New record of the Six-holed Keyhole Urchin , Leodia sexiesperforata ( Leske , 1778 ) ( Clypeasteroida , Mellitidae ) , from the Brazilian coast , with an updated distribution map

A new record of Leodia sexiesperforata is reported from the coast of Rio Grande do Norte state, northeastern Brazil. An updated distribution map based on data collected from literature, museums, and scientific collections is also presented. This new report fills a distribution gap on the coast of northeastern Brazil. Leodia sexiesperforata has a continuous range between the states of Ceará and Alagoas.


Introduction
The Six-holed Keyhole Urchin, Leodia sexiesperforata (Leske, 1778) (Clypeasteroida, Mellitidae), is an irregular Echinoidea with a wide distribution along the coast of the Americas, from eastern North America to Uruguay (Clark 1933, Mooi andPeterson 2000), with records from the United States of America, Mexico, Belize, Bahamas, Cuba, Puerto Rico, Barbados, Venezuela, and Brazil. Clark (1933) stated that this species occurs in Jamaica, Saint Kitts, Martinique, Saint Vincent, and Tobago.Herrera-Moreno and Bitencourt (2013) listed L. sexiesperforata as occurring in Honduras, Costa Rica, Dominican Republic, Panama, Colombia, and Uruguay.In Brazil, its distribution is widely known, but with some gaps, and has been recorded from the states of Ceará, Paraíba, Pernambuco, Alagoas, Bahia, Espírito Santo, and Rio de Janeiro (Rathbun 1879, Lima-Verde 1969, Alves and Cerqueira 2000, Ventura et al. 2006, Gondim et al. 2008, Miranda et al. 2012).
The Brazilian Northeastern Region extends for over 19 degrees in latitude (between 01°02′30″ N and 18°20′07″ S), comprising a coastline of approximately 3400 km, and holding a wide variety of coastal environments such as beaches, dunes, cliffs, estuaries, deltas, sandbanks, islands, and coral reefs, among oth-NOTES ON GEOGRAPHIC DISTRIBUTION ers (Pinheiro et al. 2008).In this region, pioneering work includes the publications of Verrill (1868), studying material collected in Abrolhos Archipelago, Bahia coast; Rathbun (1879), with collections conducted in several sites of the Brazilian coast including the northeastern region; and Lima-Verde (1969), with collections from Piauí (Parnaíba river mouth) to Alagoas (São Francisco river mouth).
Despite the above-mentioned papers, the knowledge of echinoderm biodiversity in Brazil remains sparse (Ventura et al. 2006), especially in the Northeastern Region (Miranda et al. 2012).Thus, the aim of this paper is to report the first record of L. sexiesperforata from the coast of Rio Grande do Norte and provide an updated distribution map based on literature and field samples.

Methods
Between June 2013 and February 2015 seasonal benthic biodiversity expeditions were conducted on the shallow continental shelf off the Porto do Mangue region of Rio Grande do Norte, northeastern Brazil (Fig. 1).The timing of the surveys was determined based on the historic rainfall data for Porto do Mangue municipality over a period of 10 years  provided by EMPARN (Empresa de Pesquisa Agropecuária do Rio Grande do Norte).Thus, the expeditions were scheduled for the dry (March-May and June-August) and rainy season (September-November and December-February).In each expedition, trawl fishing for biological collections was conducted at georeferenced sites (Fig. 2) by utilizing an artisanal trawl fishing boat.In addition, environmental data were collected, including depth (in meters), water transparency, temperature, salinity, dissolved oxygen, and pH from the water column bottom.The capture effort in each site had 20 min duration at an approximate speed of 2 knots, with a 4 mm mesh fishing net reaching the bottom.
The sand dollars were identified following what was introduced by Tommasi (1966) and Hendler et al. (1995).Later, the specimens were stored in 70% alcohol and deposited at the collection of Grupo de Estudos em Ecologia e Fisiologia de Animais Aquáticos (GEEFAA), with the voucher number GEEFAA/UFRN-361.
Collection data from this study (primary data) were compiled along with a bibliographic survey (secondary data) to prepare an updated distribution map of L. sex iesperforata.Geographic coordinate data were gathered information from 2 different sources.The first source was the reviewing of publications, lists of specimens, biodiversity surveys, and scientific reports (Table 1).The second source was the revision of deposited material in scientific collections of research institutes and museums accessible through the Global Biodiversity Information Facility (GBIF 2013).Records without precise taxonomy, invalid geographic coordinates, or missing information on the collection and the institutions to which they belonged were disregarded.Fossils were ignored as well, because they escaped the goal of this survey.Lastly, occurrences having no geographic coordinates but with satisfactory sampling location details had their location estimated using Google Earth Pro® software version 7.1.2.2041.
Facilities consulted using the GBIF directory were:  resulting tables were imported into QuantumMap 2.14.0 (QGIS Development Team 2016) software using the datum WGS84.Marine ecoregion delimitations, as proposed by Spalding et al. (2007), were added.These were obtained through the Marineregions.org(http://www.marineregions.org)online portal.Lastly, each occurrence of the species underwent a 1° buffer, and the final updated geographic distribution map of L. sexiesperforata was generated.5).Five short petals, similar in length (Fig. 4).Apical disk with 4 genital pores (Fig. 6).Six similar lunules, narrow and elongate, including 5 ambulacral lunules and 1 anal lunule (Figs 4,5).Peristome situated in middle of oral surface (Fig. 5).Periproct placed in the oral region between peristome and the anal lunule and positioned closer to peristome (Fig. 7).

Class
One specimen of L. sexiesperforata was captured at site IV and another at site V, both during the 2015 December-February expedition (sample in February) (Fig. 1).These specimens represent the first record of this species from the Rio Grande do Norte coast (Table 1).Both sample sites IV and V presented similar abiotic factors such as depth, salinity, dissolved oxygen, and pH.Water transparency and bottom temperature were equal at both sites (Secchi = 1.5 m, Temperature = 28.5 °C).Average depth at both sample sites was 3.5 m (Table 2).In addition, the region where both sites are located is mostly formed by predominantly sand sediments.

Discussion
The geographic distribution of L. sexiesperforata is situated entirely within 3 marine realms: Temperate Northern Atlantic, Tropical Atlantic, and Temperate South America (Fig. 3).The Temperate Northern Atlantic shows a predominance of records from the east coast of the United States, Carolinian Ecoregion.In the Tropical Atlantic, the data comes from 2 broad areas divided by an extensive gap.The first is in the Caribbean and along the southeastern coast of the United States (Tropical Northwestern Atlantic province), with the most number of occurrences of L. sexiesperforata.The second area extends from the Brazilian Northeast Region as far south as the Cabo Frio resurgence zone at the southern limit of the Tropical Southwestern Atlantic province, Rio de Janeiro; here information is sparse and there are multiple gaps in the known distribution of L. sexiesperforata.Between these 2 areas the North Brazilian Shelf province (from the state of Piauí to Venezuela) has no record of this species.Lastly, records of L. sexiesperforata are known from the Warm Temperate Southwestern Atlantic province, with a distribution gap between the Brazilian Southeast Region and Uruguay (Fig. 3).
The new record of L. sexiesperforata from Rio Grande do Norte fills the gap in the known distribution of the species.Therefore, the distribution of this species extends continuously along the Brazilian Northeast coast from Ceará to Alagoas.Recent studies, such as by Gondim et al. (2013) with material collected along the coast of Maranhão and Piauí and Oliveira et al. (2010), who includes few materials collected on the coast of Sergipe, have not reported the occurrence of L. sexiesperforata, but this might be due to a lack of sampling.
The distribution gaps of macrobenthic species on the northeast Brazilian coast may be due to the sparsity of surveys, although there has been an increase in recent records.This is particularly highlighted along the coast of Rio Grande do Norte state, where recent surveys for benthic biodiversity and accidental sampling has accounted for new records (Gondim et al. 2012, 2015a, 2015b, 2015c, Manso et al. 2014, Moraes et al. 2015) and ecological interactions (Alencar et al. 2014).Thus, continuous benthic biodiversity surveys along the Brazilian northeast coast is paramount for a better understanding of the geographic distribution of L. sexiesperforata.
It is known that Echinodermata have a fundamental role in marine environments (Benitez-Villalobos 2001), occupying several trophic levels in the food chain (herbivore, carnivore, detritophage, and omnivore), regulating the density of species, participating in the recycling of nutrients, bioerosive processes, and even in the epibiosis with other animals and plants (Caso 1978, Hadel et al. 1999, Ventura et al. 2006).Therefore, new records, such as those presented hereby, not only contribute to a better knowledge of the fauna but also aid in evolutionary and marine conservation studies.

Table 2 .
Abiotic factors in each sample point where Leodia sexiesperforata was captured.CLT = current local time, Dep = depth, Secchi = water transparency, T = bottom temperature of the water column, Sal = bottom salinity of the water column, DO = dissolved oxygen.
(Lavrado and Ignacio 2006)ore(Lavrado and Ignacio 2006), and National Museum of Natural History, Smithsonian Institution (NMNH DwC-Archive, information provided with the permission of the NMNH).All obtained data (primary and secondary) were compiled and added to a geospatial database, and the 1 Original geographic coordinates (other coordinates were estimated, see Methods for further information). 2Apud Francisco and Pauls (2008).* Locality and geographic coordinates not avaliable.** Geographic coordinate not avaliable.NA: Not avaliable.

Table 1 .
Leodia sexiesperforata occurrences from literature data.Present study highlighted in bold.