Eucidaris tribuloides ( Lamarck, 1816 )

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 : 10-11

Eucidaris tribuloides ( Lamarck, 1816)

Figures 3 A–M, 18 A, 19 A

Cidarites tribuloides Lamarck, 1816: 56 .

Cidaris tribuloides L. Agassiz & Desor, 1846: 326 .– Rathbun, 1879: 143.– L. Agassiz, 1835: 188.– Brito, 1962: 5; 1968: 17–18, pl. 8, fig. 1; 1971: 263.

Cidaris annulata Gray, 1855a: 37 .

Eucidaris tribuloides Döderlein, 1887: 42 .– Bernasconi, 1955: 52 –54, pl. 1, figs 1, 5.– Tommasi, 1958a: 2, 4, pl. 1, fig. 2; 1959: 602, 603; 1964: 83–84; 1966a: 6; 1972: 21, figs 30–33.– Brito, 1960b: 2, fig. 2e; 1971: 263.– Lima-Verde, 1969: 10.– Tommasi & Aron, 1987: 3; 1988: 2.– Alves & Cerqueira, 2000: 547.– Fernandes et al., 2002: 422.– Santos et al., 2002: 295 – 297.– Magalhães et al., 2005: 63.– Netto et al. 2005: 213.– Ventura et al., 2007b: 279, tab. 11.2, 289, app. 11.1.– Campos & Moura, 2008: 136, 139, fig. 2b.– Manso et al., 2008: 182, figs 3a–d.– Correia & Sovierzoski, 2009: 1087.– Xavier, 2010: 75.– Oliveira et al., 2010: 10, fig. 4a.– Martins et al., 2012a: 55.– Miranda et al., 2012: 142, fig. 4a.–Ventura, 2013: 104, fig. 119a,b.– Ventura et al., 2014: 65, fig.– Martins et al., 2018: 523, figs 1–3.

Cidaris minor Koehler, 1908: 302 –303, pl. 15, figs 136–138.

Eucidaris tribuloides africana Mortensen, 1909: 40 –43, pl. 6, figs 3, 13, pl. 10, fig. 4, pl. 13, fig. 17, pl. 14, figs 12–13, pl. 15, fig. 1, 15, 19, pl. 16, fig. 19.

Eucidaris clavata Mortensen, 1928: 408 –411, pl. 42, figs 1–4, pl. 47, figs 10–11, pl. 73, fig. 2, pl. 86, fig. 15.

Eucidaris tribuloides africana cf. attenuata A.M. Clark, 1955: 51, pl. 2.

Eucidaris tribuloides tribuloides Serafy, 1979: 15 .

Stylocidaris lineata Ventura, 2013: 105 , fig. 120a, b [not Stylocidaris lineata Mortensen, 1910 ].

Material examined. Paraíba: Project Algas—1 spm, 6°55′S 34°48′W, st. 58, 12 m, 04.II.1981 [UFPB/ECH.1362]; 4 spms, 7°10′S 34°38′W, st. 37, 25 m, 26.III.1981 [UFPB/ECH.1620]; 2 spms, 6°37′S 34°51′W, st. 80, 20 m, 02.VI.1981 [UFPB/ECH.1621]; 1 spm, 6°46′S 34°50′W, st. 68, 14 m, 19.V.1981 [UFPB/ECH.1624]; 2 spms, 7°12′5″S 34°36′W, st. 31, 26 m, 01. IV.1981 [UFPB/ECH.1626]; 1 spm, 7°21′S 34°38′W, st. 19, 16 m, 13.V.1981 [UFPB/ECH.1627]; 1 spm, 7°13′S 34°42′W, st. 33, 20m, 27.III.1981 [UFPB/ECH.1628]; 1 spm, 7°31′S 34°31′W, st. 5, 34 m, 29.I.1981 [UFPB/ECH.1636]; 7 spms, 7°34′S 34°45′W, st. 1, 11 m, 21.I.1981 [UFPB/ECH.1638]; 1 spm, 7°10′S 34°38′W, st. 37, 25 m [UFPB/ECH.1640]; 3 spms, 6°37′5″S 34°46′W, st. 78, 35 m, 29.V.1981 [UFPB/ ECH.1643]; 1 spm, 7°07′S 34°37′W, st. 38, 27 m, 25.III.1981 [UFPB/ECH.1727]; 6 spms, 6°55′S 34°46′05″W, st. 58, 12 m, 06.II.1981 [UFPB/ECH.1728]; 4 spms, 7°04′S 34°38′W, st. 45, 26 m, 17.II.1981 [UFPB/ECH.1734]; 8 spms, 6°26′S 34°52′W, st. 93, 26 m, 11.VI.1981 [UFPB/ECH.1735]; 3 spms, 7°31′S 34°42′W, st. 7, 16 m, 23.I.1981 [UFPB/ECH.1738]; 2 spms, 7°01′S 34°30′W, st. 47, 26 m, 13.II.1981 [UFPB/ECH.1739]; 9 spms, 7°15′05″S 34°36′W, st. 29, 28 m, 02. IV.1981 [UFPB/ECH.1755]; 3 spms, 7°12′5″S 34°39′W, st. 32, 20 m, 01. IV.1981 [UFPB/ECH.1756]; 1 spm, 6°50′S 34°47′W, st. 65, 18 m, 12.III.1981 [UFPB/ECH.1757]; 8 spms, 7°13′S 34°45′W, st. 34, 10 m, 27.III.1981 [UFPB/ECH.1758]; 2 spms, 6°50′S 34°50′W, st. 66, 10 m, 12.III.1981 [UFPB/ECH.1759]; 1 spm, 6°55′S 34°43′05″W, st. 56, 21 m, 11.II.1981 [UFPB/ECH.1761]; 2 spms, 7°34′S 34°42′W, st. 2, 20 m, 21. IV.1981 [UFPB/ECH.1762]; 1 spm, 7°10′S 34°45′W, st. 35, 10 m, 26.III.1981 [UFPB/ ECH.1763]; 1 spm, 7°34′S 34°36′W, st. 4, 33 m, 22.I.1981 [UFPB/ECH.1764]; 1 spm, 7°34′S 34°39′W, st. 3, 26 m, 22.I.1981 [UFPB/ECH.1765]; 3 spms, 6°57′S 34°38′W, st. 54, 30 m, 12.II.1981 [UFPB/ECH.1766]; 2 spms, 6°33′S 34°51′W, st. 85, 20 m, 04.VI.1981 [UFPB/ECH.1767]; 4 spms, 6°33′S 34°47′W, st. 86, 26 m, 04.VI.1981 [UFPB/ECH.1768]; 1 spm, 7°07′S 34°43′W, st. 40, 17 m, 19.III.1981 [UFPB/ECH.1769]; 2 spms, 6°55′S 34°40′W, st. 55, 28 m, 11.II.1981 [UFPB/ECH.1770]; 2 spms, 7°04′S 34°41′W, st. 44, 22 m, 16.II.1981 [UFPB/ECH.1771]; 2 spms, 7°15′5″S 34°33′W, st. 30, 35 m, 01. IV.1981 [UFPB/ECH.1777]; 1 spm, 7°01′S 34°30′W, st. 47, 26 m, 13.II.1981 [UFPB/ECH.1785]; 1 spm, 7°28′S 34°37′W, st. 11, 24 m, 05.V.1981 [UFPB/ECH.1786]; 1 spm, 6°52′S 34°42′W, st. 61, 20 m, 20.II.1981 [UFPB/ECH.1787]; 1 spm, 7°34′S 34°39′W, st. 3, 26 m, 22.I.1981 [UFPB/ ECH.1788]; 1 spm, 6°57′S 34°41′W, st. 53, 26 m, 12.II.1981 [UFPB/ECH.1789]; 1 spm, 6°43′S 34°45′W, st. 71, 22

m, 20.V.1981 [UFPB/ECH.1790]; 3 spms, 7°25′S 34°34′W, st. 15, 14 m, 07.V.1981 [UFPB/ECH.1810]; 1 spm, 7°21′9″S 34°31′W; Geomar XXIV, st. 97, 38 m , 30.V.1985 [UFPB/ECH.1821]. Pernambuco : 1 spm, Ponta de Serrambi, Ipojuca , 05.IX.1982 [UFPB/ECH.1820]; 1 spm, Fernando de Noronha Archipelago , 28.IV.2001 [UFPB/ ECH.1917]. Alagoas : 2 spms, Saco da Pedra Reef, Maceió , 10.II.2009 [UFSITAB-230]; 3 spms, Saco da Pedra Reef , 10.II.2009 [UFSITAB-230]; 1 spm, Francês Beach , Marechal Deodoro , 13.XI.1983 [UFPB/ECH.1337]; 15 spms, Francês Beach , Marechal Deodoro , 02.II.1983 [UFPB/ECH.1813]; 4 spms, Francês Beach , Marechal Deodoro , 19.II.2011 [UFPB/ECH.1902]. Bahia : 2 spms, Itapuã Beach, Salvador , 16.II.2007 [UFSITAB-75]; 15 spms, Itapuã Beach , 21.XII.1984 [UFPB/ECH.1736]; 2 spms, Itapuã Beach , 17.IX.1982 [UFPB/ECH.1737]; 2 spms, Pitanga Beach , Lauro de Freitas , 16.IX.1982 [UFPB/ECH.1814]; 1 spm, Ponta de Aratuba , Itaparica , 18.X.1982 [UFPB/ECH.1815]; 1 spm, Ponta da Coroa Vermelha , Santa Cruz de Cabrália , 15.X.1982 [UFPB/ ECH.1816]; 3 spms, Arembepe Beach , Camaçari , 16.IX.1982 [UFPB/ECH.1817]; 1 spm, Pituba Beach , Salvador , 17.IX.1982 [UFPB/ECH.1818].

Description. Test circular, slightly flattened both orally and aborally (TD = 3.3 to 45.4 mm; TH = 1.4 to 30.2 mm) ( Fig. 3 A–C, G, H). Apical system hemicyclic, uniformly tuberculate ( Fig. 3G, J ). Periproct pentagonal, covered by tuberculated plates that decrease in size towards the anus ( Fig. 3G, J ). Ambulacra narrow and slightly sinuous ( Fig. 3G, H, L ). Interambulacra wide, with clear vertical series of primary spines ( Fig. 3G, H, M ). Ambulacral plating simple ( Fig. 3L ). Interambulacral plates bearing single, perforate and non-crenulate primary tubercle, surrounded by many scrobicular tubercles ( Fig. 3M ). Primary spines thick and cylindrical ( Fig. 3 A–C), arranged into 10 vertical series, ending in crown of small projections. Secondary spines short and compressed. Oral-most primary spines often banded dirty white and light pinkish. Peristomial membrane densely covered by flat and imbricated small plates arranged in vertical parallel series ( Fig. 3K ). Tube foot spicules are rods with several blunt short spines and elongated flattened plates with perforations restricted to middle and one side ( Fig. 3E ).

Pedicellariae. Tridentate and globiferous pedicellariae spread over the whole test, the latter more numerous around the primary spines and peristome. Fistulate globiferous pedicellariae small, without a neck. Valve oval, with serrated margin, and denticulate foramen ( Fig. 3F ). Tridentate pedicellariae short, without a neck. Valve long, narrow, with denticulate margin ( Fig. 3D ).

Colour. Ground colour of the test is light brown to red-brown. The muscle bases of all secondary spines are brown to red-brown, spine are shafts dirty white, and the distal ends are lightly tinged with light brown ( Hendler et al. 1995). Naked test greenish, except for pore zones, which are white.

Distribution. North Carolina, Gulf of Mexico, Mexico, Guatemala, Belize, Cuba, Honduras, Jamaica, Nicaragua, Haiti, Dominican Republic, Costa Rica, Puerto Rico, Panama, Colombia, Venezuela, and Brazil ( Hendler et al. 1995; Alvarado et al. 2008; Solís-Marín et al. 2013; Kroh & Mooi 2016). In Brazil from PE, AL, BA, SP, RJ, and SC, including Abrolhos Archipelago, São Pedro and São Paulo Archipelago, Fernando de Noronha, Trindade and Martin Vaz Islands ( H.L. Clark 1907; Tommasi 1958a; Brito 1962; Lima-Verde 1969; Tommasi & Aron 1988; Fernandes et al. 2002; Magalhães et al. 2005; Netto et al. 2005; Manso et al. 2008; Correia & Sovierzoski 2009; Xavier 2010; Martins et al. 2018). This is the first record of this species for the coast of Paraíba. From 0 to 800 m, but most commonly in less than 50 m ( Hendler et al. 1995).

Remarks. The genus Eucidaris contains five living and three fossil species ( Kroh & Mooi 2016). In their phylogenetic study of the genus, Lessios et al. (1999) did not find differences between E. tribuloides from the west Atlantic and E. tribuloides africana , from Africa. Their results suggest that Atlantic Eucidaris belong to a single panmictic unit over the entire western Atlantic ( Lessios et al. 1999). No morphological differences were found among the specimens in the present study. However, Bernasconi (1955) observed some variations in the aspect of ambulacral and interambulacral areas and in the ocular plate/periproct ratio in specimens sampled from the Brazilian coast. The size and thickness of primary spines in E. tribuloides can vary with habitat ( Hendler et al. 1995). In high hydrodynamic environments, the spines tend to be short and thick, while in low energy environments they are longer and thin. However, this trend was not observed in the specimens examined, since they all had short and thick spines, apart from young individuals, which exhibited slightly longer and thinner spines.

Ecological notes. This species lives in small cavities in the reef habitat, under rocks and gravel in the backreef or in seagrass beds (del Valle García et al. 2005). Eucidaris tribuloides is omnivorous; its diet varies according to food availability in the environment ( Lawrence 1975; Machado et al. 2008). Pieces of algae and bryozoans, coral fragments, gastropod shells, echinoid spines, sponges, and seagrass have been recorded as food items ( Hendler et al. 1995). This species is common in the intertidal zone along the coasts of Alagoas and Bahia, while in the remaining northeastern states it seems to be more restricted to depths greater than 10 m. Few specimens were observed in reef crevices and among macroalgae in the coral reef formations of Tamandaré, State of Pernambuco. On the other hand, the species is abundant on the reefs of Praia do Francês (State of Alagoas), where it occurs on under rocks and co-occurs with crinoids, sponges, and other invertebrates. At this beach, we observed specimens hosting an ectoparasitic gastropod belonging to the family Eulimidae Philippi ( Fig. 19A ). Numerous specimens were reported by del Valle García et al. (2005) from strongly polluted areas such as “Playa del Chivo” and the coast adjacent to the river “Quibú”. Along the Brazilian littoral, specimens are being removed in large quantities, mainly to supply the demands of aquarium enthusiasts ( Machado et al. 2008). Martins et al. (2012a) evaluated echinoderm harvesting in Todos os Santos Bay (BA) for local aquarium trade and listed E. tribuloides as the eighth most collected species for this purpose.

Figures

FIGURE 3. Morphological characters of Eucidaris tribuloides (UFPB/ECH.1902). (A) Aboral view; (B) Oral view; (C) Lateral view; (D) Valve of tridentate pedicellariae; (E) Spicules of tube feet; (F) Valve of globiferous pedicellariae; (G) Aboral view of naked test; (H) Oral view of naked test; (I) Tube foot ossicle; (J) Detail of apical system; (K) Detail of peristome; (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.