45 in conference proceedings, 41 in endangered species lists, 27 in book chapters and 16 in technical reports (see Appendix 1). The scientific databases OBIS, GBIF and SpeciesLink resulted in 60 records and 14 in zoological collections from foreigner institutions (see Appendix 2).
In total, the search revealed 66 echinoderms taxa: 61 species, three subspecies and two genera (without specific classification). All of them were classified in five classes and 36 families ( Table 1).
The largest number of recorded specimens belongs to the Class Ophiuroidea (33 species), followed by Asteroidea (12 species and three subspecies) and Echinoidea (12 species and two genera), Holothuroidea (two species) and Crinoidea (two species).
One echinoderm species not previously reported in the literature for the coast of Santa Catarina is reported herein: Ophiacantha pentacrinus Lütken, 1869.
The specimens were identified by Dr. Michella Borges, specialist and curator of the Echinoderms Collection from the Museum of Zoology of the University of Campinas (Museu de Zoologia da Universidade Estadual de Campinas -ZUEC). The specimens were labeled as ZUEC-OPH 1868; ZUEC-OPH 1871 and ZUEC-OPH 1872 (see Appendix 2). The previous southernmost record was the state of Paraná (Borges et al., 2015), in this study we extend it to the Santa Catarina coast.
Sixteen echinoderm species listed are present in the endangered species list of Santa Catarina (IMA, 2011), and seven of them are in the Brazilian Red List (ICMBio, 2018).

Echinoderm distribution along Santa Catarina coast
Of the 134 sites where echinoderm species were recorded (Fig. 2), the shallow continental shelf and the Arvoredo area concentrated the highest number of species. The continental shelf of Santa Catarina was mainly explored by the ReviZEE program (Living Resources in the Exclusive Economic Zone). The program provided the discovery of new marine species for Brazil, especially those inconspicuous and difficult to be sampled, such as ophiuroids (Borges et al., 2002. In this study, we observed that most of the ophiuroids registered for Santa Catarina came from the ReviZEE program (45%). Due to mobility, diversity of eating habits and small size, ophiuroids are able to explore habitats often unattainable by other echinoderms (Hyman, 1955;Bueno et al., 2018).
Part of Arvoredo Island is within the Arvoredo Marine Biological Reserve, a conservation unit that also includes Galé and Deserta Island, and Calhau de São Pedro . The echinoderm records reported herein are mainly from the north and center-north coast of Santa Catarina (26 species), where the Arvoredo Marine Reserve is located. Rocky shores and coastal islands characterize this coastal region, environments suitable for several echinoderm species. In addition, most marine research institutions are located in the center-north region of Santa Catarina, and thus may contribute to the largest sample effort in this area. In contrast, the results revealed a lower number of echinoderm records in the southern region of Santa Catarina. Sandy beaches and dunes characterize the southern coast of Santa Catarina, where marine and wind processes predominate. The echinoderm species reported in the literature for the southern coastal region were the epibenthic sea biscuits, Encope emarginata and Melitta quinquiesperforata (Tavares, 1996;Brustolin, 2013).
These animals live under sandy and/or muddy substrate and require different sampling techniques, such as fishing nets and trawls. The lower number of echinoderms recorded between 27°50′S and 29°20′S latitudes can indicate that the echinoderm diversity presented in this study may be underestimated due to the absence of further studies and/or appropriate sampling methods.
Ophiuroidea was the most representative class, with 33 species recorded (50%). Some authors also observed similar results for the northeast region of Brazil, such as 50% ophiuroid records in Bahia state (Alves & Cerqueira, 2000;Magalhães et al., 2005), 40% in Paraíba (Gondim et al., 2008) and 42% in Pernambuco (Lima & Fernandes, 2009). In Paraná state, southern Brazil, ophiuroid diversity (34 species) was similar to this study, comprising 55% of the echinoderm fauna (Bueno et al., 2018). Ophiuroidea representativeness is a pattern on the Brazilian coast, comprising 153 extant species (43.7% of 347 species of echinoderms) (Ventura et al., 2013). Asteroidea and Echinoidea were the second and third most representative classes at Santa Catarina (22.7% each) followed by Holothuroidea and Crinoidea (2.6% each). The starfish Asterina stellifera and Echinaster (Othilia) brasiliensis occurred in at least 29 coastal sites, and the sea urchin Echinometra lucunter and Arbacia lixula, in 25 and 21, respectively (Table 1). Our results also reveal that Santa Catarina is the southernmost record for 40 species, that is, about 60% of the species recorded (Table 1; see Geographic Range column). In addition, 12 of the recorded species listed in this study (17%) are endemic to the Brazillian coast, such as two ophiuroid species recently described, Ophiothrix tommasii Santana, Manso, Almeida &Alves, 2020 andOphiothrix troscheli Santana, Manso, Almeida &Alves, 2020. New species recorded recently (Santana et al., 2020) and new occurrences Lopes et al., 2017) show that there is still much to learn about the echinoderm fauna of Santa Catarina.
Two echinoderm genera, in the present study, are not identified at the species level, the equinoids Astroypga and Pseudoboletia. The genus Astropyga is recorded for Brazil as Astropyga nuptialis, described for the state of São Paulo (Tommasi, 1958), and as Astropyga magnifica A.H. Clark, 1934 for Santa Catarina and Pernambuco Slivak, N.N. et al.: Echinoderms from Santa Catarina Pap. Avulsos Zool., 2022;v.62: e202262004 13/25 (Oliveira et al., 1987;Lima & Fernandes, 2009). Oliveira et al. (1987) recorded A. magnifica for Deserta Island (Arvoredo Marine Reserve) at 12 m depth. Recently, echinoderm researcher Cesar Cordeiro identified this genus at Arvoredo Island (ReBio Arvoredo) (Photo: iNaturalist -61249405). However, as we did not have access to this material, we chose to keep it at genus level, and we suggest a taxonomic study to identify which of the two Astropyga species occur in Santa Catarina. Lopes et al. (2017) recorded the genus Pseudoboletia sp. at Deserta Island, Santa Catarina and Cabo Frio Island, Rio de Janeiro. The molecular results differentiated three species of this genus, two from the Indo-Pacific (P. indiana and P. maculata) and one from the Atlantic (Pseudoboletia sp. from São Tome and Brazil). Martins et al. (2018) referred the specimens from the Trindade Island, as P. maculata, whose morphological characteristics are the same as those of P. maculata from the Indo-Pacific, but different from those recorded by Lopes et al. (2017) in Rio de Janeiro and Santa Catarina.
In this study, we adopted a method of taxonomic reliability (see "Record Type" in Table 1). Direct access to the documented literature material is not always possible, but it is important to validate this information. Although we included data from unpublished studies, these species records were included herein when also presenting photographs of the reported species. Most studies are specific publications on echinoderms (about 90%), carried out by experts in the group. We emphasize the importance of this literature for this checklist and for future studies on local biodiversity and ecology.
During this work, one ophiuroid species was reported for the first time in Santa Catarina, Ophiacantha pentacrinus. This specimen was identified by Dr. Michela Borges, ophiuroids specialist, and deposited in the Museu de Zoologia da UNICAMP (Coleção de Ophiuroidea) (UNICAMP Museum of Zoology (Collection of Ophiuroidea)), but was not previously reported in the literature. The species Ophiacantha cosmica and Ophiacantha pentacrinus have long been confused, taxonomically. Species identified as O. cosmica may actually be of this species or an O. pentacrinus (Tommasi, 1999). Even today, echinoderm specialists work with these two species in order to guarantee the correct identification. In addition to being a new record of this species in Brazil, Santa Catarina is the southernmost location for the distribution of O. pentacrinus.

Habitat distribution
Echinoderms inhabit all types of marine substrate . Most species of ophiuroids are bottom dwellers on the sea floor, buried in mud or hidden in crevices and holes in rock or coral (Stöhr et al., 2008(Stöhr et al., , 2012. In Santa Catarina, we observed that some ophiuroid species are epizoic, such as Ophiactis savignyi, which colonizes other ophiuroids species, and Astrocyclus caecilia, which was observed on Ellisella elongata (Pallas, 1766), a gorgonian species (Oliveira, 1989;Stöhr et al., 2012). Starfishes occur in unconsolidated (sandy, muddy) and consolidated (rocks) substrates. All starfish species recorded in this work occur in soft botton. The species of the families Astropectinidae and Luidiidae are infaunal, that is, they spend most of their time under the substrate, such as Astropecten brasiliensis and Luidia senegalensis (Clark & Downey, 1992). However, Echinaster (Othilia) brasiliensis, for example, lives on rocks, rhodolites and shells, as they are mainly sponge-eating animals (Fergunson, 1969).
Crinoids occur in all oceans and ranging from coastal to abyssal depths, such as Tropiometra carinata, a common species on the Brazilian coast (MacCord & Duarte, 2002;Souto & Martins, 2017). This species was usually observed by the first and second authors as attached to the lateral surface of rocks, such as illustrated by Ventura et al. (2016). Democrinus conifer was collected on the outer continental shelf, in Santa Catarina, through the Living Resources Program in the Exclusive Economic Zone (ReviZEE), Score Sul/Bentos (Tommasi, 2004). This species has been recorded for Rio de Janeiro, São Paulo and Paraná (Bueno et al., 2018), however little information about this species in Brazilian waters is available.
Two holothurians species are present in this study, Holothuria (Halodeima) grisea and Isostichopus badionotus. Mendes et al. (2006) reported Holothuria (Halodeima) grisea in Armação do Itapocoroy Bay with a clumped distribution on rocky bottoms, however in sandy bottom areas, there was a high frequency of isolated specimens (not clumped). This seems to be a pattern along the Brazilian coast (Alves & Cerqueira, 2000;Miranda et al., 2012;Alitto et al., 2016;Leite-Castro et al., 2016). Isostichopus badionotus is an epibenthic holothurian widely distributed on shallow muddy, sandy and seagrass bed, but can also be found in coral reefs (Zacarías-Soto et al., 2013). In Santa Catarina, this species was observed in Arvoredo Island on sandy substrate, with different color patterns. There is little information about this species in Brazilian waters.

Threatened species
In this study, 16 threatened species were recorded (21% of total) (IMA, 2011). Of the 16 starfish species recorded, six are on the endangered national fauna list (ICMBio, 2018). According to Ventura et al. (2013), accidental capture by shrimp trawlers is one of the main threats to echinoderms, especially for asteroids that live in sandy and muddy bottoms, such as Astropecten brasiliensis, Astropecten cingulatus, Luidia clathrata and Luidia senegalensis. In Santa Catarina, Branco et al. (2015) recorded 11 echinoderms species as bycatch in artisanal fishing for the seabob shrimp Xiphopenaeus kroyeri (Heller, 1862), that is, 68.75% of the total threatened echinoderm species in the Santa Catarina coast. In this context, knowledge about factors that affect the structure of communities in the areas in which trawling fisheries operate can be an important tool for the correct and sustainable management of fisheries (Barrilli, 2018).
Other potential threats to echinoderms in Santa Catarina are aquarium trade and commercial fishing for souvenirs and decorative items that affect starfishes such as Oreaster reticulatus and Asterina stellifera, which are captured and marketed to tourists (Ventura et al., 2013;Branco et al., 2015;Souto & Martins, 2017). In addition, although the echinoderm exploration for food purpose in Brazil is still small, the echinoid Echinometra lucunter  Slivak, N.N. et al.: Echinoderms from Santa Catarina Pap. Avulsos Zool., 2022;v.62: e202262004 15/25 is already marketed as a delicacy and there is evidence of illegal exploitation of the holothuroids Isostichopus badionotus and Holothuria (H.) grisea in Brazil (Souto & Martins, 2017). Besides that, echinoderms, such as those recorded in the North and South Bays of Santa Catarina directly associated with the bottom, can be susceptible to contaminants stored in marine sediment caused by the progressive occupation and environmental degradation in favor of urban expansion (Moreira, 2011). Therefore, studies on reproductive biology, population dynamics and genetics are needed. To achieve this knowledge, it is essential to protect these species. Currently, the Institute of the Environment of Santa Catarina (Instituto do Meio Ambiente de Santa Catarina, IMA), works with environmental protection programs in Hydrographic Basins and Federal Marine-Coastal Conservation Units, such as the Arvoredo Biological Marine Reserve (Reserva Biológica Marinha do Arvoredo), which shelter most echinoderm species listed in this study (IMA, 2011).

CONCLUSION
Considering the great length of the Brazilian's coastline, information on the occurrence and distribution of extant echinoderms species seems to be insufficient. Regional biodiversity inventories are the first step in understanding coastal ecological processes even at ocean scales. The remarkable number of new records, in recent years, of Echinodermata fauna listed in this study for Santa Catarina, reveals the lack of taxonomic studies. Updated checklists, as presented herein, may help monitor anthropic impacts, foster conservation strategies and generate subsidies for future studies of taxonomy, ecology and related fields.