First Record of Glycerella Magellanica (Polychaeta: Glyceridae) for The

Marine Biodiversity Records, page 1 of 5. # Marine Biological Association of the United Kingdom, 2014 doi:10.1017/S1755267214000359; Vol. 7; e35; 2014 Published online First record of Glycerella magellanica (Polychaeta: Glyceridae) for the South Atlantic and in association with Solenosmilia variabilis (Anthozoa: Caryophyllidae) vini’cius da rocha miranda1, alexandra elaine rizzo2 and ana claudia dos santos brasil1 1Universidade Federal Rural do Rio de Janeiro (UFRRJ), Instituto de Biologia, Departamento de Biologia Animal–Zoologia, Laborato´rio de Polychaeta, BR 465, Km 7, Caixa Postal 74524, CEP 23851-970, Serope´dica, Rio de Janeiro, Brazil, 2Universidade do Estado do Rio de Janeiro (UERJ), IBRAG, Departamento de Zoologia, Rua Sa˜o Francisco Xavier, 524, Maracana˜, 20.550–900, Rio de Janeiro, Brazil

The species of Glycerella share a prostomium with four rings bearing four distal appendages, and proboscis with rod-like aileron. They also have the first two parapodia uniramous, while the following are biramous, with dorsal and ventral cirri; the notopodia bear simple capillaries chaetae. The neuropodia are provided in the upper part with compound spinigerous chaetae while those in the lower part are falcigerous. Glycerella magellanica has been reported in the south-west Indian Ocean, south and north-west Pacific Ocean, and north and central Atlantic Ocean. Herein, the first record of this species is reported in the south-west Atlantic, specifically off the north-east coast of Rio de Janeiro, in the Campos Basin. A single specimen of this species was collected during the ECOPROF project coordinated by CENPES/PETROBRAS, although this species has been recorded elsewhere in muddy sediments. In this study the specimen was collected in a dead fragment of the coral Solenosmilia variabilis, at 745 m depth. Morphologically the specimen is very similar to that used in the original description. However, some morphological differences were found related to the appearance of the compound chaetae and aileron. These differences may indicate either that in the original description these features were overlooked, or rather a case of intra-specific variation.

Keywords: Glyceriformia, deep sea, coral reef, endofauna, cold water coral mounds

Submitted 13 October 2013; accepted 28 February 2014

INTRODUCTION their jaws, but the ailerons also show differences among genera: being rod-like shape in Glycerella and Hemipodia The Glyceridae Grube, 1850 are burrower polychaetes, occur- and sub-triangular or ‘Y’ shape in Glycera. Based on these ring from the intertidal down to the abyssal environment, and other characteristics, Bo¨ggemann (2002) in a phylogen- and distributed worldwide (Rouse & Pleijel, 2001; etic study of the family, proposed Glycerella as a sister Bo¨ggemann, 2002). The family is subdivided in three group of Glycera and Hemipodia. genera: Glycera Savigny 1818, Hemipodia Kinberg 1865, In his review for the family Glyceridae, Bo¨ggeman (2002) and Glycerella Arwidsson 1899 (Bo¨ggemann, 2002), which reiterates Glycerella magellanica (McIntosh, 1885) as the can be differentiated based on the characteristics commonly only valid species in the genus, considering both Glycerella used in polychaete systematics, such as the shape of the para- atlantica Wesenberg-Lund, 1950 and Pseudolacydonia podia, which are uniramous in Hemipodia and mostly caeca Rullier, 1964 as junior synonyms. The species G. biramous in Glycera and Glycerella; by the presence of falci- magellanica occurs in the North Atlantic, Caribbean Sea, gerous and spinigerous neurochaetae in Glycerella, while Agulhas Basin (South Africa), south-west Indian Ocean, Glycera and Hemipodia only bear spinigerous neurochaetae, the Pacific north-west coast and Pacific–Antarctic Basin which vary morphologically throughout the body in these (near the west coast of South America), collected from two genera (Parapar & Moreira, 2010). Glycera and shallow-water (45 m) down to deep-water (1,960 m) Glycerella also possess capillary notochaetae, which is mainly in muddy sediments. Herein, the first record of G. absent in Hemipodia. They do not differ in the shape of magellanica is presented in the South Atlantic (off the Brazilian coast) filling a gap in the Atlantic distribution of this species. Also, this is the first record of this species associated with an anthozoan coral environment, in a dead frag- Corresponding author: V.D. Miranda ment of the Caryophyllidae Solenosmilia variabilis (Duncan, Email: [email protected] 1873).

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MATERIALS AND METHODS RESULTS

A single specimen was collected from the Campos Basin, on the south-east continental margin of Brazil, between 20.58 systematics and 248S(Figure 1). The material was collected under the Order PHYLLODOCIDA scope of the research Deep-Sea Ecosystems Project Suborder GLYCERIFORMIA (ECOPROF), conducted by the Research and Development Family GLYCERIDAE Grube, 1850 Center of the Brazilian Energy Company, PETROBRAS, Genus Glycerella Arwidsson, 1899 between 2008 and 2011. On each campaign, five samples con- magellanica (McIntosh, 1885) by monotypy taining five different species of anthozoan corals were col- (Figures 2A–Q) lected: Lophelia pertusa (Linnaeus, 1758); Madrepora oculata Linnaeus, 1758; Enallopsammia rostrata (Pourtale`s, Hemipodus magellanicus McIntosh, 1885, 349; pl. 42, 1878); Solenosmilia variabilis; and the hydrocoral Errina sp. figures11–15; pl. 22a, figures 12–15; pl. 35a, figures 5 & 7. The specimen was deposited in the Edmundo Ferraz Glycerella atlantica Wesenberg-Lund, 1950, 24, pl. 5, figure 22; Nonato collection located at the Biology Institute of the pl. 6, figure 28; O’Connor, 1987, 21, figure 3a–c. Federal University of Rio de Janeiro (IBUFRJ). Pseudolacydonia caeca Rullier, 1964, 151, figure 8a–k. Fragments of corals were collected using a remotely oper- Glycerella magellanica Bo¨ggemann, 2002, 78, figures 124–126; ated vehicle. The corals, including the associated fauna, were Imajima 2005, 81, figure 35a–i; Parapar & Moreira, 2009, 231, fixed in a combination of formaldehyde and borax, in a 10% figures 1–5. concentration, without any anaesthetic process. In the labora- tory, the polychaetes were sorted from the corals and studied diagnosis (according to bo¤ggemann, 2002) under a stereomicroscope. Drawings were made with the aid Body with numerous segments, elongated, tapering at both of a camera lucida attached to the Zeiss V8 stereomicroscope ends. Segments superficially triannulated. Prostomium con- and to a Wild M20 microscope. Three parapodia (anterior, sisting of four rings, appendages relatively long. Aileron median and posterior) were detached from the body and rod-like. The first two parapodia uniramous consisting of neu- parts of the proboscis were mounted in permanent slides ropodium, ventral cirri and compound chaetae, dorsal cirrus using the mounting medium Gray & Wess’ (PVA) from the second parapodium; the following parapodia (Humason, 1979) or Hoyer’s medium. biramous with dorsal and ventral cirri; notopodia and

Fig. 1. Sampling area (upper map) and occurrence area of Glycerella magellanica in ECOPROF project (lower map) (maps from Google Earth#).

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neuropodia indistinctly separated from each other; each para- neurochaetae with blade long on the anterior parapodia podium with two prechaetal and two postchaetal lobes. (Figure 2K), becoming shorter and distally curved on the pos- Branchiae absent. Notopodia with simple capillary chaetae; terior parapodia (Figure 2P); shaft end of all neurochaetae neuropodia with compound chaetae of two types: dorsal spi- with accessory lateral teeth on one side (Figure 2L, Q). nigerous and ventral falcigerous. Pygidial cirri lost. material examined 1 specimen (IBUFRJ 2125): located inside a dead base of the deep-sea coral Solenosmilia variabilis at 745 m depth; col- DISCUSSION lected in the Campos Basin (Brazil) at 40814′4578′′W 22831′197′′S, on 17 March 2006. This specimen seems morphologically similar to those examined and originally described by McIntosh (1885) and later by description Bo¨ggemann (2002) during their re-description of the species. Body complete, broken into two parts near the most posterior However the presence of a rudimentary interramal plate was region, measuring 16.77 mm long and with 77 chaetigers observed on the side of the aileron, a feature that may have (Figure 2A). Brownish body. The anterior segments uniannu- passed unnoticed by other authors, as observed in the draw- lated, biannulated from the 9th chaetiger, triannulate ings provided by Bo¨ggemann (2002) and by Parapar & mid-body from the 22nd chaetiger; anterior annulus the Moreira (2009, 2010). Bo¨ggemann (2002) also proposed a shortest and medium annulus the longest. Prostomium phylogenetic relationship for Glyceridae, in which the short and conical, consisting of 4 rings, posteriormost rod-like aileron is the basal characteristic within the family. annulus with indication of a 5th incomplete ring finishing Therefore this interramal plate, which is rudimentary in before the nuchal organ (Figure 2B). Four appendages in Glycerella, may disappear completely in Hemipodia and distal anterior part (a pair of dorsal antennae and a pair of develop into a plate in Glycera. ventral palpi; the two on the right lost) dorsoventrally Bo¨ggemann (2002) considers the chaetae as a weak charac- flatted. The posteriormost annulus with one pair of half-moon teristic to diagnose species of Glyceridae, because it shows shaped nuchal organs. Palps reaching the fifth annulus and little variation at an interspecific level. However, recent antenna surpassing the fourth annulus. Proboscis with studies with Glycera and Hemipodia showed differences in numerous digitiform papillae with a more or less distinctly the morphology of the chaetae along the body in the same spe- straight, median, longitudinal ridge; some digitiform papillae cimen (Rizzo et al., 2007; Parapar & Moreira, 2010). A mor- slightly shorter, basally larger and distally more rounded phological variation among the neurochaetae was also than the majority (Figure 2C, D); all papillae presenting cilia observed throughout the body; they become smaller to the at the top, the longer with two to three cilia and the shorter end of the body and present a clear indentation at the end with one. Ailerons rod-like, slightly enlarged, seems rudimen- of the falcigerous neurochaetae. In addition, Parapar & tary interramal plate (Figure 2E). The first two parapodia uni- Moreira (2009) noted the the border of the blade on some spe- ramous with one slender triangular prechaetal lobe and one cimens of G. magellanica can be serrated or smooth; the more rounded and shorter postchaetal lobe (Figure 2F). The border of the blade of all chaetae examined in the studied spe- following parapodia biramous with two slender triangular to cimen are smooth. However to explore these differences, digitiform prechaetal lobes; notopodial lobe always slightly which are only properly seen with the scanning electron longer and wider than the neuropodial lobe (Figure 2I); microscope, may reveal interspecific differences which can both becoming slightly smaller in posterior parapodia be used in future phylogenetic studies, even though they (Figure 2M). The last three parapodia with their notopodial would not be applicable in routine identification work lobe broken. Two shorter postchaetal lobes; both lobes (Parapar & Moreira, 2010), among other things due to the rounded anteriorly; notopodial lobe elongated and the follow- small number of specimens. ing parapodia blunt triangular, slightly longer than rounded The presence of a secondary tooth at the shaft end of the neuropodial lobe; in most posterior parapodia, notopodial neurochaeta was observed as well. No reference was found lobe usually shorter and rounded than those from anterior for this characteristic, neither in the descriptions of and median parapodia. Dorsal cirri from the second parapo- McIntosh (1885), nor Bo¨ggemann (2002) nor Parapar & dia, conical to oval; inserted on the body wall, above parapo- Moreira (2009, 2010), and since there was only one specimen dial base. Ventral cirri in anterior parapodia relatively wide it was considered as a mere variation present in this specimen, and conical (Figure 2I); in the posterior parapodia more or rather, that this may have been overlooked in previous slender triangular to digitiform, about as long as the neuropo- work. Therefore, such a feature does not justify by itself creat- dial postchaetal lobe, and situated near the parapodial base. ing a new species for the Brazilian specimen. Branchiae absent. Parapodia with one noto- and one neuroa- For the Brazilian coast, among the 16 species recorded cicula. Notochaetae simple, capillary, marginally slightly ser- belonging to the Glyceridae, 14 correspond to the genus rated at the border, surface rough on the whole extension Glycera and the other two to Hemipodia (Amaral et al., on the dorsalmost (Figure 2N) and only on the distal end of 2012; Rizzo, unpublished data); therefore, this represents the the lowermost. Neurochaetae of two types: spinigerous on first record of the genus Glycerella for the South Atlantic. dorsal neuropodia (Figure 2G, H, J, O) and falcigerous on According to Bo¨ggemann (2002) and Parapar & Moreira ventral neuropodia (Figure 2K, P); all chaetae with blade (2009), G. magellanica had been previously recorded, in all rough (Figure 2G, H, J, K, O, P). Spinigerous neurochaetae other global regions, to the Caribbean Sea (Barbados’s coast) with blade very long and distally slender on the anterior para- and to the Strait of Magellan (Chilean coast), with a gap occur- podia (Figure 2 J), becoming slightly shorter, larger and distal- ring along the entire east coast of South America, which is par- ly curved on the posterior parapodia (Figure 2O). Falcigerous tially filled with this new record.

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Fig. 2. Glycerella magellanica (McIntosh, 1885): (A) complete specimen showing pharynx partially everted, dorsal view; (B) prostomium of the same; left lateral view; (C) anterior view of longer papillae; (D) anterior view of shorter papillae; (E) aileron; (F) ﬁrst parapodium; (G) spinigerous neurochaeta of chaetiger 1; (H) detail of blade of the same neurochaeta; (I) posterior parapodium; (J) capillary notochaeta; (K) spinigerous neurochaeta; (L) falcigerous neurochaeta; (M) detail of the shaft end with secondary tooth; (N) middle parapodium; (O) spinigerous neurochaeta; (P) falcigerous neurochaeta; (Q) detail of the shaft end with secondary tooth. Scale bars: (A) 1.55 mm; (B) 350 mm; (C, E) 105 mm; (D, K, O, P) 40 mm; (F, N) 130 mm; (G, H) 74 mm; (I) 54 mm; (J, L) 15 mm; (M, Q) 4 mm.

This species was mostly collected below 100 m inside a dead portion of the Caryophyllidae S. variabilis. (Bo¨ggemann, 2002); this may suggest that G. magellanica is Parapar & Moreira (2009) previously reported this specimen more common in deeper waters. Also the species mainly in association with coral debris, however due to the sampling occurs in muddy environments, with or without shell or methodology used in their work (dredge), it was not possible coral debris (Bo¨ggemann, 2002; Imajima, 2005; Parapar & to afﬁrm if the specimens were among the coral debris or if Moreira, 2009), and was never found in an anthozoan coral they were carried to the debris during the dredging. environment, as reported here, since this specimen was Probably the paucity of studies in deeper water habitats,

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along the east coast of South America, might explain the McIntosh W.C. (1885) Report on the Annelida Polychaeta collected by absence of records of this species there. By increasing the H.M.S. Challenger during the years 1873–1876. Report on the numbers of studies in the Brazilian deep-sea it is expected Scientiﬁc Results of the Voyage of H.M.S.Challenger during the years the number of glycerid taxa occurring there may also increase 1872–76, Series Zoology 12, 1–554. and therefore the actual diversity of this family might be truly O’Connor B.D.S. (1987) The Glyceridae (Polychaeta) of the North assessed. Atlantic and Mediterranean, with description of two new species. Journal of Natural History 21, 167–189.

Parapar J. and Moreira J. (2009) Sobre la presencia de Glycerella magel- ACKNOWLEDGEMENTS lanica (McIntosh,1885) (Polychaeta, Glyceridae) en el litoral de la penıńsula Ibe´rica. Graellsia 65, 225–233. We thank CENPES/PETROBRAS S.A. for providing the studied material and Dr. Helio R. Silva for reviewing this Parapar J. and Moreira J. (2010) Aproximacioń al estudio de la manuscript. CAPES (Coordenadoria de Aperfeiçoamento de morfologıá setı´gera en algunas especies ibe´ricas de los geńeros Pessoal de Ensino Superior) funded the first author with a Glycera Savigny, 1818 y Glycerella Ardwidsson, 1899 (Polychaeta, scholarship that allowed him to accomplish this study. The Glyceridae). Graellsia 66, 119–130. comments and suggestions provided by the referees are Rizzo A.E., Steiner T.M. and Amaral A.C.Z. (2007) Glyceridae Grube, greatly appreciated. 1850 (Annelida: Polychaeta) from Southern and Southeastern Brazil, including a new species of Glycera. Biota Neotropica 7, 41–59.

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