Cnidaria: Antipatharia) from Brazil: an Overview

Black corals (Cnidaria: Antipatharia) from Brazil: an overview

Livia de Laia Loiola

Abstract There are few records of black corals (Cnidaria: Antipatharia) from Brazil, where there are previous reports of only 18 species from the families Antipathidae, Myrio- pathidae, and Schizopathidae. Most of these records are from the deep-sea, especially from southwestern Atlantic seamounts and the Brazilian continental shelf margins. Most specimens were collected between 13° and 22°S, during a study to survey the living resources off Brazil (REVIZEE Program), carried out by the Brazilian govern- ment. This paper is an historical overview concerning the geographic and bathymetric distribution of black coral species reported off Brazil. The genus Chrysopathes is herein reported for the first time in the Atlantic Ocean and the family Aphanipathidae (Subfamilies Acanthopathinae and Aphanipathinae) is reported for the first time in the southwestern Atlantic.

Taxonomic studies of deep-sea black corals in Brazil were intensified during the 1990s, specifically due to material collected by the REVIZEE Program, an official project to survey the living resources of the Brazilian Economic Exclusive Zone. The Antipatharia specimens provided by this program, collected between 13° and 22°S, were deposited in the Cnidaria Collection of the Museu Nacional–Rio de Janeiro, and they have been examined during the last 6 yrs, especially those from the family Myriopathidae (see Loiola and Castro, 2005). According to Castro et al. (2006), the greatest black coral richness off Brazil occurs in the area near the Cape of São Tomé (about 22°S), in depths between 100 and 500 m, with six species co-occurring there. This paper is an overview of the antipatharians reported off Brazil; the geographic and bathymetric distribution of the families are described and represented in tables and maps. Also, the first records of the genus Chrysopathes in the Atlantic Ocean, and of the family Aphanipathidae, both subfamilies Acanthopathinae and Aphanipathinae, in the southwestern Atlantic, are herein reported, and briefly described.

Previous Records

Order Antipatharia Family Antipathidae

The majority of black corals reported off Brazil are assigned to Antipathidae, represented by two genera: Antipathes, with three identified species and two different species yet to be identified at the specific level, andCirrhipathes , with one identified species and

George, R. Y. and S. D. Cairns, eds. 2007. Conservation and adaptive 253 management of seamount and deep-sea coral ecosystems. Rosenstiel School of Marine and Atmospheric Science, University of Miami. 254 LOIOLA

Table 1. General information about Antipathidae species that occur off Brazil: species, localities, and references.

Species Localities References Antipathes columnaris Northern Bahamas to Brazil (01°N); Opresko, 1974 (Duchassaing, 1870) Caribbean Antipathes atlantica Gray, 1857 West Indies, Brook, 1889; Gulf of Mexico; Cairns et al., 1993; Jamaica and Trinidad; Warner, 1981; Brazil (13°03ʹS–22°22ʹ57ʺS) Loiola and Castro, 2001; Castro et al., 2006 Antipathes furcata Gray, 1857 Madeira; Opresko, 1974; Caribbean; Barbados to Trinidad; Cairns et al., 1993; Gulf of Mexico; Loiola and Castro, 2001; Brazil (20°40ʹS–22°22ʹ57ʺS) Castro et al., 2006 Antipathes sp. 1 Brazil (13°20.87ʹS–19°45ʹ53ʺS) Castro et al., 2006 Antipathes sp. 2 Brazil (18°S) Castro, 1994 Cirrhipathes secchini Brazil (18°S) Castro, 1994; Echeverría, 2002 Echeverría, 2002 Cirrhipathes sp. 1 Brazil (13°03ʹ02ʺS) Castro et al., 2006 Cirrhipathes sp. 2 Brazil (19°37.49ʹS–22°22ʹ57ʺS) Castro et al., 2006 Cirrhipathes sp. 3 Brazil (20°40ʹ27ʺS) Castro et al., 2006 Cirrhipathes sp. 4 Brazil (12°58.65ʹS–22°22ʹ57ʺS) Castro et al., 2006 four species unidentified. General information about records of Antipathidae species that occur in Brazil are shown in Table 1.

Genus Antipathes

A single specimen of Antipathes columnaris was reported by Opresko (1974, see Ech- everría and Castro, 1995), only from off the Amazon River mouth. Antipathes atlantica is the Antipathidae species reported with a wider latitudinal distribution off the eastern coast of Brazil, in depths between 50–300 m (Loiola and Castro, 2001; Castro et al., 2006). Also from this region, Antipathes furcata was reported at depths of 100–300 m (Loiola and Castro, 2001; Castro et al., 2006). Two unidentifiedAntipathes species were reported: one from deeper areas (66–390 m, see Castro et al., 2006), and another from shallow reef areas (up to 20 m), on the Abrolhos Bank (Castro, 1994). These two species have fan-shaped corallum, branched in a single plane. The geographic distribution of Antipathes species off Brazil, between 13° and 22°S, is shown in Figure 1.

Genus Cirrhipathes

A species of Cirrhipathes was reported from shallow reef areas (10–25 m) on the Abrolhos Bank (Castro, 1994), and later described as a new species: Cirrhipathes secchini. Four unidentified species were reported by Castro et al. (2006) at depths of 50–706 m, off the Brazilian eastern coast. These four species differ with regard to the size and shape of their spines (C. B. Castro, Museu Nacional, Universidade Federal do Rio de Janeiro, pers. comm.). The geographic distribution of this genus off Brazil, between 13° and 22°S, is shown in Figure 2. BRAZILIAN BLACK CORALS 255

Figure 1. Distribution of Antipathidae—genus Antipathes, off Brazil, between 13°–22°S: n Anti- pathes atlantica; ▲ Antipathes furcata; ◆ Antipathes sp. 1; ✖ Antipathes sp. 2.

Figure 2. Distribution of Antipathidae—genus Cirrhipathes, off Brazil, between 13°–22° S: n Cirrhipathes sp. 1; ◆ Cirrhipathes sp. 2; Cirrhipathes sp. 3; l Cirrhipathes sp. 4. 256 LOIOLA

Figure 3. Distribution of Myriopathidae—genus Tanacetipathes, off Brazil, between 13°–22°S: l Tanacetipathes barbadensis (Brook, 1889); n Tanacetipathes tanacetum (Pourtalès, 1880); ◆ Tanacetipathes hirta (Gray, 1857); ✖ Tanacetipathes thamnea (Warner, 1981); ▲ Tanacetipathes longipinnula n. sp.; ✚ Tanacetipathes thalassoros n. sp. Family Myriopathidae

Records of Myriopathidae from the eastern coast of Brazil between 13° and 22°S (Fig. 3) include one Plumapathes species and six Tanacetipathes species (Loiola and Castro, 2005). General information about records of Myriopathidae species that occur in Brazil are shown in Table 2. Plumapathes fernandezi (Pourtalès, 1874) was reported by Echeverría (2002) as a unique specimen, collected from off Rio Grande do Sul State, depth unknown. Tanacetipathes barbadensis was reported by Loiola and Castro (2005) in shallow reefs (8–20 m) on the Abrolhos Bank. These specimens are mentioned as Antipathes sp. in Castro (1994), and the same specimens were erroneously identified as Antipathes hirta Gray, 1857 by Echeverría (2002). Tanacetipathes hirta (Gray, 1857) occurs at two points along the Brazilian eastern coast, between 100–417 m (Loiola and Castro, 2005; Castro et al., 2006). Pérez et al. (2005) described Tanacetipathes paula Pérez, Costa and Opresko, 2005 as a new species from the Archipelago of Saint Peter and Saint Paul, but this species was later considered by Loiola and Castro (2005) to be a synonym of Tanacetipathes thamnea. The Myriopathidae species with greater latitudinal distribution along the Brazilian eastern coast is T. thamnea, which occurs at depths of 53–558 m (Loiola and Castro, 2005; Castro et al., 2006). Tanacetipathes tanacetum is the most abundant species along Brazilian seamounts and continental slope off the eastern coast. Opresko (1972) mentioned two records of this species (off the Parcel of Manoel Luís, and off the Atol das Rocas). Other records of T. tanacetum are from off southeastern Brazil, at depths ranging from 60 to 706 m (Echeverría and Castro, 1995; Loiola and Castro, 2005; Castro et al., 2006). BRAZILIAN BLACK CORALS 257

Table 2. General information about Myriopathidae species that occur off Brazil: species, localities, and references.

Species Localities References Plumapathes fernandezi Eastern Pacific; Opresko, 2001; (Pourtalès, 1874) Brazil (29°–34°S) Echeverría, 2002 Tanacetipathes barbadensis Barbados; Brook, 1889; (Brook, 1889) Trinidad; Warner, 1981; Brazil (18°S) Loiola and Castro, 2005 Tanacetipathes hirta Florida; Brook, 1889; (Gray, 1857) Venezuela; Opresko, 1972 Caribbean; Warner, 1981; Trinidad; Loiola and Castro, 2005; Brazil (19°43.86ʹS–21°38ʹ57ʺS) Castro et al., 2006 Tanacetipathes tanacetum “Lesser Antilles”; Pourtalès, 1880; (Pourtalès, 1880) Brazil (00°17ʹN; 03°50ʹS; Brook, 1889; 19°37.49ʹS–23°01ʹS) Opresko, 1972; Echeverría and Castro, 2005; Loiola and Castro, 2005; Castro et al., 2006 Tanacetipathes thamnea Trinidad; Warner, 1981; (Warner, 1981) Brazil (00°55ʹN; 13°06.79ʹS–20°40, Pérez el al., 2005; 07ʹS) Loiola and Castro, 2005; Castro et al., 2006 Tanacetipathes longipinnula Brazil (20°29.06ʹS–22°22ʹ57˝ S) Loiola and Castro, 2005 Loiola and Castro, 2005 Castro et al., 2006 Tanacetipathes thalassoros Brazil (20°S–20°57ʹS) Loiola and Castro, 2005 Loiola and Castro, 2005 Castro et al., 2006 Two new species of Tanacetipathes were described by Loiola and Castro (2005), Tanacetipathes longipinnula and Tanacetipathes thalassoros, both from off the southeastern coast of Brazil; the first one at Almirante Saldanha Bank, from 50–300 m, and the second restricted to the Vitória Trindade seamounts chain, at depths of 50–100 m (Loiola and Castro, 2005).

Family Schizopathidae

The Schizopathidae from Brazil is represented by two specimens, collected off the Bahia State coast (Fig. 4), 2137 m, and identified as Schizopathes affinis (Loiola and Castro, 2001). This species represents the deepest record of a black coral off Brazil. General information about records of Schizopathidae species that occur in Brazil are shown in Table 3.

New Records

Family Aphanipathidae Subfamily Acanthopathinae Acanthopathes humilis (Pourtalès, 1867)

Antipathes humilis Pourtalès, 1867: 112; 1880: 118, pl. 3, figs. 18, 19, and 32. Aphanipathes humilis: Brook, 1889: 131; Opresko, 1972: 994–999, fig. 10. Acanthopathes humilis: Opresko, 2004: 230–232, fig. 12 a–b. 258 LOIOLA

Figure 4. Distribution of Acanthopathidae, Cladopathidae, and Schizopathidae off Brazil, between 13°–22°S: n Acanthopathes humilis; ✖ Aphanipathes sp.; l Chrysopathes sp.; ▲ Schyzo- pathes affinis. Material examined.—Brazil, off Vitória, 20°10´S, 39°48´W, 315 m (MNRJ 5445: 1 colony). Brief description.—Colony 8.0 cm tall, 14.0 cm wide. Stem small, 3.0 mm in diameter near the base, from where two lateral series of branches develop. Successive branches added laterally predominantly on the outer side of the lower branches, most of them being curved upwards near their point of insertion, and thus becoming parallel to the stem. Few smaller branchlets developed on the inner side of branches. Colony expands more laterally than vertically, resulting in a candelabrum-like shape. Branches up to the 14th order, lower order branches long (18–56 mm long, 0.7–1.5 mm in diameter), reaching the top of the colony; upper order branches short (4–23 mm, 0.5–0.7 mm in diameter); distance between points of insertion 2.5–20 mm (Fig. 5A). Spines anisomorphic, ornamented near the apex, cylindrical; hypostomal spines reduced in size (0.13–0.18 mm tall, 0.04–0.05 mm wide), circumpolypar spines larger (0.4–0.5 mm tall, 0.06–0.08 mm wide) than interpolypar (0.3–0.4 mm tall, 0.04–0.08 mm wide) and abpolypar spines (0.2–0.3 mm tall, 0.04–0.06 mm wide) (Fig. 5B–E). Spines on polypar side stand at 90° Table 3. General information about Aphanipathidae, Cladopathidae, and Schizopathidae species that occur off Brazil: species, localities, and references.

Species Localities References Acanthopathes humilis Western Atlantic; Opresko, 2004; present record (Pourtalès, 1867) Brazil (20°10ʹS) Aphanipathes sp. Brazil (20°30ʹS) Castro et al., 2006; present record Chrysopathes sp. Brazil (13°23ʹS; 22°24.655ʹS) Present record Schizopathes affinis Cosmopolitan; Opresko, 1997 Brook, 1889 Brazil (13°26.455ʹS) Loiola and Castro, 2001 Castro et al., 2006 BRAZILIAN BLACK CORALS 259

Figure 5. Acanthopathes humilis (MNRJ 5445) (A) Colony; (B) polypar spines; (C) abpolypar spines; (D) polypar spines of the middle region of a branch, HP–hipostomal spines; (E) abpolypar spines, closer view. Scale bars: A = 1.0 cm; B–C = 0.02 cm; D–E = 0.06 mm. to branch or slightly curved upwards, some of them only with apexes curved, spines on abpolypar side extremely curved upwards. In thicker branches and in the stem, spines in 28–30 longitudinal rows, in narrower branches, 18–20 rows, 6–8 spines per mm in each row. Polyps badly preserved. Remarks.—The Brazilian specimen greatly resembles the candelabrum variety of A. humilis described by Opresko (1972). There are small differences in spine size between the Brazilian and Opresko’s (2004) specimens, but the planar branching pattern, the tendency of branchlets to develop on the convex side of the lower order branches, and the distinctly anisomorphic spines, characteristics of A. humilis, are found in the Brazilian specimen. 260 LOIOLA

Aphanipathidae was recently established by Opresko (2004), and A. humilis was previously recorded in the western Atlantic from the Bahamas to Grenada (Opresko, 1972, 2004). This is the first record of this family in the southwestern Atlantic (Fig. 4). General information about records of Aphanipathidae species that occur in Brazil are shown in Table 3.

Subfamily Aphanipathinae Aphanipathes sp.

Aphanipathes Brook, 1889: 121; Opresko, 2004: 212–214, fig. 1.

Material examined.—Brazil, off Trindade island, 20°30´S, 029°16´W, 360 m, RE- VIZEE Central V Sta. # 41 (MNRJ 4865: 1 colony). Brief description.—Colony 8.0 cm tall, 11.0 cm wide, 6.0 cm thick. No distinct stem or basal plate, colony base fused to a scleractinian coral. Colony bushy, basal branches straight, nearly horizontal, distal branches 45–90° to basal ones. Branching up to the 5th order, lower order branches 30–41 mm long, 0.5–0.9 mm in diameter, upper order branches 8–25 mm long, 0.1–0.4 mm in diameter. Distance between points of insertion 2–10 mm (Fig. 6A). Spines triangular, conical, curved towards the branch apex, with acute apex; at midpoint of branches spines with big knob-like tubercles over apical half surface, at basal and distal ends of branches, spines less ornamented or smooth. No differences in size between polypar and abpolypar spines—0.10–0.14 mm tall, 0.05–0.09 mm wide at base. Spines arranged in 6–8 longitudinal rows on narrower branches, and in 8–10 rows on thicker branches, 4–5 spines per mm in each row (Fig. 6B–D). Polyps badly preserved. Remarks.—This specimen was identified as Aphanipathes because of the bushy form of the corallum, with straight ascending branches, and the spines being conical with conical tubercles on the surface, like the four species assigned to this genus by Opresko (2004). Aphanipathes sarothamnoides Brook, 1889, the type species of this genus, has longer branchlets (5–10 cm) occurring farther apart from each other (1.5–2.5 cm), and taller spines (about 0.20 mm) (Brook, 1889; Opresko, 2004), than Brazilian specimen: branchlets 0.8–4.1 cm long, 0.2–1.0 cm apart, and spines 0.10–0.14 tall. Aphanipathes salix (Pourtalès, 1880) has branchlets 2–3 cm long, 0.3–2.0 cm apart, but the spines are taller than in Brazilian specimen—polypar 0.22 mm, and abpolypar 0.13 mm (Opresko, 1972). Aphanipathes verticillata Brook, 1889 differs from Brazilian specimens in that the spines are arranged in verticils (Brook, 1889; Opresko, 1972, 2004). Aphanipathes pedata (Gray, 1857) is branched strictly in one plane (Brook, 1889; Opresko, 1972), and according to the illustration given by Brook (1889: pl. 11, fig. 12), the spines are more extensively covered by tubercles than in the Brazilian specimen. Further studies of additional Brazilian specimens might confirm that this Brazilian specimen is a new species. This subfamily is herein reported for the first time in the southwestern Atlantic, off Trindade Island, 360 m (Fig. 4). According to Brook (1889) and Opresko (2004), species of this genus have been reported from the West Indies (A. pedata and A. salix), south Pacific A.( sarothamnoides), and Indian Ocean (A. verticillata). BRAZILIAN BLACK CORALS 261

Figure 6. Aphanipathes sp. (MNRJ 4865) (A) Colony; (B) spines of the middle region of a branch; (C) spines of the basal region of a branch; and (D) spines, close view. Scale bars: A = 1.0 cm; B–C = 0.02 cm; D = 0.06 mm.

Family Cladopathidae Chrysopathes sp.

Chrysopathes Opresko, 2003: 498; 515.

Material examined.—Brazil: off Salvador, 13°23′S, 038°37′W, 761 m, REVIZEE Ba- hia-2 Sta. # E0499 (MNRJ 4627: 1 colony); off Campos, 22°24.655′S, 039°55.413′W, 1130 m, BC-Sul-CENPES/UFRJ, (MNRJ 5150: 1 colony). Brief description.—Colonies 10.0 (off Salvador) and 19.5 cm (off Campos) tall, 4.0 and 15.0 cm wide, respectively. Axis 0.5 and 1.0 mm in diameter near the base; basal plate, 10.5 and 4.0 mm in diameter, respectively. Branching lateral, up to the 2nd or- 262 LOIOLA

Figure 7. Chrysopathes sp. (MNRJ 5150) (A) Colony; (B) transversal view of a colony, cycle of pinnules; (C) spines of the basal region of a pinnule; (D) spines of the middle region of a pinnule; (E) polypar spines of the middle region of a pinnule, close view; and (F) abpolypar spines of the middle region of a pinnule, close view. Scale bars: A = 1.0 cm; B = 0.5 cm; C–D = 0.2 mm; E–F = 0.02 mm. der, colonies fan shaped (Fig. 7A). Primary pinnules in six rows, in laterally alternating groups of three primaries each (Fig. 7B); polypar and abpolypar primaries 4.0–16.0 mm long; diameter of primaries 0.12–0.20 mm; distance between adjacent (in the same row) primaries 2.1–4.4 mm (Fig. 7A). Four to five primary pinnule cycles per cm of axis (Fig. 7B). Secondary pinnules only on the proximal half of primaries, on the abpolypar side or on a plane perpendicular to the plane defined by the primaries, either towards the distal or the proximal end of the colony, 0–2 per primary pinnules; 2–6 mm long, 0.08–0.16 mm in diameter; the secondary pinnules can occur on anterior, posterior and lateral primaries on all parts of the colony (Fig. 7B). Tertiary pinnules rarely present, only one per secondary, within a plane defined by the primaries (Fig. 7B). Spines conical, com- pressed, smooth; apices of polypar and abpolypar spines curved towards the distal end of the pinnules; furcated spines rarely present; six regular longitudinal rows (around the whole pinnule); polypar and abpolypar spines not differentiated in size, 0.02–0.09 mm tall, 0.03–0.07 mm wide at base; four to six spines per mm in a row; distance between adjacent spines in each row 0.14–0.34 mm (Fig. 7C–F). Polyps badly preserved. BRAZILIAN BLACK CORALS 263

Remarks.—Although the Brazilian specimens have a general corallum appearance similar to Chrysopathes formosa Opresko, 2003, there are some substantial differences in the subpinnulation pattern that indicate they are different species. Brazilian specimens can have single secondary pinnules, or subopposite pairs of secondaries per primary, and occasionally have tertiary pinnules; C. formosa has lateral primary pinnules with a single secondary, and tertiary pinnules are absent (Opresko, 2003). Chrysopathes speciosa Opresko, 2003 differs from Brazilian Chrysopathes also in the secondary pinnules pattern: up to four secondaries on some primary pinnules, with arrangements highly variable, either alternate, uniserial, subopposite, or irregular (Opresko, 2003). Further studies and comparisons with other Atlantic specimens from this family might indicate that these Brazilian specimens could be a new species, and that this genus could have a wider geographic distribution (D. M. Opresko, Oak Ridge National Laboratory, unpubl. data). This is the first record ofChrysopathes in the Atlantic ocean, in two different Brazil- ian regions: off Salvador and off Campos (Fig. 4). Previously this genus was reported only in the eastern Pacific (Opresko, 2003). General information about records of Clado- pathidae species that occur in Brazil are shown in Table 3.

Acknowledgments

I thank the REVIZEE Program for providing the specimens, and Conselho Nacional de De- senvolvimento Científico e Tecnológico (CNPq) for grants and fellowships that aided the develop- ment of this study. Also, C. Castro (Museu Nacional, Universidade Federal do Rio de Janeiro) and D. Opresko (Oak Ridge National Laboratory) for helpful comments and suggestions throughout this study; M. Medeiros (Museu Nacional, Universidade Federal do Rio de Janeiro) for help in preparation of illustrations; and B. Vale (Departamento de Patologia, Fundação Oswaldo Cruz) for preparing the samples and images for SEM.

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