Lytechinus variegatus ( 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 : 24-25

Lytechinus variegatus ( Lamarck, 1816)

Figures 7 A–O, 18 D, 19 C–D

Cidaris variegata Leske, 1778: 85 .

Echinus variegatus Lamarck, 1816: 48 .

Psammechinus variegatus L. Agassiz & Desor, 1846: 368 .

Toxopneustes variegatus A. Agassiz, 1872: 168 .― Rathbun, 1879: 144.

Lytechinus variegatus A. Agassiz, 1863: 24 .― H.L. Clark, 1925: 120 –121.― Krau, 1950: 358.– Bernasconi, 1955: 60 –61, pl. 2, figs 2, 6.– Tommasi, 1957: 21, 25, 26, figs 12–15; pl. 1, fig. 5; 1964: 92; 1966a: 14–15; 1966b: 254–256; 1967: 50; 1972: 26, figs 51–52.― Brito, 1960b: 3, pl. 1a, 2c, f; 1962: 5; 1968: 23, pl. 10, fig. 4.― Lima-Verde, 1968: 155; 1969: 10.― Tommasi & Aron, 1987: 3; 1988: 2.― Manso, 1989: 357.― Castro et al., 1995: 476.― Magalhães et al., 2005: 63.– Martins & Martins de Queiroz, 2006: 208.– Ventura et al., 2007a: 251; 2007b: 279, tab. 11.2, 280, fig. 11.1a, 290, anexo 11.1; 2014: 65, with one figure.– Gondim et al., 2008: 155; 2014a: 99.– Manso et al., 2008: 183, figs 4a–b.– Xavier, 2010: 75.– Miranda et al., 2012: 142, fig. 4d.– Alitto et al., 2016: 10.

Lytechinus variegatus atlanticus H.L. Clark, 1942: 380 .

Litechinus variegatus Alves & Cerqueira, 2000 . 547.

Lytechinus variegatus variegatus Tommasi, 1959: 602 , 603.― Fernandes et al., 2002: 422.― Oliveira et al., 2010: 11, fig. 4c.

Material examined. Paraíba: 1 spm, Cabo Branco Beach, João Pessoa, 25.IX.2007 [UFPB/ECH.1158]; 1 spm, Cabo Branco Beach, 21.III.2000 [UFPB/ECH.1321]; 1 spm, Cabo Branco Beach, 20.XI.1980 [UFPB/ECH.1364]; 1 spm, Galé Reef, Pitimbú, 12.XII.2008 [UFPB/ECH.1461]; 2 spms, Cabo Branco Beach, 29.V.2009 [UFPB/ ECH.1552]; 1 spm, 7°07′00″S 34°43′54″W, 14.III.2006 [UFPB/ECH.1718]; 1 spm, Bessa Beach, João Pessoa, 20.VIII.2005 [UFPB/ECH.1719]; 1 spm, 6°55′S 34°47′W, 03.VII.2006, 10 m [UFPB/ECH.574]; 1 spm, Ponta do Seixas, João Pessoa, 12. IV.2006 [UFPB/ECH.1811]; Project Algas—5 spms, 6°50′S 34°50′W, st. 66, 10 m 12.III.1981 [UFPB/ECH.1363]; 1 spm, 6°46′S 34°53′W, st. 67, 10 m, 13.III.1981 [UFPB/ECH.1631]; 2 spms, 7°10′S 34°38′W, st. 37, 35 m, 26.III.1981 [UFPB/ECH.1639]; 3 spms, 7°01′S 34°41′W, st. 49, 16 m, 06.II.1981 [UFPB/ECH.1644]; 1 spm, 7°01′S 34°47′05″W, st. 50, 11 m, 05.II.1981 [UFPB/ECH.1703]; 1 spm, 7°01′S 34°41′05″W, st. 48, 24 m, 13.II.1981 [UFPB/ECH.1704]; 1 spm, 7°28′S 34°40′W, st. 10, 14 m, 05.V.1981 [UFPB/ ECH.1705]; 5 spms, 6°29′S 34°57′W, st. 90, 12 m, 10.VI.1981 [UFPB/ECH.1706]; 4 spms, 6°33′S 34°57′W, st. 83, 12 m, 03.VI.1981 [UFPB/ECH.1707]; 3 spms, 7°10′S 34°38′W, st. 37, 25 m, 26.III.1981 [UFPB/ECH.1708]; 1 spm, 6°55′S 34°46′05″W, st. 57, 18 m, 06.II.1981 [UFPB/ECH.1709]; 1 spm, 7°10′S 34°45′W, st. 35, 10 m, 26.III.1981 [UFPB/ECH.1710]; 1 spm, 7°15′05″S 34°42′W, st. 27, 16 m, 13. IV.1981 [UFPB/ECH.1711]; 2 spms, 6°55′S 34°48′W, st. 58, 12 m, 04.II.1981 [UFPB/ECH.1712]; 1 spm, 6°58′S 34°46′05″W, st. 51, 14 m, 05.II.1981 [UFPB/ECH.1713]; 2 spms, 7°34′S 34°42′W, st. 2, 20 m, 21. IV.1981 [UFPB/ECH.1714]; 1 spm, 7°13′S 34°42′W, st. 33, 20 m, 27.III.1981 [UFPB/ECH.1715]; 1 spm, 6°36′S 34°43′W, st. 79, 22 m, 29.V.1981 [UFPB/ECH.1717]; 1 spm, 6°50′S 34°50′W, st. 66, 10 m, 12.III.1981 [UFPB/ECH.1760]; 1 spm, 6°52′S 34°48′W, st. 59, 10 m, 04.II.1981 [UFPB/ECH.1776]; 1 spm, 7°13′S 34°42′W, st. 33, 20 m, 27.III.1981 [UFPB/ECH.1812]. Pernambuco: 4 spms, Itaparica Island, V.1980 [UFPB/ECH.24]. Alagoas: 3 spms, Paripueira Beach, 01.II.1983 [UFPB/ECH.17]; 1 spm, Mangue Beach, 03.II.1983 [UFPB/ECH.18]; 3 spms, Ponta Verde Reef, Maceió, 26.VI.2007 [UFSITAB- 78]. Bahia: 7 spms, Ponta da Coroa Vermelha, Santa Cruz da Cabrália, 15.X.1982 [UFPB/ECH.07]; 4 spms, coral reef between Cumuruxatiba and Imbaçuaba Beach, Prado, 28.XI.1982 [UFPB/ECH.14]; 2 spms, Itaparica Beach, Salvador, 22.XII.1984 [UFPB/ECH.19]; 4 spms, Coroa Vermelha, Santa Cruz da Cabrália, 20.XII.1984 [UFPB/ ECH.20]; 3 spms, Imbaçuaba, Prado, 14.X.1982 [UFPB/ECH.32]; 4 spms, Cabuçu Beach, Santo Amaro, 19.IX.1982 [UFPB/ECH.1720]; 1 spm, Itaparica Beach, Salvador, 22.XII.1984 [UFPB/ECH.1721]; 3 spms, Maré Island, Salvador, 01.II.2002 [UFSITAB-119]; 1 spm, Santa Cruz da Cabrália, 6–7 m [MZUSP, without voucher].

Description. Test hemispherical, slightly pentagonal with flat oral side (TD = 4.4 to 81.7 mm; TH = 1.8 to 38.6 mm) ( Fig. 7A, B, I, J ). Apical system hemicyclic, ocular plates I and V insert ( Fig. 7L ). Genital plates with two or three tubercles ( Fig. 7L ). Ocular plates with five to eight small tubercles ( Fig. 7L ). Ambulacra broad at ambitus, almost as broad as interambulacra ( Fig. 7I, J ). Ambulacral plate trigeminate (echinoid type), with one primary tubercle and three pairs of pores arranged in vertical row ( Fig. 7N ). Interambulacral plate with one to five primary

tubercles ( Fig. 7O ); number of tubercles tend to increase toward oral region. Primary spines short, with tapering tips, and arranged into clear vertical rows in ambulacra and interambulacra. Secondary spines smaller and narrower than primary spines. Tubercles non-crenulate and non-perforate ( Fig. 7I, J, N, O ). Peristomial membrane densely covered by peristomial plates ( Fig. 7N ), with many ophicephalous and triphyllous pedicellariae.

Pedicellariae. Globiferous pedicellariae with a long stalk, without a neck, and with many C-shaped and dumbbell-shaped spicules. Valves long, with a long end tooth ( Fig. 7C, D ). White ophicephalous pedicellariae over entire test ( Fig. 7A ). Ophicephalous pedicellariae with long stalk and neck, with a small number of C-shaped and dumbbell-shaped spicules ( Fig. 7H ). Valves short, oval, with margin denticulate and slightly serrate ( Fig. 7E ). Tridentate pedicellariae short, with a long neck and C-shaped and dumbbell-shaped spicules. Valves long and narrow, with margin slightly denticulate, these teeth being short, the longest occurring near base of the blade ( Fig. 7E ). Triphyllous pedicellariae with large C-shaped spicules ( Fig. 7H ) and short, broad, perforated blade, perforations on external margin longer and narrower ( Fig. 7G ).

Colour. Corona greenish, with white ambulacra and spines with purplish tips ( Fig. 7A, B ). Globiferous pedicellariae large, white, visible to the naked eye ( Fig. 7A ). Test and spines colour variable and used to identify subspecies of L. variegatus ( Serafy 1973) . Hendler et al. (1995) indicated that colour of the test and spines may vary within a single population. We did not observe this variation on populations from the NE Brazil.

Distribution. Mexico, Gulf of Mexico, Cuba, Jamaica, Haiti, Belize, Guatemala, Honduras, Dominican Republic, Puerto Rico, Caribbean Sea, Costa Rica, Panama, Colombia, Venezuela, and Brazil ( Alvarado et al. 2008; del Valle García et al. 2008; Kroh & Mooi 2016). In Brazil, from CE, PB, PE, AL, BA, RJ, SP, SC, RS, including Abrolhos and Fernando de Noronha Islands ( Rathbun 1879; H.L. Clark 1925; Tommasi 1966a, 1972; Brito 1968; Lima-Verde 1969; Tommasi & Aron 1988; Manso 1989; Fernandes et al. 2002; Magalhães et al. 2005; Netto et al. 2005; Gondim et al. 2008; Lima & Fernandes 2009; Oliveira et al. 2010; Xavier 2010). Herein we establish a new record of L. variegatus for the State of Rio Grande do Norte. The species occurs from 0 to 250 m, being more common above depths of 50 m ( Hendler et al. 1995).

Remarks. Lytechinus is currently known from three fossil and eight living species, four of which come from the tropical West Atlantic ( L. variegatus ; L. callipeplus H.L. Clark, 1912 ; L. euerces H.L. Clark, 1912 ; and L. williamsi Chesher, 1968 ). Only L. variegatus and the subspecies L. variegatus carolinus A. Agassiz, 1863 are known from Brazilian waters. Lytechinus variegatus differs from L. callipeplus by having tridentate and triphyllous pedicellariae and by its peristomial membrane, which is covered by whitish plates. Lytechinus euerces differs from L. variegatus by having test and spines white, and short primary spines. Lytechinus williamsi differs from L. variegatus by having a beige test and large, purple globiferous pedicellariae. Mortensen (1943a) separated L. variegatus into allopatric subspecies. Tommasi (1966a) provided a taxonomic key for these subspecies and considered the peristomial membrane, spines, and test colour important characters. Serafy (1973) studied morphological variation in L. variegatus from the West Atlantic and concluded that three ( L. variegatus atlanticus , L. variegatus carolinus , and L. variegatus variegatus ) of the four subspecies proposed by Mortensen (1933) were valid, raising L. variegatus pallidus H.L. Clark, 1925 to species category. On the other hand, Hendler et al. (1995) highlighted the need for further studies to support validity of these subspecies. A study carried out by Zigler & Lessios (2004), showed that the L. variegatus variegatus mtDNA is distinct from that of L. variegatus carolinus from the North American seaboard and the Gulf of Mexico, whereas their bindins are very similar. Here, young and adult specimens of L. variegatus were examined, and only variation in the apical system arrangement was observed, being dicyclic in the young and hemicyclic in adults. Bernasconi (1955) examined specimens from São Sebastião (SP) and observed variations in the number of secondary tubercles in the interambulacral plates, which can reach up to 2–3 in the adapical series and 2 in the adradial series at the ambitus.

Ecological notes. This species is preferentially found in calm waters, especially in banks of seagrass and on rocky and sandy substrates (del Valle García et al. 2005). According to Lessios (1998), L. variegatus is normally abundant in Thalassia beds in the Caribbean. Lima-Verde (1968) observed this species in calm waters with rocky or sandy substrates in the coastal areas of Ceará and Pernambuco, Brazil. Recently, this species was observed inhabiting hypersaline estuaries along the semiarid littoral of Rio Grande do Norte, being associated with sand-mud bottoms with a salinity of 42. In general, it is herbivorous ( Lawrence 1975), but its food preference is probably conditioned by the defensive chemistry produced by certain species of algae ( Souza et al. 2008). Inside its stomach, fragments of bryozoans, Foraminifera, diatoms, and several benthic marine invertebrates have been recorded ( Tommasi 1964). Like other species of Toxopneustidae , L. variegatus shows a "covering behaviour" using fragments of shells, gravel, and algae ( Hendler et al. 1995) ( Fig. 19C ). The same behavior was recorded for specimens from hypersaline habitats. Although there is much controversy about the meaning of this behaviour, it can provide protection against predators or physical factors such as light and temperature, thus preventing body dehydration ( Verling et al. 2004). In some areas along northeastern Brazil, L. variegatus displays population outbreaks in shallow, warm waters. At the reefs of Tamandaré, located in the Environmental Protection Area known as the Coral Coast (State of Pernambuco), dense populations of this species are commonly observed during the dry period, between September and February. Martins et al. (2012a) documented the aquarium fishery of this species along the coast of Salvador (BA). It is also one of the most important prey of the king helmet, Cassis tuberosa, in Brazilian waters ( Dias et al. 2017) ( Fig. 19D ).

Figures

FIGURE 7. Morphological characters of Lytechinus variegatus (UFPB/ECH.32). (A) Aboral view; (B) Oral view; (C–D) Valve of globiferous pedicellariae; (E) Valve of ophicephalous pedicellariae; (F) Valve of tridentate pedicellariae; (G) Valve of triphyllous pedicellariae; (H) Spicules of the tube feet; (I) Aboral view of naked test; (J) Oral view of naked test; (K) Tube foot ossicle; (L) Detail of the apical system; (M) Peristome; (N) Ambulacral plates; (O) 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.