Echinometra lucunter ( Linnaeus, 1758 )

Gondim, Anne Isabelley, Moura, Rafael Bendayan De, Christoffersen, Martin Lindsey & Dias, Thelma Lúcia Pereira, 2018, Taxonomic guide and historical review of echinoids (Echinodermata: Echinoidea) from northeastern Brazil, Zootaxa 4529 (1), pp. 1-72 : 19-21

Echinometra lucunter ( Linnaeus, 1758)

Figures 6 A–M, 18 C, 19 B

Echinus lucunter Linnaeus, 1758: 665 .

Echinometra sublangularis A. Agassiz, 1872: 72 –74.– Rathbun, 1879: 143.

Echinometra lucunter Gray, 1825: 427 .– Krau, 1950: 358.– Bernasconi, 1955: 62 –63, pl. 2, figs 1, 5.– Tommasi, 1957: 21, 29, figs 16, 20, pl. 1, fig. 1–2; 1959: 602, 603; 1966a: 16–17.– Brito, 1960b: 4, fig. 1e; 1962: 5; 1968: 21–22, pl. 10, figs 2–3; 1971: 263.– Lima-Verde, 1969: 10.– Tommasi & Aron, 1987: 3.– Castro et al., 1995: 476.– Alves & Cerqueira, 2000: 547.– Fernandes et al., 2002: 422.– Attrill et al., 2004: 154.– Magalhães et al., 2005: 63.– Netto et al., 2005: 214.– Martins & Martins de Queiroz, 2006: 209. – Ventura et al., 2007b: 279, tab.11.2, 280, fig. 11.1b, 290, anexo 11.1.– Gondim et al., 2008: 155; 2011: 81; 2014a: 99.– Oliveira et al., 2010: 10.– Xavier, 2010: 75.– Martins et al., 2012a: 55.– Miranda et al., 2012: 142, fig. 4c.– Ventura et al., 2014: 65, fig.– Martins et al., 2018: 529, figs 6–7.

Echinometra lucunter lucunter Hendler et al., 1995: 222 –225.

Material examined. Rio Grande do Norte: 4 spms, Ponta de Cajaúna, Tibau do Sul, 19.VIII.1982 [UFPB/ ECH.22]; 11 spms, Pipa Beach, Tibau do Sul, 19.VIII.1982 [UFPB/ECH.25]; 7 spms, Barra de Maxaramguape, Ceará-Mirim, 21.VIII.1982 [UFPB/ECH.26]; 4 spms, Cabo do Cabopari, Baía Formosa, 18.VIII.1982 [UFPB/ ECH.27]; 1 spm, Cabo de São Roque, 22.VIII.1982 [UFPB/ECH.1611]; 2 spms, Pirangi do Sul, Nísia Floresta, 22.VIII.1982 [UFPB/ECH.1642]; 3 spms, Zumbi Beach, Rio do Fogo, 3–6 m, 27.XI.2009 [MZUSP, without voucher]; 2 spms, 5°19,908′S 35°21,607′ W, Zumbi Beach, 27.XI.2009 [MZUSP, without voucher]. Paraíba: 2 spms, Ponta do Seixas, João Pessoa, 8.V.1977 [UFPB/ECH.01]; 3 spms, Cabo Branco Beach, João Pessoa, 12.V.1980 [UFPB/ECH.02]; 2 spms, Ponta do Seixas, João Pessoa, 12.II.1982 [UFPB/ECH.03]; 3 spms, Cabo Branco Beach, 03.VII.1985 [UFPB/ECH.21]; 5 spms, Cabo Branco Beach, 12.III.1981 [UFPB/ECH.351]; 1 spm, Ponta de Campina, Cabedelo, 24.VIII.2006 [UFPB/ECH.352]; 3 spms, Cabo Branco Beach, 04.XI.2006 [UFPB/ ECH.354]; 1 spm, Cabo Branco Beach, 09.IX.2006 [UFPB/ECH.355]; 1 spm, 6°55'S 34°47′W, 10 m, 03.VII.2006 [UFPB/ECH.573]; 1 spm, Cabo Branco Beach, 26.IX.2007 [UFPB/ECH.702]; 5 spms, Coqueirinho Beach, Conde, 27.X.2007 [UFPB/ECH.777]; 2 spms, Seixas Reef, 22.XII.2007 [UFPB/ECH.1018]; 4 spms, Baía da Traição Beach, 24.XI.2007 [UFPB/ECH.1020]; 1 spms, Barra de Camaratuba Beach, Mataraca, 23.I.2008 [UFPB/ ECH.1146]; 2 spms, Areia Vermelha Reef, Cabedelo, 22. II.2008 [UFPB/ECH.1148]; 2 spms, Baía da Traição Beach, 04.V.2008 [UFPB/ECH.1181]; 2 spms, Barra de Camaratuba Beach, Mataraca, 06.V.2008 [UFPB/ ECH.1182]; 3 spms, Areia Vermelha Reef, Cabedelo, 06.IV.2008 [UFPB/ECH.1212]; 1 spm, Cabo Branco Beach, 28.X.2007 [UFPB/ECH.1315]; 5 spms, Cabo Branco Beach, 16.XII.1997 [UFPB/ECH.1317]; 3 spms, Cabo Branco Beach, 25.X.2007 [UFPB/ECH.1319]; 2 spms, Cabo Branco Beach, 21.III.2000 [UFPB/ECH.1320]; 2 spms, Ponta do Seixas, 25.V.1998 UFPB/ECH.1322]; 4 spms, Cabo Branco Beach, 07.VI.2001 [UFPB/ ECH.1323]; 3 spms, Santa Catarina Beach, Cabedelo, 18.V.2007 [UFPB/ECH.1324]; 3 spms, Tambaba Beach, Conde, 28.IX.2007 [UFPB/ECH.1325]; 12 spms, Cabo Branco Beach, 0 9.III.2005 [UFPB/ECH.1326]; 1 spm., Cabo Branco Beach, 25.X.2007 [UFPB/ECH.1328]; 3 spms, Ponta do Seixas, João Pessoa, 03.XI.1982 [UFPB/ ECH.1329]; 2 spms, Cabo Branco Beach, 19.IX.2005 [UFPB/ECH.1331]; 3 spms, Cabo Branco Beach, 09.II.2001 [UFPB/ECH.1335]; 18 spms, Cabo Branco Beach, 01.XII.1975 [UFPB/ECH.1336]; 9 spms, Galé Reef, Pitimbú, 12.XII.2008 [UFPB/ECH.1455]; 2 spms, Barra de Mamanguape Reef, Rio Tinto, 10.I.2009 [UFPB/ECH.1456]; 2 spms, Areia Vermelha Reef, Cabedelo, 06.IV.2008 [UFPB/ECH.1472]; 3 spms, Cabo Branco Beach, 13.XI.2008 [UFPB/ECH.1473]; 1 spm, Pier de Cabedelo, Cabedelo, 05.V.2008 [UFPB/ECH.1476]; 5 spms, Seixas Reef, João Pessoa, 12.I.2009 [UFPB/ECH.1477]; 2 spms, Maceiozinho Beach, Jacumã, 06.V.2008 [UFPB/ECH.1482]; 2 spms, Tabatinga Beach, Conde, 10.II.2009 [UFPB/ECH.1512]; 3 spms, Coqueirinho Beach, Conde, 03.VI.2008 [UFPB/ECH.1513]; 1 spm, Tambaba, Beach Conde, 10.II.2009 [UFPB/ECH.1514]; 2 spms, Barra de Mamanguape Reef, Rio Tinto, 11.II.2009 [UFPB/ECH.1515]; 1 spm, Cabo Branco Beach, 03.XI.1982 [UFPB/ ECH.1649]; 1 spm, Pitimbú Reef, Pitimbú, 16.IX.2006 [UFPB/ECH.1656]; 2 spms, Pitimbú Reefs, Pitumbú, 16.IX.2005 [UFPB/ECH.1675]; 1 spm, Cabo Branco Beach, 16.III.2002 [UFPB/ECH.1701]; 1 spm, Cabo Branco Beach, 29.V.2009 [UFPB/ECH.1702]; 1 spm, Cabo Branco Beach, 09.IV.2005 [UFPB/ECH.1729]; 2 spms, Tambaba Beach, Conde, 04.VI.2008 [UFPB/ECH.1730]. Pernambuco: 13 spms, rocky shore between the Gabu Beach and Cabo de Santo Agostinho, 04.IX.1982 [UFPB/ECH.04]; 6 spms, Itarema Beach, Cabo, 03.IX.1982 [UFPB/ECH.05]; 6 spms, Ponta de Pedras, 30.X.1982 [UFPB/ECH.11]; 3 spms, Candeias Reef, Jaboatão, 02.XI.1982 [UFPB/ECH.12]; 1 spm, Piedade Reef, Jaboatão, 2.XI.1982 [UFPB/ECH.13]; 3 spms, Gabu Reef, Cabo, 03.IX.1982 [UFPB/ECH.29]; 1 spm, São José da Coroa Grande, 06.IX.1982 [UFPB/ECH.1316]; 5 spms, Pau Amarelo Reef, Paulista, 01.XI.1982 [UFPB/ECH.1327]; 1 spm, Catuama, Goiana, 31.X.1982 [UFPB/ ECH.1332]; 2 spms, Gamela Sirinhaén, 05.IX.1982 [UFPB/ECH.1659]; 1 spm, Ponta de Serrambi Beach, Ipojuca, 05.IX.1982 [UFPB/ECH.1670]. Alagoas: 1 spm, Pajuçara Beach, Maceió, 21.IX.1982 [UFPB/ECH.06]; 3 spms, Francês Beach, Marechal Deodoro, 19.X.1982 [UFPB/ECH.10]; 3 spms, Riacho Doce Beach, 31.I.1983 [UFPB/ ECH.16]; 3 spms, Ponta Verde Beach, Maceió, 20.X.1982 [UFPB/ECH.28]; 1 spm, Ponta Verde Beach, 31.I.1983 [UFPB/ECH.1330]; 1 spm, Paripueira Beach, 01.II.1983 [UFPB/ECH.1653]; 2 spms, Francês Beach, Marechal Deodoro, 29.I.1983 [UFPB/ECH.1655]; 1 spm, Pontal do Cururipe, Curuipe, 26.I.1983 [UFPB/ECH.1733]; 1 spm., Saco da Pedra Reef, Maceió, 10.II.2009 [UFSITAB-206]; 1 spm, Saco da Pedra Reef, 10.II.2009 [UFSITAB- 208]; 1 spm, Saco da Pedra Reef, 10.II.2009 [UFSITAB-250]. Bahia: 4 spms, Ponta da Coroa Vermelha, Santa Cruz da Cabrália, 15.X.1982 [UFPB/ECH.08]; 1 spm, Ponta Grande Reef, Porto Seguro, 15.X.1982 [UFPB/ ECH.09]; 2 spms, South of the Redonda Island, Abrolhos, 01.II.1982 [UFPB/ECH.15]; 5 spms, Ponta de Imbaçuaba, Cumuruxatiba, 13.X.1982 [UFPB/ECH.23]; 1 spm, reef between Cumuruxatiba and Ponta de Ibaçuaba, Prado, 28.IX.1982 [UFPB/ECH.30]; 4 spms, south-west of Siriba Islands, Abrolhos, 30.XI.1982 [UFPB/ ECH.31]; 4 spms, Imbaçuaba Beach, Prado, 14.X.1982 [UFPB/ECH.33]; 1 spm, Pituba Beach, Salvador, 17.IX.1982 [UFPB/ECH.1318]; 1 spm, Pitanga Beach, Lauro Freitas, 16.IX.1982 [UFPB/ECH.1333]; 1 spm, Coroa Beach, Itaparica, 18.IX.1982 [UFPB/ECH.1334]; 1 spm, Pituba Beach, Salvador, 17.IX.1982 [UFPB/ ECH.1634]; 1 spm, Penha Beach, Vera Cruz, Itaparica, 08.IX.1982 [UFPB/ECH.1654]; 3 spms, Arembepe Beach, Camaçari, 16.IX.1982 [UFPB/ECH.1658]; 1 spm, Itaparica Beach, 22.XII.1984 [UFPB/ECH.1674].

Description. Test elliptical, oral surface concave (TD = 5.8 to 129 mm; TH = 2.5 to 45.5 mm) ( Fig. 6A, B, I, J ). Apical system hemicyclic ( Fig. 6K ). Plates of periproct and apical system densely covered by small spines ( Fig. 6K ). Ocular and genital plates with many tubercles of various sizes ( Fig. 6K ). Ambulacral plate polygeminate (echinoid type), with six pairs of pores arranged in arc, one primary tubercle and few secondary tubercles ( Fig. 6L ). Interambulacral plate with one primary tubercle and many secondary tubercles ( Fig. 6M ). Primary and secondary tubercles of ambulacra and interambulacra non-crenulate and non-perforate ( Fig. 6I, L, M ). Primary spines of variable length, thick at base and thin at tip ( Fig. 6A ). Secondary spines thin and short. Peristome large, with few buccal plates densely covered by purple ophicephalous pedicellariae ( Fig. 6B ). Tube feet with C-shaped spicules and ossicles forming rosette in terminal discs ( Fig. 6G, H ). Spicules of tube feet often organized into longitudinal rows.

Pedicellariae. Globiferous, ophicephalous, tridentate and triphyllous pedicellariae present over entire test. Globiferous pedicellariae of various sizes, with a long stalk, without a neck, and with three pairs of well-developed venom glands, in which C-shaped spicules are found. Valves with lateral tooth paired or unpaired and a single end tooth ( Fig. 6C, D ). Ophicephalous pedicellariae with a long stalk and short neck. Valves with small marginal teeth that are serrate (like shark teeth) ( Fig. 6E ). Tridentate pedicellariae short, with stalk and neck long, in which Cshaped spicules similar to those of the tube feet are found. Valves narrow, long, with margins slightly serrate ( Fig. 6F ). Triphyllous pedicellariae with a long neck, about the same length as stalk. Valves short and broad, being narrower at the base and widening towards the tip.

Colour. Echinometra lucunter can be black, gray, green, red, or even bluish, displaying a high degree of colour polymorphism ( Lessios 1998). The spines are black but may have a greenish tinge at the base and a purple tinge at the apex. Naked test white.

Distribution. Mexico, Cuba, Belize, Guatemala, Honduras, Nicaragua, Jamaica, Haiti, Dominican Republic, Caribbean Sea, Costa Rica, Panama, Puerto Rico, Madagascar, Mozambique, Colombia, Venezuela, and Brazil (del Valle García et al. 2008; Alvarado et al. 2008; Kroh & Mooi 2016). In Brazil from CE, PB, PE, AL, BA, ES, RJ, SP, SC, including Abrolhos, Fernando, Fernando de Noronha, Trindade and Martin Vaz Islands ( Rathbun 1879; H.L. Clark 1925; Brito 1962, 1968; Tommasi 1966a; Lima-Verde 1969; Fernandes et al. 2002; Magalhães et al. 2005; Gondim et al. 2008, Lima & Fernandes 2009; Xavier 2010; Miranda et al. 2012; Martins et al. 2018). Herein we first record the species for the State of Rio Grande do Norte. The species is known to occur between 0 and 45 m ( Hendler et al. 1995), but it is almost exclusively a shallow-water species, restricted to less than 1 m of depth ( Lessios 1998).

Remarks. Presently eight species of Echinometra are known worldwide ( Bronstein & Loya 2013), two of which occur in the tropical part of the Western Atlantic [ E. lucunter and E. viridis A. Agassiz, 1863 ]. Only E. lucunter occurs along the Brazilian coastline. Echinometra lucunter differs from E. viridis in not having ambulacral plates with five pairs of pores and a reddish brown test with yellowish spines. In this study, we observed small morphological differences among adults and young individuals, such as the dicyclic apical system with few tubercles in young individuals and hemicyclic with many tubercles in adults. The length and thickness of spines were also quite variable, from long and thin to short, thick, and blunt. Apparently, these variations were not related to environment (low or high energy habitats) nor to developmental stage, but further studies are necessary to confirm this observation. Young specimens tend to have spines that are thin and long. Lewis & Storey (1984) observed that individuals living in high energy habitats tend to have thicker, smaller, and more flattened tests than specimens from low energy habitats.

Ecological notes. This species inhabits the intertidal and subtidal zones of reef environments but is common in the surf zone, where it lives inside crevices excavated by the action of their spines and teeth on the rock substrate ( Hendler et al. 1995) ( Fig. 19B ). According to Espinoza et al. (2008), this species can be also be found in sandy substrates and banks of seagrass (e.g., Thalassia testudinum K.D. Koenig, 1805 ). Echinometra lucunter is nocturnal and lives almost permanently inside of its burrow. Only a few individuals leave their burrows at night to feed. The species feeds primarily on drifting algae ( McPherson 1969), but may also prey on marine invertebrates such as sponges and cnidarians ( McClintock et al. 1982; McClanahan & Muthiga 2007). Echinometra is considered a "gardener" species, feeding on the algae that grow inside of its burrow, moving back and forth along the burrow to allow algae to regenerate as it feeds on new growth ( McClanahan & Muthiga 2007; Mooi, personal communication). Griinbaum et al. (1978) reported an agonistic behaviour in individuals of this species. During our field surveys, we observed some specimens of E. lucunter exhibiting "covering behaviour". Echinometra lucunter is the most common species in the intertidal zone of the NE coast of Brazil, forming high-density populations in these areas ( Fig. 19B ). Due to its habit of excavating rocks and forming dense populations, this species plays an important role in the bioerosion of reef environments ( Hendler et al. 1995) (Fig. 20B). Echinometra lucunter , as a specialized herbivore, also has an important role in the reef food web, where it acts in controlling macroalgal cover. It is also the most important prey of the gastropod Cassis tuberosa ( Linnaeus, 1758) throughout the Western Atlantic ( Dias et al. 2017). According to Martins et al. (2012a), E. lucunter was among the sea urchin species captured for the aquarium trade on the coast of Salvador (BA). In Cabo de Santo Agostinho (PE), there is a traditional event called "Festa da Ouriçada" (Sea Urchin Festival), which occurs every December 13 th since 1960, in devotion to Saint Luzia. Local fishermen capture sea urchins in large numbers to consume their gonads among local families ( Santos & Andrade 2013).

Figures

FIGURE 6. Morphological characters of Echinometra lucunter (UFPB/ECH.33, UFPB/ECH.1514). (A) Aboral view; (B) Oral view; (C–D) Valve of globiferous pedicellariae; (E) Valve of ophicephalous pedicellariae; (F) Valve of tridentate pedicellariae; (G) Tube foot ossicle; (H) Spicules of the tube feet; (I) Aboral view of naked test; (J) Oral view of naked test; (K) Apical system; (L) Ambulacral plates; (M) Interambulacral plates.

FIGURE 19. Ecological aspects of some echinoids from northeastern Brazil. (A) Eucidaris tribuloides parasitized by eulimid gastropod (arrow); (B) Partial view of coastal reef eroded by Echinometra lucunter; (C) Lytechinus variegatus on coral reef exhibiting covering behaviour at night; (D) Dead specimen of Lytechinus variegatus recently preyed upon (arrow) by juvenile Cassis tuberosa; (E) Dissodactylus crab associated with oral surface of sand dollar Encope emarginata on sandy beach; (F) Diseased specimen of Mellita aff. quinquiesperforata; (G) Dead sand dollars (M. aff. quinquiesperforata) on sandy beach after disease outbreak.