Accessibility / Report Error

Association between deep-water scale-worms (Annelida: Polynoidae) and black corals (Cnidaria: Antipatharia) in the Southwestern Atlantic

ABSTRACT

Polynoid scale-worms have been found living as commensals with deep-water antipatharians (commonly known as black corals) in the Potiguar Basin, off Rio Grande do Norte State, Northeastern Brazil. In this paper two polychaete species and four black corals species are redescribed. Benhamipolynoe cf. antipathicola and Parahololepidella cf. greeffi, and the black coral Stylopathes adinocrada Opresko, 2006 are recorded for the Southwestern Atlantic. Benhamipolynoe cf. antipathicola was first described from off New Zealand and the Malay Archipelago, as symbiont with the black coral Stylopathes tenuispina (Silberfeld, 1909). It was later reported for the North Atlantic, off Florida, associated with Stylopathes columnaris (Duchassaing, 1870). In our study, B. cf. antipathicola was found in association with the black coral S. adinocrada. Parahololepidella cf. greeffi was first described as a free-living from shallow waters off São Tomé and Cabo Verde Islands, West Africa, and later reported as symbiont with the black coral Tanacetipathes cf. spinescens in the same location. Our data expand both the geographical distribution and the host range of this species which is reported for the first time as symbiont with Tanacetipathes barbadensis (Brook, 1889), T. tanacetum (Pourtalès, 1880) and T. thamnea (Warner, 1981) in Brazil. The aim of this study is to discuss commensal associations between two species of scale-worm polynoids and black corals found in the Southwestern Atlantic, and also reporting their global distribution. Finally, we provided an updated list of the commensal polynoids and their black coral hosts.

KEY WORDS:
Brazil; Hexacorallia; polynoids; South America; symbiosis

INTRODUCTION

Specialized symbiotic associations involving polychaetes are ubiquitous in all oceans (Britayev and Antokhina 2012Britayev TA, Antokhina TI (2012) Symbiotic polychaetes from Nhatrang Bay, Vietnam. In: Britayev TA, Pavlov DS (Eds) Benthic fauna of the Bay of Nhatrang, Southern Vietnam. Moscow, KMK, vol. 2, 11-54.). The Polynoidae, also known as polynoids or scale-worms, includes the largest number and the most commonly reported species living as commensals, representing more than 45% of all known reports of symbiont polychaetes (Martin and Britayev 1998Martin D, Britayev TA (1998) Symbiotic polychaetes: Review of known species. Oceanography and Marine Biology: An Annual Review 36: 217-340., 2018Martin D, Britayev TA (2018) Symbiotic polychaetes revisited: an update of the known species and relationships (1998-2017). Oceanography and Marine Biology: An Annual Review 56: 367-446.). More than 200 species are involved in about 600 relationships, representing about 25% of all known polynoid species (Britayev et al. 2014Britayev TA, Gil J, Altuna Á, Calvo M, Martín D (2014) New symbiotic associations involving polynoids (Polychaeta, Polynoidae) from Atlantic waters, with redescriptions of Parahololepidella greeffi (Augener, 1918) and Gorgoniapolynoe caeciliae (Fauvel, 1913). Memoirs of the Museum Victoria 71: 27-43., Martin and Britayev 2018Martin D, Britayev TA (2018) Symbiotic polychaetes revisited: an update of the known species and relationships (1998-2017). Oceanography and Marine Biology: An Annual Review 56: 367-446., Serpetti et al. 2017Serpetti S, Taylor ML, Green DH, Rogers AD, Paterson GLJ (2017) Ecological adaptations and commensal evolution of the Polynoidae (Polychaeta) in the Southwest Indian Ocean Ridge: A phylogenetic approach. Deep Sea Research Part II: Topical Studies in Oceanography 137: 273-281.).

Polynoids are often found associated with other invertebrates, especially corals, echinoderms, mollusks, and other polychaetes (Pettibone 1991Pettibone MH (1991) Polynoid polychaetes commensal with antipatharian corals. Proceedings of the Biological Society of Washington 104: 714-726., Martin and Britayev 1998Martin D, Britayev TA (1998) Symbiotic polychaetes: Review of known species. Oceanography and Marine Biology: An Annual Review 36: 217-340., 2018Martin D, Britayev TA (2018) Symbiotic polychaetes revisited: an update of the known species and relationships (1998-2017). Oceanography and Marine Biology: An Annual Review 56: 367-446., Eckelbarger et al. 2005Eckelbarger KJ, Watling L, Fournier H (2005) Reproductive biology of the deep-sea polychaete Gorgoniapolynoe caeciliae (Polynoidae), a commensal species associated with octocorals. Journal of the Marine Biological Association of the United Kingdom 85(6): 1425-1433. https://doi.org/10.1017/S0025315405012609
https://doi.org/10.1017/S002531540501260...
). They may either construct their own refuges on the host’s surface or stimulate their hosts to build protective structures around them. Some species may live inside tunnels or gall-like cavities formed by coenenchymal walls of gorgonian or hydrocoral hosts (Martin and Britayev 1998Martin D, Britayev TA (1998) Symbiotic polychaetes: Review of known species. Oceanography and Marine Biology: An Annual Review 36: 217-340., 2018Martin D, Britayev TA (2018) Symbiotic polychaetes revisited: an update of the known species and relationships (1998-2017). Oceanography and Marine Biology: An Annual Review 56: 367-446., Williams and López-González 2005Williams GC, López-González P (2005) A new genus and species of gorgonian octocoral (Anthozoa: Plexauridae) from Antarctic waters. Proceedings of the California Academy of Sciences 56(26): 379-390., Wagner et al. 2012Wagner D, Luck DG, Toonen RJ (2012) The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Advances in Marine Biology 63: 67-132. https://doi.org/10.1016/B978-0-12-394282-1.00002-8
https://doi.org/10.1016/B978-0-12-394282...
).

Cnidarians are known to host abundant and diverse symbiotic fauna, including polychaetes, with records of 281 species of cnidarian hosts involved in 324 relationships with their hosts (Molodtsova et al. 2016Molodtsova T, Britayev TA, Martin D (2016) Cnidarians and their polychaete symbionts. In: Goffredo S, Dubinsky Z (Eds) The Cnidaria, past, present and future. The world of Medusa and her sisters. Switzerland, Springer International Publishing, 387-413.). Antipatharia (Cnidaria: Anthozoa) is the least studied group of corals (Cairns 2007Cairns SD (2007) Deep-water corals: an overview with special reference to diversity and distribution of deep-water scleractinian corals. Bulletin of Marine Science 81(3): 311-322.), particularly in the South Atlantic (Loiola 2007Loiola LL (2007) Black Corals (Cnidaria: Antipatharia) from Brazil: an overview. Conservation and Adaptive Management of Seamount and Deep-Sea Corals Ecosystems. Bulletin of Marine Science 81(Suppl. 1): 253-264.). Their colonies consist of chitinous skeletons covered with numerous tiny spines. Some families have developed close relationships with certain scale worms, forming tunnels by bending and anastomosing its branches or pinnules, providing ideal refuges (Molodtsova and Budaeva 2007Molodtsova T, Budaeva N (2007) Modifications of corallum morphology in black corals as an effect of associated fauna. Bulletin of Marine Science 81: 469-480.). Black corals are generally slow-growing and long-living organisms, generally found in areas with hard substrates, low light levels and strong currents; with longevity ranging from 12 to 4265 years, in Antipathes griggiOpresko, 2009Opresko DM (2009) Antipatharia (Cnidaria) of the Gulf of Mexico. In: Tunnell JW Jr, Felder DL, Earle SA (Eds) Gulf of Mexico origin, waters, and Biota. Corpus Christi, Texas A&M University Press, vol. 1, 359-363., known formerly as Antipathes dichotoma Pallas, 1766, and Leiopathes sp., respectively (Molodtsova and Budaeva 2007Molodtsova T, Budaeva N (2007) Modifications of corallum morphology in black corals as an effect of associated fauna. Bulletin of Marine Science 81: 469-480., Wagner et al. 2012Wagner D, Luck DG, Toonen RJ (2012) The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Advances in Marine Biology 63: 67-132. https://doi.org/10.1016/B978-0-12-394282-1.00002-8
https://doi.org/10.1016/B978-0-12-394282...
, Brugler et al. 2013Brugler MR, Opresko DM, France SC (2013) The evolutionary history of the order Antipatharia (Cnidaria: Anthozoa: Hexacorallia) as inferred from mitochondrial and nuclear DNA: implications for black coral taxonomy and systematics. Zoological Journal of the Linnean Society 169(2): 312-361. https://doi.org/10.1111/zoj.12060
https://doi.org/10.1111/zoj.12060...
). Along with octocorals, antipatharians are habitual hosts not only for polychaetes, but also for a myriad of associated organisms including barnacles, ophiuroids, copepods, crabs, shrimps, anemones, zoanthids, hydroids, crinoids, bryozoans, snails, bivalves, tunicates and fishes (Buhl-Mortensen and Mortensen 2004Buhl-Mortensen L, Mortensen PB (2004) Symbiosis in deep-water corals. Symbiosis 37: 33-61., Wagner et al. 2012Wagner D, Luck DG, Toonen RJ (2012) The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Advances in Marine Biology 63: 67-132. https://doi.org/10.1016/B978-0-12-394282-1.00002-8
https://doi.org/10.1016/B978-0-12-394282...
). The aim of this study is to discuss commensal associations between two species of scale-worm polynoids and black corals found in the Southwestern Atlantic. We redescribe and illustrate the specimens found, also reporting their global distribution and providing an updated list of the commensal polynoids and their black coral hosts.

MATERIAL AND METHODS

The specimens of scale-worms and their antipatharian hosts were collected in the Potiguar Basin, Rio Grande do Norte State, Northeastern Brazil (Fig. 1), by trawling during the surveys of the Program for megafauna characterization of the Potiguar Basin (funded by PETROBRAS), on board of the RV Seward Johnson, between 101 and 461 m depth. Specimens were fixed in a 4% formaldehyde-seawater solution, then rinsed with fresh water and preserved in 70% ethanol. The hosts were observed under a Zeiss stereomicroscope.

Figure 1
Records of association of scale-worm polynoids and black corals from deep-water in South America, Northeastern Brazil: (A) record of Benhamypolynoe cf. antipathicola, and its antipatharian hosts Stylopathes adinocrada in Potiguar Basin; (B) records of association of Parahololepidella cf. greeffi and its antipatharian hosts (Tanacetipathes barbadensis, T. tanacetum and T. thamnea) in Potiguar Basin, Brazil.

Polychaete identifications were based on chaetae, aciculae, and elytra observed under an Olympus BX41 compound microscope. Optical microscope Images were obtained with a Leica M205A. We also provide detailed scanning electron microscope (SEM) images of the parapodial structures and elytra. Measurements are given in mm. The polychaete structures were analyzed according to Pettibone (1989Pettibone MH (1989) A new species of Benhamipolynoe (Polychaeta: Polynoidae: Lepidastheniinae) from Australia, associated with the unattached stylasterid coral Conopora adeta. Proceedings of the Biological Society of Washington 102: 300-304., 1991Pettibone MH (1991) Polynoid polychaetes commensal with antipatharian corals. Proceedings of the Biological Society of Washington 104: 714-726.) and Britayev et al. 2014Britayev TA, Gil J, Altuna Á, Calvo M, Martín D (2014) New symbiotic associations involving polynoids (Polychaeta, Polynoidae) from Atlantic waters, with redescriptions of Parahololepidella greeffi (Augener, 1918) and Gorgoniapolynoe caeciliae (Fauvel, 1913). Memoirs of the Museum Victoria 71: 27-43..

Black corals were identified and described following Loiola and Castro (2005Loiola LL, Castro CB (2005) Tanacetipathes Opresko, 2001 (Cnidaria: Antipatharia: Myriopathidae) from Brazil, including two new species. Zootaxa 1081: 1-31.) and Opresko (2006Opresko DM (2006) Revision of the Antipatharia (Cnidaria: Anthozoa). Part V. Establishment of a new family, Stylopathidae. Zoologische Mededelingen Leiden 80(4): 109-138.), mainly based on pinnule and subpinnule number, order and size, branching pattern, average distance between spines, and subpinnule number per pinnule using a Leica DM 300 compound microscope. Branche microstructures were also illustrated by SEM.

Voucher specimens were deposited in the Museu de Oceanografia Prof. Petrônio Alves Coelho (MOUFPE-CNI), Universidade Federal de Pernambuco, Brazil.

TAXONOMY

An updated list of the polychaetes associated to black corals, including the new records found in our study is presented in Table 1. The symbiotic partnerships found in Potiguar Basin are reported below.

Table 1
List of known polychaete species associated with antipatharian hosts: 1: Pettibone (1970Pettibone MH (1970) Polychaeta Errantia of the Siboga Expedition. Part IV. Some additional polychaetes of the Polynoidae, Hesionidae, Nereidae, Goniadidae, Eunicidae, and Onuphidae, selected as new species by the late Dr. Hermann Augener with remarks on other related species. In: Siboga-Expeditie Uitkomsten op Zoologisch, Bonatisch, Oceanographisch en Geologisch gebied verzameld in Nederlandsch Oost-Indië. Leiden, E.J. Brill, 199-270.), 2: Wagner et al. (2012Wagner D, Luck DG, Toonen RJ (2012) The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Advances in Marine Biology 63: 67-132. https://doi.org/10.1016/B978-0-12-394282-1.00002-8
https://doi.org/10.1016/B978-0-12-394282...
), 3: Britayev et al. (2014Britayev TA, Gil J, Altuna Á, Calvo M, Martín D (2014) New symbiotic associations involving polynoids (Polychaeta, Polynoidae) from Atlantic waters, with redescriptions of Parahololepidella greeffi (Augener, 1918) and Gorgoniapolynoe caeciliae (Fauvel, 1913). Memoirs of the Museum Victoria 71: 27-43.), 4: Pettibone (1991Pettibone MH (1991) Polynoid polychaetes commensal with antipatharian corals. Proceedings of the Biological Society of Washington 104: 714-726.), 5: Martin and Britayev (1998Martin D, Britayev TA (1998) Symbiotic polychaetes: Review of known species. Oceanography and Marine Biology: An Annual Review 36: 217-340.), 6: Hanley and Burke (1991Hanley JR, Burke M (1991) A new genus and species of scaleworm (Polychaeta, Polynoidae) from the Cascade Plateau, Tasman Sea. The Beagle, Records of the Northern Territory Museum of Arts and Sciences 8(1): 97-102.), 7: Barnich et al. (2013Barnich R, Beuck L, Freiwald A (2013) Scale worms (Polychaeta: Aphroditiformia) associated with cold-water corals in the eastern Gulf of Mexico. Journal of the Marine Biological Association of the United Kingdom 93(8): 2129-2143. https://doi.org/10.1017/S002531541300088X
https://doi.org/10.1017/S002531541300088...
), 8: Molodtsova and Budaeva (2007Molodtsova T, Budaeva N (2007) Modifications of corallum morphology in black corals as an effect of associated fauna. Bulletin of Marine Science 81: 469-480.), 9: Hartmann-Schröder and Zibrowius (1998Hartmann-Schröder G, Zibrowius H (1998). Polychaeta associated with Antipatharia (Cnidaria: Anthozoa): description of Polynoidae and Eunicidae. Mitteilungen aus dem Hamburgischen zoologischen Museum und Institut 95: 29-44.), 10: Molodtsova et al. (2016Molodtsova T, Britayev TA, Martin D (2016) Cnidarians and their polychaete symbionts. In: Goffredo S, Dubinsky Z (Eds) The Cnidaria, past, present and future. The world of Medusa and her sisters. Switzerland, Springer International Publishing, 387-413.), 11: Glasby (1994Glasby CJ (1994) A new genus and species of polychaete, Bollandia antipathicola (Nereidoidea: Syllidae), from black coral. Proceedings of the Biological Society of Washington 107(4): 615-621.), O: Obligatory, F: Facultative.

Benhamipolynoe cf. antipaticola and Stylopathes adinocrada

Symbiotic scale-worm

Polynoidae

Benhamipolynoe Petttibone, 1970

Benhamipolynoe cf. antipaticola (Benham, 1927)

Figs 2-7

Lapidasthenia antipaticolaBenham, 1927Benham WB (1927). Polychaeta. British Antarctic ‘Terra Nova’ Expedition Natural History Reports, Zoology 7(2): 47-182.: 7-182, pl. 1-6.

Description. Body brownish, with continuous middorsal longitudinal reddish-brown band, transverse bands from elytra near parapodial bases. Body dorsoventrally flattened, elongate, slender, with nearly parallel sides, tapering posteriorly, subrectangular in cross-section. Seventeen symmetrical pairs of elytra; elytra colorless, transparent with median crescent-shaped dark pigmentation; on elytrophores of segments 2, 4, 5, 7, alternate segments to 29, 32, and 35; elytra continue to middle body, irregularly distributed, may be asymmetrical, with an elytron and cirrus on same segment, or from one to five cirri in succession (Figs 2-3). Elytra lacking fringes, papillae and tubercles, except for some scattered micro-tubercles. Prostomium bilobed, as wide as long, without cephalic peaks; with three antennae and two short, tapering, smooth palps. Ceratophore of median antenna short, cylindrical, inserted in anterior notch of prostomium; lateral antennae inserted terminally or subterminally on anterior part of prostomium, at the same level or slightly ventral to median antenna (without distinct ceratophores); antennae longer than prostomium, tapered, smooth; two pairs of eyes moderate in size; anterior pair on dorsolateral prostomial width, posterior pair near to posterior border. Tentacular segment anterolateral to prostomium, bearing two pairs of long tentacular cirri, upper pairs much longer than lower pairs; basis of tentacular cirri with aciculum, but lacking chaetae. Buccal segment lacking distinct nuchal fold; supporting first pair of dorsal elytra and long ventral buccal cirri (Fig. 4). Parapodia sub-biramous, with small notopodia on anterodorsal lobe; prechaetal lobe quadrangular or subtriangular, postchaetal short and subtriangular, both with acicula. Notopodia short, conical, achaetous acicular lobe. Neuropodia elongate, with a ventral and dorsal deep incision; with subequal, rounded prechaetal and postchaetal lobes (Fig. 5); with 5-11 neurochaetae, rather stout, smooth or with slight indications of spinous rows and falcate tips (Figs 6-7). Ventral cirri short, subulate, extending slightly beyond neuropodial lobe tips. Dorsal cirri with short cylindrical cirrophores; styles smooth, tapering gradually to filiform tips, extending beyond neurochaetae tips. Nephridial papillae short, starting at chaetiger 6 (Fig. 5). Pygidium short, with one pair of long anal cirri.

Figures 2-7
(2) Benhamypolynoe cf. antipathicola on the branches of Stylopathes adinocrada: (3) median chaetigers of B. antipathicola showing elytrophores, elytra and dorsal cirri; (4) head of B. antipathicola showing the prostomium, palps and antennae; (5) posterior chaetigers of B. antipathicola showing the ventral cirrus and neuropodia; (6) neurochaetae from posterior chaetigers, showing a faint serration; (7) detail of distal tip of neurochaetae. (ch) chaetae, (dc) dorsal cirrus, (el) elytra, (et) elytrophore, (ct) cirratophore, (la) lateral antennae; (ma) median antennae, (ne) neuropodium, (pa) parapodium, (pl) palp, (pr) prostomium, (tc) tentacular cirrus. Scale bars: 2-4: 1 mm, 5 = 200 µm, 6 = 100 µm, 7 = 10 µm.

Material examined. A complete specimen with 136 chaetigerous segments, with 103 mm in length, and 4 mm wide. MOUFPE-CNI 113; 04°47’50”S; 036°11’01”W (Potiguar Basin), 423-461 m depth (1 specimen).

Distribution. Pacific: Off New Zealand, 128 m depth (Benham 1927Benham WB (1927). Polychaeta. British Antarctic ‘Terra Nova’ Expedition Natural History Reports, Zoology 7(2): 47-182.), Queensland, Australia, 398 m depth (Pettibone 1989Pettibone MH (1989) A new species of Benhamipolynoe (Polychaeta: Polynoidae: Lepidastheniinae) from Australia, associated with the unattached stylasterid coral Conopora adeta. Proceedings of the Biological Society of Washington 102: 300-304.), off New Caledonia and adjacent waters, French Polynesia, Wallis and Futuna, Solomon Islands, Indonesia, and Madagascar, from 300-600 m depth (Molodtsova and Budaeva 2007Molodtsova T, Budaeva N (2007) Modifications of corallum morphology in black corals as an effect of associated fauna. Bulletin of Marine Science 81: 469-480.), Malay Archipelago; Atlantic: off Key West, Florida, 237 m depth (Pettibone 1970Pettibone MH (1970) Polychaeta Errantia of the Siboga Expedition. Part IV. Some additional polychaetes of the Polynoidae, Hesionidae, Nereidae, Goniadidae, Eunicidae, and Onuphidae, selected as new species by the late Dr. Hermann Augener with remarks on other related species. In: Siboga-Expeditie Uitkomsten op Zoologisch, Bonatisch, Oceanographisch en Geologisch gebied verzameld in Nederlandsch Oost-Indië. Leiden, E.J. Brill, 199-270.) and Northeastern Brazil, 423-461 m depth (present study), first report for the Southwestern Atlantic.

Remarks. Benhamipolynoe antipaticola was originally described as Lapidasthenia antipaticola Benham, 1927Benham WB (1927). Polychaeta. British Antarctic ‘Terra Nova’ Expedition Natural History Reports, Zoology 7(2): 47-182., from 128 m depth off New Zealand, in association with Stylopathes tenuispina (Silberfeld, 1909) (= Parantipathes tenuispina) (Opresko 2006Opresko DM (2006) Revision of the Antipatharia (Cnidaria: Anthozoa). Part V. Establishment of a new family, Stylopathidae. Zoologische Mededelingen Leiden 80(4): 109-138.). The morphological features of the Brazilian specimens agree with the original description, except in the absence of pigmentation in the holotype, according to Pettibone (1989Pettibone MH (1989) A new species of Benhamipolynoe (Polychaeta: Polynoidae: Lepidastheniinae) from Australia, associated with the unattached stylasterid coral Conopora adeta. Proceedings of the Biological Society of Washington 102: 300-304.).

Ecology. Found in association with Stylopathes adinocradaOpresko, 2006Opresko DM (2006) Revision of the Antipatharia (Cnidaria: Anthozoa). Part V. Establishment of a new family, Stylopathidae. Zoologische Mededelingen Leiden 80(4): 109-138., a new host for this species. It is also known to live in association with Stylopathes columnaris (Duchassaing, 1870) (Pettibone 1970Pettibone MH (1970) Polychaeta Errantia of the Siboga Expedition. Part IV. Some additional polychaetes of the Polynoidae, Hesionidae, Nereidae, Goniadidae, Eunicidae, and Onuphidae, selected as new species by the late Dr. Hermann Augener with remarks on other related species. In: Siboga-Expeditie Uitkomsten op Zoologisch, Bonatisch, Oceanographisch en Geologisch gebied verzameld in Nederlandsch Oost-Indië. Leiden, E.J. Brill, 199-270., Britayev et al. 2014Britayev TA, Gil J, Altuna Á, Calvo M, Martín D (2014) New symbiotic associations involving polynoids (Polychaeta, Polynoidae) from Atlantic waters, with redescriptions of Parahololepidella greeffi (Augener, 1918) and Gorgoniapolynoe caeciliae (Fauvel, 1913). Memoirs of the Museum Victoria 71: 27-43.).

Host black coral

Stylopathidae Opresko, 2006Opresko DM (2006) Revision of the Antipatharia (Cnidaria: Anthozoa). Part V. Establishment of a new family, Stylopathidae. Zoologische Mededelingen Leiden 80(4): 109-138.

Stylopathes adinocrada (Opresko, 2006)

Figs 8-10

Antipathes columnaris; Opresko, 1974Opresko DM (1974) A study of the classification of the Antipatharia (Coelenterata: Anthozoa), with redescriptions of eleven species. PhD Thesis, University of Miami, Coral Gables, 194 pp [press in 1994 by University Microfilms, Ann Arbor].: 101-115 (part).

Stylopathes adinocradaOpresko, 2006Opresko DM (2006) Revision of the Antipatharia (Cnidaria: Anthozoa). Part V. Establishment of a new family, Stylopathidae. Zoologische Mededelingen Leiden 80(4): 109-138.: 123.

Description. Colony highly pinnulated, monopodial, 19.5 cm long, with a central formation of fused pinnules forming a “worm run” harboring a polychaete (Figs 8-9). Primary pinnules with subpinnulation and a dense pinnulation pattern, arranged in three rows, 10-20 mm long, with ca. 11 secondary pinnules per posterior primary one. Colonies pinnulated to fourth order. Subpinnules slightly more abundant on abpolypar side of posterior primary pinnules; proximal end of primary pinnules with denser pinnulation pattern. Spines small, 0.024 to 0.06 mm long, arranged in ca. 5 rows in lateral view (Fig. 10), separated ca. 0.28 mm each other within same row. Polyps not seen (lost tissue).

Figures 8-10
(8) Corallum morphology of Stylopathes adinocrada; (9) pinnulation pattern of S. adinocrada, showing the “worm run”; (10) organization of spines in S. adinocrada. Scale bars: 8-9 = 10 mm, 10: 100 µm.

Material examined. MOUFPE-CNI 113; 04°47’50”S; 036°11’01”W (Potiguar Basin), 423-461 m depth (1 colony).

Distribution. Bahamas, 134-708 m depth (Opresko 2006Opresko DM (2006) Revision of the Antipatharia (Cnidaria: Anthozoa). Part V. Establishment of a new family, Stylopathidae. Zoologische Mededelingen Leiden 80(4): 109-138.), Surinam (Opresko 2006Opresko DM (2006) Revision of the Antipatharia (Cnidaria: Anthozoa). Part V. Establishment of a new family, Stylopathidae. Zoologische Mededelingen Leiden 80(4): 109-138.) and northeastern Brazil (423-461 m depth, present study). Stylopathes (as S. columnaris) was known to occur in the coast of the state of Pará (Opresko 1974Opresko DM (1974) A study of the classification of the Antipatharia (Coelenterata: Anthozoa), with redescriptions of eleven species. PhD Thesis, University of Miami, Coral Gables, 194 pp [press in 1994 by University Microfilms, Ann Arbor]., Castro et al. 2006Castro CB, Pires DO, Medeiros MS, Loiola LL, Arantes RCM, Thiago CM, Berman E (2006) Filo Cnidaria. Corais. In: Lavrado HP, Ignacio BL (Eds) Biodiversidade bentônica da região central da Zona Econômica Exclusiva brasileira. Rio de Janeiro, Museu Nacional, 147-192., Opresko 2006Opresko DM (2006) Revision of the Antipatharia (Cnidaria: Anthozoa). Part V. Establishment of a new family, Stylopathidae. Zoologische Mededelingen Leiden 80(4): 109-138.), but this is the first record of S. adinocrada for the Southwestern Atlantic.

Remarks. The studied material resemble the holotype, but was slightly larger, ca. 20 cm versus, ca. 17 cm, respectively. The pinnulation pattern was also similar but the spines were slightly smaller (up to 0.048 mm, rarely 0.06 mm) and more separated within a given row (i.e., up to 0.28 mm versus 0.1-0.2 mm the holotype). The type species of Stylopathes is S. columnaris, but two more species were included within the genus based on two morphotypes erroneously identified as S. columnaris (Opresko 2006Opresko DM (2006) Revision of the Antipatharia (Cnidaria: Anthozoa). Part V. Establishment of a new family, Stylopathidae. Zoologische Mededelingen Leiden 80(4): 109-138.). One of them, S. adinocrada, differs from S. columnaris mainly due to its scattered pinnulation pattern, although in both species the subpinules occur mainly in the distal portion of the primary pinnule, rarely covering the worm run (Opresko 2006Opresko DM (2006) Revision of the Antipatharia (Cnidaria: Anthozoa). Part V. Establishment of a new family, Stylopathidae. Zoologische Mededelingen Leiden 80(4): 109-138.).

Parahololepidella cf. greeffi and Tanacetipathes spp.

Symbiotic scale-worm

Polynoidae Kinberg, 1856

Parahololepidella Pettibone, 1969

Parahololepidella cf. greeffi (Augener, 1918)

Hololepidella greeffiAugener, 1918Augener H (1918) Polychaeta. In: Beiträge zur Kenntnis der Meeresfauna Westafrikas. Hamburg, Herausgegeben von W. Michaelsen, 67-625.: 148, pl. 2, figs 22-24, pl. 3, fig. 52, text-fig. 9.

Hololepidella fageiRullier, 1964Rullier F (1964) Résultats scientifiques des campagnes de la Calypso - Campagne de la Calypso aux îles du Cap Vert (1959) (suite): 5. Annélides polychètes. Annales de l’Institut Océanographique 41(6): 113-218.: 132, fig. 4.

Diagnosis. Body dorsoventrally flattened, elongate, with up to 140 segments (Figs 11-12). Elytra very small, leaving middorsum and parapodia uncovered. Fifty or more pairs of elytra on elytrophores of segments 2, 4, 5, 7, 9, 11, 13, 15, 17, 19, 21, 23, 26, 29, 32, alternating on posterior segments. Prostomium bilobed, with distinct cephalic peaks, and two pairs of large eyes. Ceratophores of median antenna in anterior notch, smooth, tapering, longer than palps. Lateral antennae inserted ventrally to median antenna, smooth, tapering (Fig. 13). Dorsal cirri smooth, with cylindrical long cirrophores (Fig. 15). Parapodia sub-biramous. Notopodia small, digitiform. Neuropodia with longer rounded prechaetal lobe, with subacicular digitiform acicular lobe. Notopodia with reduced number 0-5 notochaetae, unidentate, with faint serration blade (Figs 16-17). Neuropodia with 16-17 notochaetae, unidentate, with faint serration (Fig. 18). Pygidium conical, with two long cirri.

Figures 11-14
(11) Parahololepidella cf. greeffi on the branches of Tanacetipathes tanacetum; (12) median chaetigers of P. greeffi showing elytra and dorsal cirri; (13) head of P. greeffi showing the prostomium, palps and antennae; (14) elytrae from posterior chaetigers of P. cf. greeffi showing a smooth edge. (cp) Cephalic peak, (dc) dorsal cirrus, (el) elytra, (et) elythophore, (la) lateral antennae, (ma) median antennae, (pa) parapodium, (pl) palp, (pr) prostomium, (tc) tentacular cirrus. Scale bars: 11-13 = 1 mm, 14 = 100 µm.

Figures 15-18
(15) Head of P. cf. greeffi showing the prostomium and their structures; (16) Parapodia of P. cf. greeffi showing notochaetae and neurochaetae; (17) Neurochaetae from median chaetigers of P. cf. greeffi; (18) Detail of distal tip of neurochaetae. (ch) Chaetae, (cp) cephalic peak, (la) lateral antennae, (ma) median antennae, (ng) nuchal groove, (pl) palp, (pr) prostomium. Scale bars: 15 = 1 mm, 16-17 = 100 µm, 18 = 10 µm.

For complete description, see Britayev et al. (2014Britayev TA, Gil J, Altuna Á, Calvo M, Martín D (2014) New symbiotic associations involving polynoids (Polychaeta, Polynoidae) from Atlantic waters, with redescriptions of Parahololepidella greeffi (Augener, 1918) and Gorgoniapolynoe caeciliae (Fauvel, 1913). Memoirs of the Museum Victoria 71: 27-43.).

Variability. Our complete specimens varied in number of segments and elytra after chaetiger 23: specimen 1 (33 mm in length, 72 chaetigers, and 44 pairs of elytra), specimen 2 (44 mm in length, 128 chaetigers, and 70 pairs of elytra), specimen 3 (35 mm in length, 68 chaetigers, and 30 pairs of elytra) and specimen 4 (33 mm in length, 65 chaetigers, and 32 pairs of elytra. Our specimens have elytra on posterior most chaetigers.

Material examined. Two complete specimens, four anterior, and three posterior (i.e., mid-posterior body end) fragments, found on the branches of T. barbadensis. MOUFPE-CNI 351, 04°44”31’S, 36°26’19”W, 101-108 m depth (1 specimen from T. tanacetum); MOUFPE-CNI 350, same collection data (2 specimens from T. thamnea). MOUFPE-CNI 349 (same collection data 1 specimens from T. barbadensis).

Distribution. Tropical and Equatorial East Atlantic, Cabo Verde and São Tomé Archipelagos; Western Atlantic Brazil (this paper).

Remarks. Parahololepidella greeffi was originally described as Hololepidella greeffiAugener, 1918Augener H (1918) Polychaeta. In: Beiträge zur Kenntnis der Meeresfauna Westafrikas. Hamburg, Herausgegeben von W. Michaelsen, 67-625., as free-living from shallow waters off São Tomé and Cabo Verde Islands (West Africa). Posteriorly, Pettibone (1969Pettibone MH (1969) The genera Polyeunoa McIntosh, Hololepidella Willey, and three new genera (Polychaeta, Polynoidae). Proceedings of the Biological Society of Washington 82(3): 43-62.) proposed Parahololepidella to include Hololepidella. The morphological features and cryptic color in preserved specimens from Brazil mostly agree with the currently known descriptions (Augener 1918Augener H (1918) Polychaeta. In: Beiträge zur Kenntnis der Meeresfauna Westafrikas. Hamburg, Herausgegeben von W. Michaelsen, 67-625., Hartman 1959Hartman O (1959) Catalogue of the polychaetous Annelids of the World, parts 1-2. Allan Hancock Foundation Publications, Occasional Papers 23: 1-628., Pettibone 1969Pettibone MH (1969) The genera Polyeunoa McIntosh, Hololepidella Willey, and three new genera (Polychaeta, Polynoidae). Proceedings of the Biological Society of Washington 82(3): 43-62.), including the most recent redescription (Britayev et al. 2014Britayev TA, Gil J, Altuna Á, Calvo M, Martín D (2014) New symbiotic associations involving polynoids (Polychaeta, Polynoidae) from Atlantic waters, with redescriptions of Parahololepidella greeffi (Augener, 1918) and Gorgoniapolynoe caeciliae (Fauvel, 1913). Memoirs of the Museum Victoria 71: 27-43.), but elytra are present till the end of the body.

Ecology. Parahololepidella cf. greeffi was first reported as a symbiont by Britayev et al. (2014Britayev TA, Gil J, Altuna Á, Calvo M, Martín D (2014) New symbiotic associations involving polynoids (Polychaeta, Polynoidae) from Atlantic waters, with redescriptions of Parahololepidella greeffi (Augener, 1918) and Gorgoniapolynoe caeciliae (Fauvel, 1913). Memoirs of the Museum Victoria 71: 27-43.), living in association with Tanacetipathes cf. spinescens (Gray, 1857) (= Antipathes spinescens) (Opresko 2001Opresko DM (2001) Revision of the Antipatharia (Cnidaria: Anthozoa). Part I. Establishment of a new family, Myriopathidae. Zoologische Mededelingen Leiden 75(17): 343-370.). Our results confirm the commensal character of the species, which appears to be a polyxenous black coral symbiont as, in addition to T. cf. spinescens it also lives in association T. tanacetum, T. barbadensis and T. thamnea. Tanacetipathes tanacetum has also been found too harbor Antipathipolyeunoa nuttingiPettibone, 1991Pettibone MH (1991) Polynoid polychaetes commensal with antipatharian corals. Proceedings of the Biological Society of Washington 104: 714-726. for in North Atlantic Ocean and Caribbean Sea (i.e., Barbados) locations (Pettibone 1991Pettibone MH (1991) Polynoid polychaetes commensal with antipatharian corals. Proceedings of the Biological Society of Washington 104: 714-726., Molodtsova and Budaeva 2007Molodtsova T, Budaeva N (2007) Modifications of corallum morphology in black corals as an effect of associated fauna. Bulletin of Marine Science 81: 469-480.).

Host black corals

Myriopathidae Opresko, 2001Opresko DM (2001) Revision of the Antipatharia (Cnidaria: Anthozoa). Part I. Establishment of a new family, Myriopathidae. Zoologische Mededelingen Leiden 75(17): 343-370.

Tanacetipathes Opresko, 2001Opresko DM (2001) Revision of the Antipatharia (Cnidaria: Anthozoa). Part I. Establishment of a new family, Myriopathidae. Zoologische Mededelingen Leiden 75(17): 343-370.

Tanacetipathes tanacetum (Pourtalès, 1880)

Figs 19-21

Antipathes tanacetumPourtalès, 1880Pourtalès LF de (1880) Zoological results of the “Blake” expedition to the Caribbean Sea. Bulletin of the Museum of Comparative Zoology Havard 6(4): 113-118.: 116, pl. 3, fig. 13.

Description. Corallum monopodial, with branches rarely up to 2nd order, in bottlebrush pattern, and primary pinnules usually in 4 main rows (Fig. 19). Primary posterior pinnules larger than primary anterior pinnules, 6-20 mm long, varying according to colony size. Anterior primary pinnules 5-7 mm long, cycle separated by ca. 1 mm. Angle between posterior and anterior primary pinnules (polypolar and abpolypar sides, respectively) of ca. 45°. Angle between two anterior or two posterior primary pinnules (polypar/polypar sides or abpolypar/abpolypar, respectively) of ca. 160°. Secondary pinnules scarce, 3 - 7 (more common 4 - 5), usually near proximal end of posterior primary pinnules (Fig. 20). Tertiary pinnule rarely present, usually 1 or 2 per secondary pinnule when present. Spines with few ornaments, conical (Fig. 21). Polypar spines 0.048-0.1 mm long, separated by 0.12-0.18 mm. Abpolypar spines 0.036-0.06 mm long. Polyps not seen (lost tissue).

Figures 19-21
(19) Corallum morphology of Tanacetipathes tanacetum; (20) cross section showing pinnules cycle of T. tanacetum; (21) organization of spines in T. tanacetum. Sacale bars: 19, 20 = 1 cm, 21 = 200 μm.

Material examined. MOUFPE-CNI 351, 04°44”31’S; 36°26’19”W, 101-108 m (Potiguar Basin).

Distribution. Bermuda (Cairns et al. 1986Cairns SD, Hartog JC, Arneson C (1986) Marine fauna and flora of Bermuda. In: Sterrer W (Ed.) Marine fauna and flora of Bermuda: A systematic guide to the identification of marine organisms. New York, Wiley-Interscience Publications, 159-194.), Gulf of Mexico, Potiguar Basin (present study) and southern coast of Brazil (Pérez et al. 2005Pérez CD, Vila-Nova DA, Santos AM (2005) Associated community with the zoanthid Palythoa caribaeorum (Duchassaing & Michelotti, 1860) (Cnidaria, Anthozoa) from littoral of Pernambuco, Brazil. Hydrobiology 548: 207-215., Opresko 2009Opresko DM (2009) Antipatharia (Cnidaria) of the Gulf of Mexico. In: Tunnell JW Jr, Felder DL, Earle SA (Eds) Gulf of Mexico origin, waters, and Biota. Corpus Christi, Texas A&M University Press, vol. 1, 359-363.) 50 to 108 m. This is the first record for the Potiguar Basin, northeast Brazil.

Remarks. The lectotype of T. tanacetum designated by Pérez et al. (2005Pérez CD, Vila-Nova DA, Santos AM (2005) Associated community with the zoanthid Palythoa caribaeorum (Duchassaing & Michelotti, 1860) (Cnidaria, Anthozoa) from littoral of Pernambuco, Brazil. Hydrobiology 548: 207-215.) has posterior primary pinnules 1.2 cm long versus the 2 cm of the Potiguar Basin material, which also lack the characteristic curved back pinnules of the lectotype. Nevertheless, not all specimens have these pinnules (Pérez et al. 2005Pérez CD, Costa DL, Opresko DM (2005) A new species of Tanacetipathes from Brazil, with a redescription of the type species T. tanacetum (Pourtalès) (Cnidaria, Anthozoa, Antipatharia). Zootaxa 890: 1-12.). Our specimens resemble those from off Bahia, northeastern Brazil, which had polypar spines 0.04-0.27 mm long (Loiola and Castro 2005Loiola LL, Castro CB (2005) Tanacetipathes Opresko, 2001 (Cnidaria: Antipatharia: Myriopathidae) from Brazil, including two new species. Zootaxa 1081: 1-31.), in agreement with the 0.13 to 0.3 mm reported by Opresko and Sanchez (2005Opresko DM, Sanchez JA (2005) Caribbean Shallow-water Black Corals (Cnidaria: Anthozoa: Antipatharia). Caribbean Journal of Science 41(3): 492-507.). In contrast, our colonies showed polypar spines 0.048-0.1 mm long, similar to those of the specimens from Bahia (Loiola and Castro 2005Loiola LL, Castro CB (2005) Tanacetipathes Opresko, 2001 (Cnidaria: Antipatharia: Myriopathidae) from Brazil, including two new species. Zootaxa 1081: 1-31.). The original description emphasizes the presence of a “parasitic worm” similar to that occurring in S. columnaris, but which did not produced changes in host growth (Pourtalès 1880Pourtalès LF de (1880) Zoological results of the “Blake” expedition to the Caribbean Sea. Bulletin of the Museum of Comparative Zoology Havard 6(4): 113-118.). The symbiotic worm was described as Antipathipolyeunoa nuttingiPettibone, 1991Pettibone MH (1991) Polynoid polychaetes commensal with antipatharian corals. Proceedings of the Biological Society of Washington 104: 714-726. in a paper that also provided an identification key based primarily on the associated species of black corals.

Tanacetipathes barbadensis (Brook, 1889)

Figs 22-27

Aphanipathes barbadensisBrook, 1889Brook G (1889) Report on the Antipatharia collected by HMS Challenger during the years 1873-1876. Report of the scientific results of the voyage of the HMS “Challenger”. Zoology 32: 1-222.: 128, pl. II, fig. 10; pl. XI, fig. 4.

Description. Corallum monopodial or branched up to the first order with branches emerging close to base (Fig. 22). Colonies in bottlebrush pattern, with primary pinnules mainly arranged in four rows, reaching up to 6 rows. Secondary pinnules inclined towards distal end of primary posterior pinnule; anterior primary pinnules rarely with subpinnulation. 1-4 (more commonly 2-3) long secondary pinnule per posterior primary, usually at proximal end of primary pinnule (Fig. 23). No more than three tertiary pinnules, when present, near proximal end of secondary pinnule. Posterior primary pinnules 10-26 mm long. Anterior primary pinnules 3-12 mm long. Secondary pinnules 2-12 mm long (more commonly 6 mm). Smooth, conical spines, arranged in 5 to 6 rows visible under optical microscope (Fig. 26). Polypar spines 0.084-0.216 mm long (more commonly 0.144 mm). Abpolypar spines 0.048-0.084 mm long. Distance between spines mostly 0.12-0.18 mm, with ca. four spines per mm in each row. Polyps not seen (lost tissue).

Figures 22-27
(22) Corallum morphology of Tanacetipathes barbadensis; (23) cross section showing pinnules cycle of T. barbadensis; (24) organization of spines in T. barbadensis; (25) corallum morphology of Tanacetipathes thamnea; (26) cross section showing pinnules cycle of T. thamnea; (27) organization of spines in T. thamnea. Scale bars: 22, 23, 25, 26 = 1 cm, 24 = 200 μm, 27 = 150 μm.

Material examined. MOUFPE-CNI 349, 04°44”31’S; 36°26’ 19”W, 101-108 m (Potiguar Basin).

Distribution. Barbados (Brook 1889Brook G (1889) Report on the Antipatharia collected by HMS Challenger during the years 1873-1876. Report of the scientific results of the voyage of the HMS “Challenger”. Zoology 32: 1-222.); Ship Mouth, NW Trinidad (Warner 1981Warner GF (1981) Species descriptions and ecological observations of black corals. (Antipatharia) from Trinidad. Bulletin of Marine Science 31(1): 147-163.); Gulf of México (Opresko 2009Opresko DM (2009) Antipatharia (Cnidaria) of the Gulf of Mexico. In: Tunnell JW Jr, Felder DL, Earle SA (Eds) Gulf of Mexico origin, waters, and Biota. Corpus Christi, Texas A&M University Press, vol. 1, 359-363.), Brazilian coast, from Potiguar Basin, RN (present study) to the Abrolhos Bank (Loiola and Castro 2005Loiola LL, Castro CB (2005) Tanacetipathes Opresko, 2001 (Cnidaria: Antipatharia: Myriopathidae) from Brazil, including two new species. Zootaxa 1081: 1-31.), 30 to 108 m depth.

Remarks. Tanacetipathes barbadensis ressembles T. tanacetum (Pourtalès, 1880Pourtalès LF de (1880) Zoological results of the “Blake” expedition to the Caribbean Sea. Bulletin of the Museum of Comparative Zoology Havard 6(4): 113-118.), but differs in having three or less secondary pinnules per subsequent primary pinnule (instead of 3-7 in T. tanacetum). Our specimens show posterior pinnules smaller than those previously reported for the species, up to 30 mm long versus 60 mm in Opresko and Sanchez (2005Opresko DM, Sanchez JA (2005) Caribbean Shallow-water Black Corals (Cnidaria: Anthozoa: Antipatharia). Caribbean Journal of Science 41(3): 492-507.), while agreeing with those described by Brook (1889Brook G (1889) Report on the Antipatharia collected by HMS Challenger during the years 1873-1876. Report of the scientific results of the voyage of the HMS “Challenger”. Zoology 32: 1-222.) and Loiola and Castro (2005Loiola LL, Castro CB (2005) Tanacetipathes Opresko, 2001 (Cnidaria: Antipatharia: Myriopathidae) from Brazil, including two new species. Zootaxa 1081: 1-31.). The latter, also from the Brazilian continental shelf, presented posterior primary pinnules up to 45 mm long. Therefore, we suggest that the presence of small sized pinnules may be an intraspecific variation typical of Brazilian populations.

Tanacetipathes thamnea (Warner, 1981)

Figs 25-27

Antipathes thamneaWarner, 1981Warner GF (1981) Species descriptions and ecological observations of black corals. (Antipatharia) from Trinidad. Bulletin of Marine Science 31(1): 147-163.: 148-151, figs. 2-4.

Tanacetipathes paula Perez, Costa and Opresko, 2005Pérez CD, Vila-Nova DA, Santos AM (2005) Associated community with the zoanthid Palythoa caribaeorum (Duchassaing & Michelotti, 1860) (Cnidaria, Anthozoa) from littoral of Pernambuco, Brazil. Hydrobiology 548: 207-215.: 8-12, figs 5-8.

Description. Colonies 8-25 cm long, in bottlebrush pattern, monopodial, with branches absent or branching to second order, near colony base (Fig. 25). Primary pinnules usually arranged in four rows. Primary posterior pinnules 10-18 mm long (more common 14-16 mm), larger than the anterior ones (3-12 mm long, varying in juvenile colonies). Secondary pinnules tipping toward distal end of primary pinnule. 7-20 (more commonly 10-15) secondary pinnules per posterior primary pinnule (Fig. 26), 2-12 mm long. Tertiary pinnules scarce, usually more abundant on abpolipar side of posterior primary pinnule, 1-4 per posterior secondary pinnule. Angle between posterior and anterior primary pinnule (polypar and abpolypar sides, respectively) 55º-70°. Angle between two anterior or two posterior primary pinnules (polypar/polypar sides or abpolypar/abpolypar, respectively) 115-130°. Abpolypar side of posterior primary pinnules with more secondary pinnules than polypar side. Spines smooth, with few ornaments, slightly inclined toward distal end of pinnule or branch (Fig. 27). Distance between spines mainly 0.12-0.18 mm. Polypar spines 0.1-0.2 mm long; Abpolypar spines 0.036-0.084 mm long. Polyps not seen (lost tissue).

Material examined. MOUFPE-CNI 350, 04°44”31’S; 36°26’ 19”W, 101-108 m (Potiguar Basin).

Distribution. Boca de Navios, NW Trinidad (Warner 1981Warner GF (1981) Species descriptions and ecological observations of black corals. (Antipatharia) from Trinidad. Bulletin of Marine Science 31(1): 147-163.), Gulf of México (Opresko 2009Opresko DM (2009) Antipatharia (Cnidaria) of the Gulf of Mexico. In: Tunnell JW Jr, Felder DL, Earle SA (Eds) Gulf of Mexico origin, waters, and Biota. Corpus Christi, Texas A&M University Press, vol. 1, 359-363.), and Brazilian coast (Loiola and Castro 2005Loiola LL, Castro CB (2005) Tanacetipathes Opresko, 2001 (Cnidaria: Antipatharia: Myriopathidae) from Brazil, including two new species. Zootaxa 1081: 1-31., present study), 30 to 108 m depth. This is the first record of the species for the Potiguar Basin, Brazil.

Remarks. Our specimens differ from the syntype described by Warner (1981Warner GF (1981) Species descriptions and ecological observations of black corals. (Antipatharia) from Trinidad. Bulletin of Marine Science 31(1): 147-163.) in some characters. They were slightly shorter (up to 25 cm long versus 20-40 cm long). Some colonies had posterior primary pinnules more elongated and with more secondary pinnules than that described by Loiola and Castro (2005Loiola LL, Castro CB (2005) Tanacetipathes Opresko, 2001 (Cnidaria: Antipatharia: Myriopathidae) from Brazil, including two new species. Zootaxa 1081: 1-31.). Warner (1981Warner GF (1981) Species descriptions and ecological observations of black corals. (Antipatharia) from Trinidad. Bulletin of Marine Science 31(1): 147-163.) also noted that there may be 5-10 secondary pinnules per posterior primary in a10 mm primary pinnule, considering that a pinnule may reach up to 25 mm. Moreover, Loiola and Castro (2005Loiola LL, Castro CB (2005) Tanacetipathes Opresko, 2001 (Cnidaria: Antipatharia: Myriopathidae) from Brazil, including two new species. Zootaxa 1081: 1-31.) found 1-2 tertiary posterior pinnules per posterior secondary whereas our specimens had 1-4. Also, Warner (1981Warner GF (1981) Species descriptions and ecological observations of black corals. (Antipatharia) from Trinidad. Bulletin of Marine Science 31(1): 147-163.) mentioned a few distally inclined tertiary pinnules. Outnumber primary pinnules may occur especially in the more distal regions of the colonies as well as in larger colonies. Warner (1981Warner GF (1981) Species descriptions and ecological observations of black corals. (Antipatharia) from Trinidad. Bulletin of Marine Science 31(1): 147-163.) mentioned the presence of errant polychaetes in almost all colonies, living in a kind of tube formed by pinnules on the side of the colony turned toward the sea current.

DISCUSSION

Many authors have reported symbiotic relationships involving black corals since the 19th century, although most records were observations limited to strictly taxonomic papers (Brook 1889Brook G (1889) Report on the Antipatharia collected by HMS Challenger during the years 1873-1876. Report of the scientific results of the voyage of the HMS “Challenger”. Zoology 32: 1-222., Van Pesch 1914Van Pesch AJ (1914) The Antipatharia of the Siboga Expeditie. Monographe 17: 1-258., Pourtalès 1874Pourtalès LF de (1874) Crinoids and Corals. Zoological results of the “Hassler” Expedition. - Ill. Catalogue of the Museum of Comparative of Zoology, Harvard, 8: 25-50.) and the symbiotic polychaetes, especially the Polynoidae, were not an exception (Beneden 1869Beneden PJ (1869) Le commensalisme dans le règne animal. Bulletin de l’Académie royale de Belgique, Série 2, 28: 621-648., Paris 1955Paris J (1955) Commensalisme et parasitisme chez les annélides polychètes. Vie et Milieu 6: 525-536., Britayev 1989Britayev TA (1989) The symbiotic polychaetes: morphology, ecology and distribution. In: Sveshnicov VA (Ed.) Symbiosis among marine animals. Moscow, A.N. Severtzov Institute, Russian Academy of Sciences, 60-74., Martin and Britayev 1998Martin D, Britayev TA (1998) Symbiotic polychaetes: Review of known species. Oceanography and Marine Biology: An Annual Review 36: 217-340.). The paucity of ecological information was strongly related to the difficultness of conducting observational studies in deep seas, but also to the low number of taxonomists with expertise in Antipatharia (Cairns 2007Cairns SD (2007) Deep-water corals: an overview with special reference to diversity and distribution of deep-water scleractinian corals. Bulletin of Marine Science 81(3): 311-322.).

Black corals are key-species in deep-sea habitats, from sheltering quirky communities of microorganisms to nesting centers for several fish species (Tazioli et al. 2007Tazioli S, Bo M, Boyer M, Rotinsulu H, Bavestrello G (2007) Ecological observations of some common antipatharian corals in the marine park of Bunaken (North Sulawesi, Indonesia). Zoological Studies 46: 227-241., Wagner et al. 2012Wagner D, Luck DG, Toonen RJ (2012) The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Advances in Marine Biology 63: 67-132. https://doi.org/10.1016/B978-0-12-394282-1.00002-8
https://doi.org/10.1016/B978-0-12-394282...
). Some decapod crustaceans, for example, house on black coral colonies to acquire a better position in the water column for filter-feeding (Wagner et al. 2012Wagner D, Luck DG, Toonen RJ (2012) The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Advances in Marine Biology 63: 67-132. https://doi.org/10.1016/B978-0-12-394282-1.00002-8
https://doi.org/10.1016/B978-0-12-394282...
).

Molodtsova et al. (2016Molodtsova T, Britayev TA, Martin D (2016) Cnidarians and their polychaete symbionts. In: Goffredo S, Dubinsky Z (Eds) The Cnidaria, past, present and future. The world of Medusa and her sisters. Switzerland, Springer International Publishing, 387-413.) listed around 19 black coral species hosting 14 species of symbiotic polychaetes worldwide, with the Polynoidae being the most diverse polychaete family associated with antipatharians, but also with gorgonians.

In many cases, the polychaetes associated with Tanacetipathes and Stylopathes changed the coral growth and caused modifications in specific morphological characters (Pettibone 1989Pettibone MH (1989) A new species of Benhamipolynoe (Polychaeta: Polynoidae: Lepidastheniinae) from Australia, associated with the unattached stylasterid coral Conopora adeta. Proceedings of the Biological Society of Washington 102: 300-304., 1991Pettibone MH (1991) Polynoid polychaetes commensal with antipatharian corals. Proceedings of the Biological Society of Washington 104: 714-726., Molodtsova and Budaeva 2007Molodtsova T, Budaeva N (2007) Modifications of corallum morphology in black corals as an effect of associated fauna. Bulletin of Marine Science 81: 469-480., Wagner et al. 2012Wagner D, Luck DG, Toonen RJ (2012) The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Advances in Marine Biology 63: 67-132. https://doi.org/10.1016/B978-0-12-394282-1.00002-8
https://doi.org/10.1016/B978-0-12-394282...
). Therefore, some taxonomically important morphological traits must be addressed with caution in antipatharians affected by symbiotic associations (Molodtsova and Budaeva 2007Molodtsova T, Budaeva N (2007) Modifications of corallum morphology in black corals as an effect of associated fauna. Bulletin of Marine Science 81: 469-480.). The unbranched monopodial form in the examined colonies might be a physiological reaction of antipatharians to symbiotic polychaetes, as suggested by Molodtsova and Budaeva (2007Molodtsova T, Budaeva N (2007) Modifications of corallum morphology in black corals as an effect of associated fauna. Bulletin of Marine Science 81: 469-480.).

In this study, most polychaetes associated with Tanacetipathes spp. were found on the main axis of the corallum, screwing on the secondary pinnules in the posterior side of black coral. In contrast, the polychaete associated with S. adinocrada was found inside a “worm run” formed by anastomosed secondary pinnules along the corallum main axis, typical of the genus.

Indo-Pacific and Northern Atlantic species of Stylopathes have been reported with B. antipathicola as obligatory commensals (Wagner et al. 2012Wagner D, Luck DG, Toonen RJ (2012) The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Advances in Marine Biology 63: 67-132. https://doi.org/10.1016/B978-0-12-394282-1.00002-8
https://doi.org/10.1016/B978-0-12-394282...
). Although our data are insufficient to suggest coevolution, it is worth noting that the same relationship with Stylopathes seems to occur in two distinct ocean basins separated long ago. Since there is strong molecu lar evidence of vicariant speciation in deep-sea corals and polynoids between Pacific and Atlantic basins (e.g., Quattrini et al. 2013Quattrini AM, Georgian SE, Byrnes L, Stevens A, Falco R, Cordes EE (2013) Niche divergence by deep-sea octocorals in the genus Callogorgia across the continental slope of the Gulf of Mexico. Molecular Ecology 22: 4123-4140. https://doi.org/10.1111/mec.12370
https://doi.org/10.1111/mec.12370...
, Serpetti et al. 2017Serpetti S, Taylor ML, Green DH, Rogers AD, Paterson GLJ (2017) Ecological adaptations and commensal evolution of the Polynoidae (Polychaeta) in the Southwest Indian Ocean Ridge: A phylogenetic approach. Deep Sea Research Part II: Topical Studies in Oceanography 137: 273-281.), the coevolution hypothesis deserves testing, particularly because the existence of cryptic diversity in B. antipathicola cannot be discarded. The morphological differences between specimens from the two basins seems to support the idea that they correspond to different taxa. However, more careful morphological studies based on new materials, in parallel with molecular studies, is certainly needed to clarify the situation of these populations living in association with deep-water corals.

We have recorded Parahololepidella cf. greeffi living as commensal with three species of Tanacetipathes: T. thamnea, T. barbadensis and T. tanacetum, which represents a new modification of the ecological status of the species, from free living to monoxenous symbiont in Britayev et al. (2014Britayev TA, Gil J, Altuna Á, Calvo M, Martín D (2014) New symbiotic associations involving polynoids (Polychaeta, Polynoidae) from Atlantic waters, with redescriptions of Parahololepidella greeffi (Augener, 1918) and Gorgoniapolynoe caeciliae (Fauvel, 1913). Memoirs of the Museum Victoria 71: 27-43.) to polyxenous symbiont according to our data. Our results also confirm that the worms did not cause drastic modifications to their hosts.

All 300 antipatharians from Myriopathidae and Antipathidae, collected in 75 Indo-Pacific stations showed symbiotic relationships with polynoid and eunicid polychaetes, inclu ding B. antipathicola forming latticed tunnels on S. columnaris (Molodtsova and Budaeva 2007Molodtsova T, Budaeva N (2007) Modifications of corallum morphology in black corals as an effect of associated fauna. Bulletin of Marine Science 81: 469-480.). The tube was initially secreted by the polychaete and subsequently structured by anastomosis of pinules along the central axis of the colony. The same phenomenon was observed in our samples. Molodtsova and Budaeva (2007Molodtsova T, Budaeva N (2007) Modifications of corallum morphology in black corals as an effect of associated fauna. Bulletin of Marine Science 81: 469-480.) also examined Caribbean samples of Tanacetipathes (T. spinences) with P. greeffi as symbiont of the colonies. In these case, corals also present anastomosed secondary pinules but, as in the Brazilian material, they did not form exactly a “worm run”.

ACKNOWLEDGMENTS

We thank Daniel Martin (Centre d’Estudis Avançats de Blanes - CEAB/CSIC), Temir Britayev (Severtsov Institute of Ecology and Evolution RAS, Moscow, Russia), and the anonymous referees for suggestions to improve this manuscript. We heartily thank Paulo Lana (UFPR) for his suggestions to improve the manuscript. We also acknowledge Fundação de Amparo a Ciência e Tecnologia de Pernambuco for a post-doctoral scholarship to J.E. De Assis (DCR-0086-2.04/13).

LITERATURE CITED

  • Augener H (1918) Polychaeta. In: Beiträge zur Kenntnis der Meeresfauna Westafrikas. Hamburg, Herausgegeben von W. Michaelsen, 67-625.
  • Barnich R, Beuck L, Freiwald A (2013) Scale worms (Polychaeta: Aphroditiformia) associated with cold-water corals in the eastern Gulf of Mexico. Journal of the Marine Biological Association of the United Kingdom 93(8): 2129-2143. https://doi.org/10.1017/S002531541300088X
    » https://doi.org/10.1017/S002531541300088X
  • Beneden PJ (1869) Le commensalisme dans le règne animal. Bulletin de l’Académie royale de Belgique, Série 2, 28: 621-648.
  • Benham WB (1927). Polychaeta. British Antarctic ‘Terra Nova’ Expedition Natural History Reports, Zoology 7(2): 47-182.
  • Britayev TA (1989) The symbiotic polychaetes: morphology, ecology and distribution. In: Sveshnicov VA (Ed.) Symbiosis among marine animals. Moscow, A.N. Severtzov Institute, Russian Academy of Sciences, 60-74.
  • Britayev TA, Antokhina TI (2012) Symbiotic polychaetes from Nhatrang Bay, Vietnam. In: Britayev TA, Pavlov DS (Eds) Benthic fauna of the Bay of Nhatrang, Southern Vietnam. Moscow, KMK, vol. 2, 11-54.
  • Britayev TA, Gil J, Altuna Á, Calvo M, Martín D (2014) New symbiotic associations involving polynoids (Polychaeta, Polynoidae) from Atlantic waters, with redescriptions of Parahololepidella greeffi (Augener, 1918) and Gorgoniapolynoe caeciliae (Fauvel, 1913). Memoirs of the Museum Victoria 71: 27-43.
  • Brook G (1889) Report on the Antipatharia collected by HMS Challenger during the years 1873-1876. Report of the scientific results of the voyage of the HMS “Challenger”. Zoology 32: 1-222.
  • Brugler MR, Opresko DM, France SC (2013) The evolutionary history of the order Antipatharia (Cnidaria: Anthozoa: Hexacorallia) as inferred from mitochondrial and nuclear DNA: implications for black coral taxonomy and systematics. Zoological Journal of the Linnean Society 169(2): 312-361. https://doi.org/10.1111/zoj.12060
    » https://doi.org/10.1111/zoj.12060
  • Buhl-Mortensen L, Mortensen PB (2004) Symbiosis in deep-water corals. Symbiosis 37: 33-61.
  • Cairns SD (2007) Deep-water corals: an overview with special reference to diversity and distribution of deep-water scleractinian corals. Bulletin of Marine Science 81(3): 311-322.
  • Cairns SD, Hartog JC, Arneson C (1986) Marine fauna and flora of Bermuda. In: Sterrer W (Ed.) Marine fauna and flora of Bermuda: A systematic guide to the identification of marine organisms. New York, Wiley-Interscience Publications, 159-194.
  • Castro CB, Pires DO, Medeiros MS, Loiola LL, Arantes RCM, Thiago CM, Berman E (2006) Filo Cnidaria. Corais. In: Lavrado HP, Ignacio BL (Eds) Biodiversidade bentônica da região central da Zona Econômica Exclusiva brasileira. Rio de Janeiro, Museu Nacional, 147-192.
  • Eckelbarger KJ, Watling L, Fournier H (2005) Reproductive biology of the deep-sea polychaete Gorgoniapolynoe caeciliae (Polynoidae), a commensal species associated with octocorals. Journal of the Marine Biological Association of the United Kingdom 85(6): 1425-1433. https://doi.org/10.1017/S0025315405012609
    » https://doi.org/10.1017/S0025315405012609
  • Glasby CJ (1994) A new genus and species of polychaete, Bollandia antipathicola (Nereidoidea: Syllidae), from black coral. Proceedings of the Biological Society of Washington 107(4): 615-621.
  • Hanley JR, Burke M (1991) A new genus and species of scaleworm (Polychaeta, Polynoidae) from the Cascade Plateau, Tasman Sea. The Beagle, Records of the Northern Territory Museum of Arts and Sciences 8(1): 97-102.
  • Hartman O (1959) Catalogue of the polychaetous Annelids of the World, parts 1-2. Allan Hancock Foundation Publications, Occasional Papers 23: 1-628.
  • Hartmann-Schröder G, Zibrowius H (1998). Polychaeta associated with Antipatharia (Cnidaria: Anthozoa): description of Polynoidae and Eunicidae. Mitteilungen aus dem Hamburgischen zoologischen Museum und Institut 95: 29-44.
  • Loiola LL (2007) Black Corals (Cnidaria: Antipatharia) from Brazil: an overview. Conservation and Adaptive Management of Seamount and Deep-Sea Corals Ecosystems. Bulletin of Marine Science 81(Suppl. 1): 253-264.
  • Loiola LL, Castro CB (2005) Tanacetipathes Opresko, 2001 (Cnidaria: Antipatharia: Myriopathidae) from Brazil, including two new species. Zootaxa 1081: 1-31.
  • Martin D, Britayev TA (1998) Symbiotic polychaetes: Review of known species. Oceanography and Marine Biology: An Annual Review 36: 217-340.
  • Martin D, Britayev TA (2018) Symbiotic polychaetes revisited: an update of the known species and relationships (1998-2017). Oceanography and Marine Biology: An Annual Review 56: 367-446.
  • Molodtsova T, Britayev TA, Martin D (2016) Cnidarians and their polychaete symbionts. In: Goffredo S, Dubinsky Z (Eds) The Cnidaria, past, present and future. The world of Medusa and her sisters. Switzerland, Springer International Publishing, 387-413.
  • Molodtsova T, Budaeva N (2007) Modifications of corallum morphology in black corals as an effect of associated fauna. Bulletin of Marine Science 81: 469-480.
  • Opresko DM (1974) A study of the classification of the Antipatharia (Coelenterata: Anthozoa), with redescriptions of eleven species. PhD Thesis, University of Miami, Coral Gables, 194 pp [press in 1994 by University Microfilms, Ann Arbor].
  • Opresko DM (2001) Revision of the Antipatharia (Cnidaria: Anthozoa). Part I. Establishment of a new family, Myriopathidae. Zoologische Mededelingen Leiden 75(17): 343-370.
  • Opresko DM (2006) Revision of the Antipatharia (Cnidaria: Anthozoa). Part V. Establishment of a new family, Stylopathidae. Zoologische Mededelingen Leiden 80(4): 109-138.
  • Opresko DM (2009) Antipatharia (Cnidaria) of the Gulf of Mexico. In: Tunnell JW Jr, Felder DL, Earle SA (Eds) Gulf of Mexico origin, waters, and Biota. Corpus Christi, Texas A&M University Press, vol. 1, 359-363.
  • Opresko DM, Sanchez JA (2005) Caribbean Shallow-water Black Corals (Cnidaria: Anthozoa: Antipatharia). Caribbean Journal of Science 41(3): 492-507.
  • Paris J (1955) Commensalisme et parasitisme chez les annélides polychètes. Vie et Milieu 6: 525-536.
  • Pérez CD, Costa DL, Opresko DM (2005) A new species of Tanacetipathes from Brazil, with a redescription of the type species T. tanacetum (Pourtalès) (Cnidaria, Anthozoa, Antipatharia). Zootaxa 890: 1-12.
  • Pérez CD, Vila-Nova DA, Santos AM (2005) Associated community with the zoanthid Palythoa caribaeorum (Duchassaing & Michelotti, 1860) (Cnidaria, Anthozoa) from littoral of Pernambuco, Brazil. Hydrobiology 548: 207-215.
  • Pettibone MH (1969) The genera Polyeunoa McIntosh, Hololepidella Willey, and three new genera (Polychaeta, Polynoidae). Proceedings of the Biological Society of Washington 82(3): 43-62.
  • Pettibone MH (1970) Polychaeta Errantia of the Siboga Expedition. Part IV. Some additional polychaetes of the Polynoidae, Hesionidae, Nereidae, Goniadidae, Eunicidae, and Onuphidae, selected as new species by the late Dr. Hermann Augener with remarks on other related species. In: Siboga-Expeditie Uitkomsten op Zoologisch, Bonatisch, Oceanographisch en Geologisch gebied verzameld in Nederlandsch Oost-Indië. Leiden, E.J. Brill, 199-270.
  • Pettibone MH (1989) A new species of Benhamipolynoe (Polychaeta: Polynoidae: Lepidastheniinae) from Australia, associated with the unattached stylasterid coral Conopora adeta Proceedings of the Biological Society of Washington 102: 300-304.
  • Pettibone MH (1991) Polynoid polychaetes commensal with antipatharian corals. Proceedings of the Biological Society of Washington 104: 714-726.
  • Pourtalès LF de (1874) Crinoids and Corals. Zoological results of the “Hassler” Expedition. - Ill. Catalogue of the Museum of Comparative of Zoology, Harvard, 8: 25-50.
  • Pourtalès LF de (1880) Zoological results of the “Blake” expedition to the Caribbean Sea. Bulletin of the Museum of Comparative Zoology Havard 6(4): 113-118.
  • Quattrini AM, Georgian SE, Byrnes L, Stevens A, Falco R, Cordes EE (2013) Niche divergence by deep-sea octocorals in the genus Callogorgia across the continental slope of the Gulf of Mexico. Molecular Ecology 22: 4123-4140. https://doi.org/10.1111/mec.12370
    » https://doi.org/10.1111/mec.12370
  • Rullier F (1964) Résultats scientifiques des campagnes de la Calypso - Campagne de la Calypso aux îles du Cap Vert (1959) (suite): 5. Annélides polychètes. Annales de l’Institut Océanographique 41(6): 113-218.
  • Serpetti S, Taylor ML, Green DH, Rogers AD, Paterson GLJ (2017) Ecological adaptations and commensal evolution of the Polynoidae (Polychaeta) in the Southwest Indian Ocean Ridge: A phylogenetic approach. Deep Sea Research Part II: Topical Studies in Oceanography 137: 273-281.
  • Tazioli S, Bo M, Boyer M, Rotinsulu H, Bavestrello G (2007) Ecological observations of some common antipatharian corals in the marine park of Bunaken (North Sulawesi, Indonesia). Zoological Studies 46: 227-241.
  • Van Pesch AJ (1914) The Antipatharia of the Siboga Expeditie. Monographe 17: 1-258.
  • Warner GF (1981) Species descriptions and ecological observations of black corals. (Antipatharia) from Trinidad. Bulletin of Marine Science 31(1): 147-163.
  • Wagner D, Luck DG, Toonen RJ (2012) The biology and ecology of black corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia). Advances in Marine Biology 63: 67-132. https://doi.org/10.1016/B978-0-12-394282-1.00002-8
    » https://doi.org/10.1016/B978-0-12-394282-1.00002-8
  • Williams GC, López-González P (2005) A new genus and species of gorgonian octocoral (Anthozoa: Plexauridae) from Antarctic waters. Proceedings of the California Academy of Sciences 56(26): 379-390.

Publication Notes

  • Available online:

    June 18, 2019
  • Zoobank Register:

    http://zoobank.org/D3CA2A3E-20A6-4A59-8D4E-A0242B3526A1
  • Publisher:

    © 2019 Sociedade Brasileira de Zoologia. Published by Pensoft Publishers at https://zoologia.pensoft.net

Edited by

Editorial responsibility:

Paulo da Cunha Lana

Publication Dates

  • Publication in this collection
    27 June 2019
  • Date of issue
    2019

History

  • Received
    29 July 2018
  • Accepted
    08 Dec 2018
  • Published
    18 June 2019
Sociedade Brasileira de Zoologia Caixa Postal 19020, 81531-980 Curitiba PR Brasil, Tel./Fax: (55 41) 3266-6823 - Curitiba - PR - Brazil
E-mail: sbz@sbzoologia.org.br