INTRODUCTION
The Saint Peter and Saint Paul Archipelago (SPSPA) (00°55′N 29°21′W) is a group of very small islets located on the mid-Atlantic ridge, 1010 km from the Cape of Calcanhar, on the north-eastern coast of Brazil and 1824 km from Africa. The SPSPA is a unique setting in the Atlantic Ocean, as the islands were formed by a geological uplift of the seafloor rather than through volcanic activity and have only a thin layer of sedimentary covering (Campos et al., Reference Campos, Petta, Theye, Sichel, Simões, Srivastava, Motoki, Neto, Andrade and Hazin2009). Due to its very small size and isolation, the SPSPA is of historical and biogeographical interest (Edwards & Lubbock, Reference Edwards and Lubbock1983a, Reference Edwards and Lubbockb). It was visited by Charles Darwin during the Beagle Expedition in the first half of the 19th Century, followed by the H.M.S. Challenger some decades later. Over the next hundred years, only sporadic scientific reports have come to light. Several manuscripts appeared as a result of the Cambridge Expedition (1979) (Edwards & Lubbock, Reference Edwards and Lubbock1983a, and references therein) and investigations at SPSPA were intensified after the implementation of the Brazilian scientific station in 1998. Since then, there has been a great increase in knowledge of the biodiversity and ecology from SPSPA (Hazin, Reference Hazin2009 and references therein).
Brittle stars, a very common group in benthic communities, live in a great variety of habitats, from sea shores to the deep ocean, in soft sediments or on rocks and in association with corals, sponges, algae and thermal seeps (Hendler et al., Reference Hendler, Miller, Pawson and Kier1995; Stöhr et al., Reference Stöhr, O'Hara and Thuy2012). With a total of 2138 described species and subspecies (Stöhr et al., Reference Stöhr, O'Hara and Thuy2014), they comprise the most diverse class of echinoderms, a group that also includes sea urchins, sea cucumbers, sea stars and sea lilies. O'Hara et al. (Reference O'Hara, Hugall, Thuy and Moussalli2014) published the most complete phylogeny yet of brittle stars using molecular and fossil data. They used all extant echinoderms classes and confirmed the hypothesis that brittle stars are a sister group of sea stars with a mid-Permian origin. Species that have been recorded from the Brazilian coast constitute about 6% of those known worldwide (Barboza & Borges, Reference Barboza and Borges2012). Records from the north-eastern coast and their oceanic islands, such as the Fernando de Noronha Archipelago, are evidence of a tropical fauna that shares most of the species from the Caribbean Sea, revealing the great affinity between the two regions. Bearing in mind the scarcity of records on the diversity and ecology of echinoderms from SPSPA, this article is a contribution towards bridging this gap, by increasing the number of brittle star records, with the inclusion of diagnoses and images and the provision of mitochondrial DNA sequences.
MATERIAL AND METHODS
Study area
SPSPA comprises four larger islets plus several minor rocks, rising 4000 m from the ocean depths (Figure 1). The emerged area of the archipelago is about 13,000 m2, 420 m across at the greatest breadth. The maximum height is 18 m. Belmonte, the largest islet, together with Saint Paul, Saint Peter and Barão de Teffé, constitute a horseshoe-shaped cove 100 m long, 50 m wide and with a maximum depth of around 15–18 m (Figure 1). We sampled the four distinctive sublittoral zones recognized by Edwards & Lubbock (Reference Edwards and Lubbock1983a): (1) the Palythoa zone (3–8 m), dominated by Palythoa caribaeum (Duchassaing & Michelotti, Reference Duchassaing and Michelotti1860) with the presence of the green alga Caulerpa racemosa (Forsskål) J. Agardh, Reference Agardh1873 in the more sheltered areas. The brown alga Dictyota dichotoma (Hudson) J.V. Lamouroux, Reference Lamouroux1809a, sponges and hydroids dominate the substrates where P. caribaeum is absent; (2) the Caulerpa racemosa zone, formed by dense carpets at depths between 3 and 8 m and then between 30 and 6 m, and absent in unstable substrates; (3) the sub-Caulerpa zone, which occupies depths deeper than 30–36 m, where Caulerpa is replaced by D. dichotoma, Ceratodictyon planicaule (W.R. Taylor) M.J. Wynne, Reference Wynne2011, Bryopsis pennata J.V. Lamouroux, Reference Lamouroux1809b, crustose lithothamnia, bryozoans, Antipathes black corals and sponges; (4) the zones of patches of unstable substrates that occur at depths between 3 and 25 m. This substrate is mainly formed by coarse sand, rubble and rocks (Figure 1D).
Location of Saint Peter and Saint Paul's Archipelago (A), dive points distribution (B) and details of sampling sites (C–E).
The oceanographic regime of the Archipelago is dominated by the influence of the South Equatorial Current (SEC) and the Atlantic Equatorial Undercurrent (UEC) (Araujo & Cintra, Reference Araújo, Cintra and Hazin2009). The SEC, the prevailing surface current of the region, flows westward providing connections with east Atlantic waters (Briggs, Reference Briggs1974). As a branch derived from the North Brazilian Current, the UEC flows eastwards at subsurface depths between 60 and 100 m and reaches speeds higher than 100 cm seg−1 (Macedo et al., Reference Macedo, Montes, Costa and Hazin2009). Thus, despite a westward-prevailing current system, SPSPA is also influenced by western Atlantic waters.
Sampling procedures
Field sampling was conducted by scuba diving during the months of June 2011 and July 2013, in the areas indicated in Figure 1B. Samples of alga-turf, tubes of the polychaete Chaetopterus and sponges scraped from rock surfaces were collected at depths between 3 and 30 m. All the material was placed in plastic bags for further sieving. Samples of soft sediments were also collected and subsequently washed through a 0.5 mm mesh. All brittle star individuals were preserved in a 95% alcohol solution. All specimens were deposited at the collection of the National Museum of Rio de Janeiro.
Molecular data
Tissue of brittle star arms was used for DNA extraction, according to the NaOH protocol (Floyd et al., Reference Floyd, Abebe, Papert and Blaxter2002). Fragments of COI were amplified using the forward primer COIf (5′-CCTGCAGGAGGAGGAGAYCC-3′) and the reverse primer COIa (5′-AGTATAAGCGTCTGGGTAGTC-3′) (Palumbi et al., Reference Palumbi, Martin, Romano, McMillan, Stice and Grabowski1991). Fragments of 16S were amplified using a contig of the forward primers 16SarL (5′-CGCCTGTTTATCAAAAACAT-3′) and 16SF2 (5′-GTTTCGGTTTACCAAAAACAT-3′), and reverse primers 16SAN-R (5′-GCTTACGCCGGTCTGAACTCAG-3′) and 16SR2 (5′-AGGTTTTTCTGATCCAACATCG-3′) (Palumbi et al., Reference Palumbi, Martin, Romano, McMillan, Stice and Grabowski1991; Le Gac et al., Reference Le Gac, Féral, Poulin, Veyret and Chenuil2004; Zanol et al., Reference Zanol, Halanych, Struck and Fauchald2010). PCRs were carried out at a total volume of 25 µL, with an annealing temperature of 45°C (COI) and 50°C (16S). Bidirectional sequencing was performed using the same amplification primers. Sequence data were aligned through Muscle using Mega 6.0 (Tamura et al., Reference Tamura, Stecher, Peterson, Filipski and Kumar2013). For 16S fragments the unalignable bits were removed using GBlocks within SeaView v.4.3.5 (Gouy et al., Reference Gouy, Guindon and Gascuel2010) applying all the less stringent selection options. Sequences were submitted to GenBank (accession numbers: KP128035-42) and to BOLDSYSTEMS (Brazilian Barcode of Life database [BrBOL]).
To source out to which clade our specimens belong we used GenBank sequences from the brittle star genera Amphipholis, Amphiura, Ophiactis, Ophionereis, Ophiopholis, Ophiothrix, Macrophiothrix, Ophiocoma, Ophiopeza and the sea star Luidia clathrata (Say, Reference Say1825) (accession numbers: AF331527-30, AF331533, AF331534, AF331536, AF331537, AF331539-73, AF331591, AF331592, AF331594, AF331595, AF331600, AF331601, AF331603-16, AF331629, AF331632, AF331634-36, AF480892-480905, EU583176, EU583205, NC013876, AY652509, KC760129, DQ297108, AY652511-13, AY365182, AY365179, AY365169, AY365176, AY365153-55, AY365161, AY365147, AY365158, AY365143, AY365165, AY365170, AY365174, KF662941-42, DQ297102, KC760098, HM473899, DQ297096). Maximum-likelihood (ML) trees were obtained using the program Mega 6.0 (Tamura et al., Reference Tamura, Stecher, Peterson, Filipski and Kumar2013) using GTR + G + I (16S) and T92 + G + I (COI) models of evolution and 1000 pseudo-replicates to calculate bootstrap values.
RESULTS
A total of 108 individuals of five species representing four families were sampled: Ophiotrichidae, Ophiothrix (Ophiothrix) angulata (Say, Reference Say1825) (N = 1); Ophiocomidae, Ophiocomella ophiactoides (H.L. Clark, Reference Clark1900) (N = 3); Amphiuridae, Amphipholis squamata (Delle Chiaje, Reference Delle Chiaje1828) (N = 43); Ophiactidae, Ophiactis lymani Ljungman, Reference Ljungman1872 (N = 89); and Ophiactis savignyi (Müller & Troschel, Reference Müller and Troschel1842) (N = 6).
Taxonomic account
SYSTEMATICS
Order ophiurida Müller & Troschel, Reference Müller and Troschell1840
Family ophiotrichidae Ljungman, Reference Ljungman1867
Ophiothrix (Ophiothrix) angulata Say, Reference Say1825
(Figures 2A, 3A–E)
MATERIAL EXAMINED
One individual (0.91°N 29.34°W, 5 m, July 2013). Disk diameter: 5 mm.
DIAGNOSIS
A living individual is presented in Figure 2A. Disk bears long spines with bifid and trifid tips (Figure 3A, B). The spines also cover the radial shields, but less densely. Oral shields wider than long. Adoral shields wing-like and separated at the proximal edge (Figure 3C). A clump of oral papillae at the tip of each jaw (Figure 3C). Dorsal arm plates longer than wide, the convex distal edge slightly lobed (Figure 3D). Ventral plates longer than wide with a median depression on distal edge (Figure 3E). Seven to eight very thorny arm spines. Dorsal ones are three segments in length, decreasing ventrally. One very small tentacle scale. The ground colour is violet. Arms have regular transverse violet banding pattern that extend to the spines. The distal edge of the dorsal arm plates is white. These plates also have irregular white spots. A longitudinal stripe on the upper side of the arm is wanting.
Living individuals of Ophiothrix (Ophiothrix) angulata (A) and Ophiocomella ophiactoides (B). Disk diameters are: 5 mm (A), 3.5 mm (B).
Ophiothrix (Ophiothrix) angulata: dorsal view (A), details from the spines of the disk (B), ventral view (C), dorsal view of the arms (D), ventral view of the arms (E). Ophiocomella ophiactoides: dorsal view (F), ventral view (G). Ophiactis savignyi: dorsal view (H), ventral view (K). Ophiactis lymani: dorsal view (I), ventral view (L). Amphipholis squamata: dorsal view (J), ventral view (M). Disk diameters are: 5 mm (A and C), 3.5 mm (F–G), 2.8 mm (H–K), 2.3 mm (I–L) and 2.8 mm (J–M). Scale bars: B, 0.2 mm, D and E, 1.25 mm.
DISTRIBUTION
West coast of Mexico, Florida, Gulf of Mexico and the Caribbean, between 0 and 540 m (Hendler et al., Reference Hendler, Miller, Pawson and Kier1995; Miloslavich et al., Reference Miloslavich, Díaz, Klein, Alvarado, Díaz, Gobin, Escobar-Briones, Cruz-Motta, Weil, Cortés, Bastidas, Robertson, Zapata, Martín, Castillo, Kazandjian, Ortiz and Hernández2010; Stöhr et al., Reference Stöhr, O'Hara and Thuy2014). Recorded along the entire Brazilian coast (Barboza & Borges, Reference Barboza and Borges2012 and references therein).
REMARKS
Ophiothrix (Ophiothrix) angulata has a great diversity in all characters used to distinguish the Ophiothrix species (Clark, Reference Clark1918). From a typical form sensu Clark (Reference Clark1918), our specimen differs by lacking a white longitudinal stripe on the upper side of the arms and flattened or smoothed upper arm spines. In this study, it was sampled and associated with Chaetopterus polychaete tubes.
Order ophiurida Müller & Troschel, Reference Müller and Troschell1840
Family ophiocomidae Ljungman, Reference Ljungman1867
Ophiocomella ophiactoides H.L. Clark, Reference Clark1900
(Figures 2B, 3F–G)
MATERIAL EXAMINED
Four individuals (0.91°N 29.34°W, 5–15 m, July 2013). Disk diameter: 1.5–3.5 mm.
DIAGNOSIS
A living individual is presented in Figure 2B (one broken arm). Hexamerous, fissiparous species. Disk dorsally covered with scales bearing conical spines (Figure 3F). Only the tips of the radial shields are visible. Each jaw, longer than wide, bears two apical and three lateral papillae (Figure 3G). Oral shields slightly longer than wide with a distal lobe. Adoral shields long, with flaring distal edge (Figure 3G). Dorsal arm plates longer than wide with a convex distal edge. Ventral plates longer than wide with truncated edge. Three or four conical spines and one tentacle scale.
DISTRIBUTION
A shallow water species recorded from the west coast of Mexico, Gulf of Mexico and the Caribbean (Hendler et al., Reference Hendler, Miller, Pawson and Kier1995; Miloslavich et al., Reference Miloslavich, Díaz, Klein, Alvarado, Díaz, Gobin, Escobar-Briones, Cruz-Motta, Weil, Cortés, Bastidas, Robertson, Zapata, Martín, Castillo, Kazandjian, Ortiz and Hernández2010; Stöhr et al., Reference Stöhr, O'Hara and Thuy2014). In Brazil, it has been recorded from the Vitoria–Trindade Seamount Chain to the north-east coast (Barboza & Borges, Reference Barboza and Borges2012 and references therein).
REMARKS
Ophiocomella ophiactoides is a common brittle star from north-eastern Brazil. In this study it was sampled associated with algae (absent on Caulerpa turfs).
Order Ophiurida Müller & Troschel, Reference Müller and Troschell1840
Family Ophiactidae Matsumoto, Reference Matsumoto1915
Ophiactis savignyi (Müller & Troschel, Reference Müller and Troschel1842)
(Figure 3H–K)
MATERIAL EXAMINED
Five individuals (0.91°N 29.34°W, 15 m, June 2011); one individual (0.91°N 29.34°W, 8 m, July 2013). Disk diameter: 1–3 mm.
DIAGNOSIS
Hexamerous brittle star. Disk with conical spines at the distal edge and between the pairs of radial shields (Figure 3H). The latter are contiguous lengthwise over at least half of the internal edges. Oral shields with rounded edges as wide as long. Each jaw bears a rectangular tooth at the tip (Figure 3K). The number of lateral oral papillae can vary from no papillae, to one, two or three. Variability can occur in a single individual (Figure 3K). Dorsal arm plates as wide as long. Ventral plates with a slightly convex distal edge. Four to five thorny arm-spines. One tentacle scale.
DISTRIBUTION
Cosmopolitan species from tropical and temperate waters between depths of 0 and 550 m (Roy & Sponer, Reference Roy and Sponer2002; Pawson et al., Reference Pawson, Vance, Messing, Solis-Marin, Mah, Felder and Camp2009). Recorded along the entire Brazilian coast (Barboza & Borges, Reference Barboza and Borges2012 and references therein). Suspected to be a species complex.
REMARKS
Clark (Reference Clark1918) reported individuals with none, one or two papillae. This variability was also pointed out by Tommasi (Reference Tommasi1970). Here, as mentioned by Clark (Reference Clark1918), small specimens have less fan-shaped dorsal arm plates and coarser dorsal disk scales. In this study individuals were sampled associated with algae (absent on Caulerpa turfs). Most presented evidence of regeneration.
Order Ophiurida Müller & Troschel, Reference Müller and Troschell1840
Family Ophiactidae Matsumoto, Reference Matsumoto1915
Ophiactis lymani Ljungman, Reference Ljungman1872
(Figure 3I–L)
MATERIAL EXAMINED
24 individuals(0.91°N 29.34°W, 5–30 m, June 2011); 65 individuals (0.91°N 29.34°W, 5–20 m, July 2013). Disk diameter: 0.5–2.5 mm.
DIAGNOSIS
Hexamerous species. Disk covered above (Figure 3I) and below (Figure 3L) with scales. Radial shields separated proximally and in contact at distal edge. Oral shields rhombic. Adoral shields distally enlarged and separated at proximal edge. A distinctive rectangular tooth at the tip of each jaw. One lateral oral papilla (Figure 3L). Fan-shaped dorsal arm-plates, wider than long on proximal segments and as wide as long on distal ones. Ventral plates pentagonal. Three conical, minutely thorny arm-spines. One tentacle scale.
DISTRIBUTION
Caribbean Sea and South Atlantic, between depths of 0 and 600 m (Tommasi, Reference Tommasi1970; Monteiro, Reference Monteiro1987; Miloslavich et al., Reference Miloslavich, Díaz, Klein, Alvarado, Díaz, Gobin, Escobar-Briones, Cruz-Motta, Weil, Cortés, Bastidas, Robertson, Zapata, Martín, Castillo, Kazandjian, Ortiz and Hernández2010; Stöhr et al., Reference Stöhr, O'Hara and Thuy2014). Recorded along the entire Brazilian coast (Barboza & Borges, Reference Barboza and Borges2012 and references therein).
REMARKS
Ophiactis lymani is a very common brittle stars species from the western Atlantic that can be distinguished from Ophiactis savignyi by: (1) the shape of the dorsal scales of the disk; (2) the more fan-shaped dorsal arm plates; (3) the morphology of the arm spines. In this study Ophiactis lymani was primarily sampled associated with algae (absent on Caulerpa turfs). Almost all the individuals were regenerating parts of the arms or the disk.
Order Ophiurida Müller & Troschel, Reference Müller and Troschell1840
Family Amphiuridae Ljungman, Reference Ljungman1867
Amphipholis squamata (Delle Chiaje, Reference Delle Chiaje1828)
(Figure 3J–M)
MATERIAL EXAMINED
Five individuals (0.91°N 29.34°W, 5–30 m, June 2011); 38 individuals (0.91°N 29.34°W, 5–20 m, July 2013). Disk diameter: 1–3 mm.
DIAGNOSIS
Both sides of the disc covered with plates. Radial shields internally united (Figure 3J). Oral shields rhombic (Figure 3M). Longer than wide wing-like adoral shields meet inter-radially. Two apical papillae. Two lateral oral papillae, the distal one enlarged (Figure 3M). Dorsal arm-plates with rounded distal edges. Ventral arm-plates pentagonal. Three to four conical and minutely thorny arm-spines. Two small tentacle scales.
DISTRIBUTION
Cosmopolitan species of tropical and temperate waters between depths of 0 and 1.200 m (Paterson, Reference Paterson1985; Boissin et al., Reference Boissin, Féral and Chenuil2008; Stöhr et al., Reference Stöhr, O'Hara and Thuy2014). Recorded along the entire Brazilian coast (Barboza & Borges, Reference Barboza and Borges2012 and references therein). Suspected to be a species complex.
REMARKS
Due to the size of the examined specimens there are no visible primary plates on the disc as an adult. In this study Amphipholis squamata, a common brittle star in SPSPA, was sampled associated with algae (absent for Caulerpa turfs) and in soft substrates.
Molecular results
Sequences were obtained for four of the five species, 16S: Ophiothrix (Ophiothrix) angulata (1; 433 bp), Ophiocomella ophiactoides (1; 433 bp), Ophiactis lymani (3; 433 bp); COI Ophiactis savignyi (1; 301 bp), Ophiactis lymani (1; 227 bp) and Ophiocomella ophiactoides (1; 409 bp). Ophiactis lymani formed a single clade with high support in the 16S and COI trees (Figure 4). However, we got a high molecular divergence (p-distance = 8.5) between sequences of the 16S tree (Figure 4A). Our sequence of Ophiactis savignyi was included in a clade formed by western Atlantic sequences from the Caribbean, Florida and Brazil (Figure 4B). The Ophiactis savignyi species complex was formed by multiple lineages with molecular divergence, ranging from 0.0 to 5.4%. In the 16S tree, Ophiothrix (Ophiothrix) angulata was included in the clade of Ophiotrichidae sequences. Our 16S sequence of Ophiocomella ophiactoides formed the sister group of the genus Ophiocoma with high molecular support (Figure 4A). In the COI tree, the resulting topology was a long branch without support inside the Ophiactis clade (data not presented).
Maximum-likelihood trees of the 16S (A) and COI (B) mitochondrial fragments. Parentheses indicate the number of sequences from each location. Values associated with nodes are bootstrap support (1000 replicates) using GTR + G + I (16S) and T92 + G + I (COI) models. Figure at the bottom right represents the localities of sequences (COI) from Ophiactis savignyi.
DISCUSSION
This article is instrumental in updating the records of brittle stars from SPSPA, since only Ophiactis savignyi had been previously recorded (Edwards & Lubbock, Reference Edwards and Lubbock1983a) and in adding new sequences to Genbank that could surrogate future phylogeography investigations. The very low brittle star diversity is probably due to islets isolations and a small area of shallow waters (<50 m) of less than 0.5 km2 (Edwards & Lubbock, Reference Edwards and Lubbock1983b), thereby resulting in reduced habitat heterogeneity.
It is noteworthy that, in contrast to the endemism expected to be found at oceanic islands (MacArthur & Wilson, Reference MacArthur and Wilson1967), and as observed for the reef fishes (Feitoza et al., Reference Feitoza, Rocha, Luiz-Júnior, Floeter and Gasparini2003), molluscs (Oliveira et al., Reference Oliveira, Martins-Silva, Barros, Swoboda, Francisco, Schneider, Batista, Aquino, Vianna, Coutinho and Hazin2009) and sponges (Moraes et al., Reference Moraes, Ventura, Klautau, Hajdu, Muricy, Alves and Castro2006) from SPSPA, all the brittle stars recorded in this study have a global or wide-geographic distribution. However, molecular results showed that we must take care with these results and diversity could be underestimated. Ophiactis savignyi, a complex of species recorded in tropical waters worldwide, has been extensively studied (Clark, Reference Clark1946; Roy & Sponer, Reference Roy and Sponer2002). Commonly found in the fouling communities of harbours and ship hulls, over time this wide distribution has probably been enhanced by anthropogenic influence (Hendler et al., Reference Hendler, Baldwin, Smith and Thacker1999; Paulay et al., Reference Paulay, Kirkendale, Lambert and Meyer2002; Roy & Sponer, Reference Roy and Sponer2002; Hendler & Brugneaux, Reference Hendler and Brugneaux2013). Considering a within-species molecular p-distance ranging from 0 to 2.2% baseline for brittle-star COI-sequence divergence (Ward et al., Reference Ward, Holmes and O'Hara2008), our results revisited the existence of multiple cryptic lineages of Ophiactis savignyi. However, the minimum pairwise distance of 0.0% from SPSPA sequence and available western Atlantic sequences contradicts the idea of endemic genetic lineage in SPSPA. On the other hand, one sequence of Ophiactis lymani diverged by 8.5% from the clade formed by the other two, revealing the existence of two lineages. Ophiactis lymani is a very common amphi-Atlantic brittle star and elucidation requires further molecular analyses. Amphipholis squamata is another example of a complex of species recorded worldwide and commonly found on corals, sponges, algal turf and bryozoan colonies (Boissin et al., Reference Boissin, Féral and Chenuil2008). Amphipholis squamata predominates in the scarce soft substrate of SPSPA, probably by taking advantage of the absence of other common species of coarse sand and rubble, such as species of the genera Ophiophragmus and Microphiopholis.
Despite the fact that our 16S tree is congruent in resolving the position of species sequences in relation to family and genera levels, it is not a probable phylogenetic reconstruction of the families' relationships – that is a subject beyond the scope of our study. The position of Ophiocomidae has a low bootstrap support, Amphiuridae is probably not a sister taxon of Ophionereididae and the position of the long branch of Ophiopeza (Ophiodermatidae) is also probably wrong (see Smith et al., Reference Smith, Paterson and Lafay1995; O'Hara et al., Reference O'Hara, Hugall, Thuy and Moussalli2014). The relationship between Ophiactidae and Ophiotrichidae is well supported by other studies (Smith et al., Reference Smith, Paterson and Lafay1995; O'Hara et al., Reference O'Hara, Hugall, Thuy and Moussalli2014). The relationship between Ophiopholis (Ophiactidae) and Ophiotrichidae was got by Smith et al. (Reference Smith, Paterson and Lafay1995) and our results indicated that Ophiopholis is closer with Ophiotrichidae than Ophiactidae.
Whilst A. squamata and Ophiactis savignyi are cosmopolitan species that occur in the eastern Atlantic, the other three are common brittle stars from the Caribbean, the Gulf of Mexico and north-eastern Brazil. More than 70% of the benthic species of SPSPA included in the analysis of Edwards & Lubbock (Reference Stöhr, O'Hara and Thuy1983b) are exclusively from the western Atlantic. According to them, the transportation of larvae and small organisms from Brazil to SPSPA can passively occur over a period of three to five weeks, time enough for planktonic echinoderm larvae to reach the rocks. For example, the late ophiopluteus stage of Ophiactis savignyi is reached in about 21 days (Mortensen, Reference Mortensen1931). Furthermore, if the proper environmental conditions are not encountered, metamorphosis can be delayed for several more days (Thorson, Reference Thorson1950). Chesher (Reference Chesher1966) suggested that the transportation of echinoid larvae by the UEC from the west to east Atlantic, a trip that would take at least 43 days, 70 at the most, is enough to maintain genetic flow between populations. Our molecular results support the idea of a western Atlantic colonization. The Fernando de Noronha Archipelago, 627 km to the west, is the closest source of potential colonists via UEC. Colonization by juveniles and adults associated with drifting algae is also a very plausible hypothesis (Winston, Reference Winston2012).
The transportation of immigrants from the east Atlantic by the SEC, the prevailing surface current, must be considered for the sea urchin Eucidaris clavata Mortensen, Reference Mortensen1928 and the sea cucumber Holothuria (Halodeima) manningi Pawson, Reference Pawson1978, two further echinoderm species from SPSPA that also occur at Ascension Island, 1940 km off in the south-east Atlantic (Edwards & Lubbock, Reference Hendler, Baldwin, Smith and Thacker1983b). Another hypothesis could be the multiple colonization of SPSPA, which seems to have occurred with the fireworm Eurythoe complanata Pallas, Reference Pallas1766 (Barroso et al., Reference Barroso, Klautau, Solé-Cava and Paiva2010). Edwards & Lubbock (Reference Stöhr, O'Hara and Thuy1983b) suggested that for many species, arrival is only occasional, as exemplified by the single young individual of Eucidaris clavata collected by the Cambridge Expedition. After more than 40 diving-hours, we also found only two individuals. Eucidaris clavata was also seen by other research divers in the past (unpublished data). This shows that even species found at very low densities can commonly reach the rocks and the SPSPA may serve as stepping stones for larval dispersal across the Atlantic. Even so, simple arrival is insufficient to colonize a site. At this point, it is important to highlight that three (Ophiactis lymani, Ophiactis savignyi, Ophiocomella ophiactoides) of the five species of brittle stars recorded in SPSPA are fissiparous, possibly an important mechanism for enhancing population density by cloning individuals.
Fishing boats and vessels have been visiting SPSPA or the surrounding waters for a long time and occasional arrival events mediated by anthropogenic vectors cannot be discharged. However, against this hypothesis, Ophiothela mirabilis Verrill, Reference Verrill1867, a native Pacific species that invaded the Atlantic Ocean during the last decades through the probable association with ship hulls and today occurs along almost the entire Brazilian coast (Hendler et al., Reference Hendler, Migotto, Ventura and Wilk2012), is completely absent in SPSPA.
The records of brittle stars from SPSPA, a rather poor fauna in a small isolated oceanic archipelago, are updated. The list is composed of cosmopolitan species and those with a wide geographic distribution, commonly found along the Brazilian and Caribbean coasts. There are indications that, similar to Ophiactis savignyi, the common amphi-Atlantic brittle star Ophiactis lymani comprises a species complex, but this topic requires future molecular investigations. Data pointed to a prevailing western Atlantic colonization of SPSPA.
ACKNOWLEDGEMENTS
Financial support was provided by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-405411/2012-0) and Brazilian Barcode of Life (MCT/CNPq/FNDCT No. 50/2010). Logistics were supported by the PROARQUIPÉLAGO Program. Authors are grateful to Tatiana S. Leite and Igor Emiliano for providing specimens (CNPq-557157/2009-9). Carlos Alberto de Moura Barboza thanks the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Gustavo Mattos thanks the Fundação de Amparo à Pesquisa do Estado Rio de Janeiro (FAPERJ). We thank two anonymous referees for their valuable comments.
