Zootaxa 4466 (1): 197–204 ISSN 1175-5326 (print edition) http://www.mapress.com/j/zt/ Article ZOOTAXA Copyright © 2018 Magnolia Press ISSN 1175-5334 (online edition) https://doi.org/10.11646/zootaxa.4466.1.15 http://zoobank.org/urn:lsid:zoobank.org:pub:1BCC4BD8-A168-408A-8DFD-407DFA44C91D

When is an aster not an aster? A new deep-sea Discorhabdella (Demospongiae, ) with asters, from the Mozambique Channel

JEAN VACELET1,3 & PACO CÁRDENAS1,2 1IMBE, CNRS, Aix Marseille Univ, Univ Avignon, IRD, Station Marine d’Endoume, 13007 Marseille, France. 2Pharmacognosy, Department of Medicinal Chemistry, Uppsala University, Uppsala 75123, Sweden. http://orcid.org/0000-0003- 4045-6718 3Corresponding author. E-mail: [email protected]

Abstract

Discorhabdella pseudaster n. sp. is an incrusting from the upper bathyal zone of the ‘Banc du Geyser’, north of Madagascar, Mozambique Channel. This new species is described only from a single specimen but it is remarkable by the presence of spicules similar to euasters, a type of microsclere unknown in Poecilosclerida. These spicules are in fact a new example of homoplasy, being derivatives of the typical Discorhabdella pseudoastrose acanthostyles, which are here re- duced to the aster-like tyles. The isochelae with a large lamella on the shaft are also quite unique in Poeciloclerida.

Key words: Porifera, new species, Madagascar, bathyal, homoplasy

Introduction

The Mozambique Channel is still a poorly explored area for Demospongiae, despite the works of Bösraug (1913), Lévi (1956, 1964), Vacelet & Vasseur (1965, 1971) and Vacelet et al. (1976), Vasseur & Lévi (1976) who collected extensively in W Madagascar and Europa Island. The ‘Benthédi’ 1977 campaign in the Mozambique Channel collected shallow and deep-sea but they have been barely studied apart from the calcareous keratose Vaceletia crypta by Vacelet (1977, 1979), collected from shallow waters around the Glorieuses Islands. The rest of the ‘Benthédi’ material (currently stored in the collections of the ‘Muséum National d’Histoire Naturelle’, Paris, France) remains to this day undescribed. These few studies focused on shallow-water sponges, up to 70 m for Lévi (1964), so that the bathyal fauna in this region is largely unknown. The BIOMAGLO expedition (https://expeditions.mnhn.fr/campaign/biomaglo) organized by the Muséum National d’Histoire Naturelle (MNHN, Paris, France) in collaboration with the IFREMER took place in January- February 2017. The aim of BIOMAGLO was precisely to investigate the deep-sea benthos in the Mozambique Channel, with a special focus around Mayotte, Comoros and Glorieuses Islands. While sorting this large collection, a puzzling observation in an incrusting sponge attracted our attention: euasters in a poecilosclerid sponge, when asterose microscleres are unknown in this large order and currently found only in the orders Chondrosiida, Axinellida (Stelligeridae), Tetractinellida, Clionaida (, Spirastrellidae) and Tethyida (Morrow & Cárdenas 2015). We show here that these “asters of a new Discorhabdella species are not true asterose microscleres, but derivatives of the pseudoastrose acanthostyles megascleres characteristic of this , which once more hints at the extraordinary capacity of sponges to re-invent the same spicule types through convergent evolution.

Material and methods

The specimen of the new species was collected by dredging on ‘Banc du Geyser’, placed between Mayotte and Glorieuses Islands. Soon after collection with a Warén dredge, a photograph was taken (Fig. 1) and the specimen was preserved in 95% ethanol.

Accepted by M. Klautau: 19 Jun. 2018; published: 31 Aug. 2018 197 Due to the small size of the unique specimen, spicule preparations were made by boiling a very small piece of the sponge in a few drops of nitric acid directly on microscope slides. After rinsing in distilled water, the slides were either mounted in Araldite for light microscopy or sputter-coated with gold–palladium for scanning electron microscopy (SEM) with a Hitachi S570. A section was hand made through the sponge for examination of skeletal organization. Molecular analysis, which would have destroyed the remaining tiny specimen with uncertain chances of success, was not undertaken. The type specimen is deposited in the MNHN, at room temperature, with a slide of spicule preparation.

Description

Class Demospongiae Sollas, 1885

Subclass Cárdenas, Pérez & Boury-Esnault, 2012

Order Poecilosclerida Topsent, 1928

Family Lévi, 1963

Genus Discorhabdella Dendy, 1924

Discorhabdella pseudaster n. sp.

Holotype. MNHN-IP-2015-1083, station DW 4788, Warén dredge, 22/01/2017, Banc du Geyser, 12°22’ S, 46°25’ E, 346–349 m depth, rocks and pebbles. Field# PMG 05, coll. C. Debitus, ethanol 95%. Description. A minute, incrusting sponge, 4 x 2.5 mm and 200 µm thick, hispid (Fig. 2 A). Color grayish white alive and in alcohol. No visible aperture. A stoloniferous calcified octocoral, possibly Scleranthellia (Gary Williams, pers. com.), is growing on the same rock. Skeleton. The skeleton is made of long styles with a barely inflated head bearing low, round tubercles. These styles are disposed vertically on the substratum and give the long hispidation. They are surrounded by smaller tylostyles irregularly arranged, sometimes forming poorly defined bouquets. Pseudoastrose acanthostyles are arranged vertically, with the head on the substratum. Pseudoasters and isochelae are dispersed in the whole choanosome. Spicules. (1) Subtylostyles (Fig. 2 B), straight or slightly curved, with a barely tuberculated head, all broken in the spicule or skeleton slides. Axial canal ending in a small vesicle in the head (not divided), although faint, radiating darker lines could be seen (Fig. 3 A). Maximum length of the broken spicules: 600 µm, diameter 40–56 µm near the base.(2) Tylostyles (Fig. 2 C), straight or slightly curved, with a well-marked oval head, 240– 370 x 9–10 µm.(3) Pseudoastrose acanthostyles (Fig. 2 D–F). Spine-like rays of the head obtuse, those of the end of the shaft generally more acute. Total length 35–45 µm, diameter of the head 35–40 µm, shaft 20-25 x 12 µm with spines at the extremity. Axial canal barely visible by transparency (not divided in the head), although faint, radiating darker lines could be seen in the head (Fig. 3 B). Some rare spicules, likely juvenile, are a little smaller (e.g. 28 µm in length), and have more acute spines.(4) Pseudoasters (Fig. 2 G–I), similar to spherasters, very abundant, 12.5–18 µm in diameter, with conical, sharp spine-like rays, 2.5–4 µm long. No visible axial canals in the spines.(5) Unguiferous cleistochelae (Fig. 2 J), small, 12–15 µm. Shaft straight, 4 or 5 teeth nearly in contact, often with the end on one side blunt and the other slightly indented. The shaft bears a conspicuous lamella, attached by a part of its length, similar to a hatchet. The free part of the hatchet is most often directed towards the non- indented teeth, but the opposite case has also been observed. Etymology. From Latin pseudo (meaning false) and aster. Remarks. The presence of chelae makes this sponge a Poecilosclerida. This minute sponge clearly belongs to the genus Discorhabdella by its shape, skeleton and especially the diagnostic club-shaped pseudoastrose acanthostyles. Unfortunately, the unique specimen is too small to allow obtaining sequences, so the affinities between Discorhabdella and remain likely (Maldonado & Uriz 1996), but not formerly demonstrated. It is rather puzzling to find “aster” spicules in a poecilosclerid, which moreover have the same position in the skeleton as true asters in non-poecilosclerid encrusting sponges (e.g. Spirastrellidae, Chondrillida or Tethyida). The

198 · Zootaxa 4466 (1) © 2018 Magnolia Press VACEL ET & CÁRDENAS true nature of these asters is questionable. It is essential in and phylogeny to use homologous morphological characters, and that is not always obvious as clearly shown by Fromont & Bergquist (1990) with the example of sigma microscleres or acanthose megascleres. Here, the most likely explanation is that the “asters” derive from the pseudoastrose acanthostyles with reduced shaft typical of Discorhabdella by complete loss of the shaft. The presence of “asteroid” corpuscules somewhat similar to asters have been described in two other members of the family Crambeidae, Crambe tuberosa Maldonado & Benito, 1991, and Crambe chilensis Esteves et al., 2007; these spicules, which in C. tuberosa have axial filaments in the actines, were interpreted as developmental stages of desmas, otherwise present in Crambe spp. (Maldonado & Benito 1991; Uriz & Maldonado 1995; Maldonado & Uriz 1996).

FIGURE 1. On-deck picture of the piece of rock bearing the specimen (arrow). Square = 25 mm.

NEW DISCORHABDELLA WITH ASTERS Zootaxa 4466 (1) © 2018 Magnolia Press · 199 FIGURE 2. Discorhabdella pseudaster n. sp., A, habitus of holotype (arrow). B, large subtylostyle. C, tylostyle. D, pseudoastrose acanthotyle. E, immature pseudoastrose acanthotyle. F, pseudoastrose acanthotyle seen from the tip. G, H & I, pseudoasters. J, unguiferous cleistochelae.

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1–1.3 1–1.3 26–34* 26–34* 28 x 1.3 28 x 19–26 & sigmas 13–16 13–16 sigmas Oxydiscorhabds 33–51* 33–51* ––– 48 48 ––– ––– 22–27 Sigmas 11–16 x x 11–16 Sigmas ––– 22–27 Pseudoasters Isochelae Other microscleres Other Isochelae Pseudoasters ? ? ? 52/40 52/40 36–53* 36–53* head 36–39 acanthostyles

540/12 Tylostyles Pseudoastrose Tylostyles Pseudoastrose II: 37 29 x 357–592 x 10–15 * 357–592x

1700/50 650 x 28 x 650 330 130 ––– 25 ––– subtylostyles subtylostyles Tuberculated Tuberculated > 600 x 40–50 240–370 9–10x 35–45 12.5–18 12–15 ––– 117–300 x 5–10 117–300x 2.5–4 130–180 x 26–40 ––– ––– 13–15 Sigmas species showing spicule measurements spicule (in measurements species μm). showing 380–750 x 19–42 180–220 x 5–7 23–37 ––– 26–29 Acanthomicroxea 855–1556 34–52 x 276–445 5.2 x 43–57 x 8–10, 900–1700 x 28–61 * 900–1700 x Discorhabdella range 183 m 183 m 736 m 736 m Azores Azores 10–30 m 10–30 m 55–73 m 534–604 m 534–604 m 346–349 m 346–349 m Alboran Sea New ZealandNew New ZealandNew 45 ? x I: 43 35&x South Australia ? ? 180 ? ? 180 ? Australia South Banc du Geyser Banc du Geyser Panama (Pacific) (Pacific) Panama (Pacific) Panama .

, measurements by van Soest the by (2002), holotype. measurements from .

sp n. sp n. species species depth and Region Comparative table world of Comparative incrustans D. incrustans . cf. . cf. ** From Hinde (1892): Holmes ** & Fig p.194,Pl.VIII, 29. (2015) identification one Łukowiak spicule.*** Tentative Eocene by from TABLE 1. TABLE 1. D. hindei D. incrustans *For Discorhabdella D. littoralis D. tuberosocapitatum urizae D. pseudoaster D. (late Eocene ***) (late Eocene ***) Discorhabdella (late Eocene **) (late Eocene **) D

NEW DISCORHABDELLA WITH ASTERS Zootaxa 4466 (1) © 2018 Magnolia Press · 201 It has been suggested that pseudoastrose acanthostyles are polyaxial spicules, on the basis of SEM observations (Uriz & Maldonado 1995; Maldonado & Uriz 1996). However, in our opinion, the presence of axial canals in the spines of the head of the pseudoastrose acanthostyles remains doubtful: in a few immature spicules, some actines of the head show a very small hole at their end (Fig. 2 E), but a canal could not be seen in transparency under a light microscope in the actin of mature spicules, while the axial canal of the shaft of the same spicules is clearly visible. Similarly, the subtylostyles with a slightly tuberculated head show by transparency a clear axial canal ending in a vesicle in the head, without division. However, it must be noted that from this vesicle, there are very faint radiating lines, which could indicate remains of axial filaments present during the spicule formation (Fig. 3 A). The same very faint radiating lines are barely visible in the head of pseudoastrose acanthostyles (Fig. 3 B). It is also possible that these extra spines and bulges are produced by secondary axial canals not conected to the main shaft axial canal, but somehow added later, just like the axial canals in the rosette formation of geodiid sterrasters (Cárdenas & Rapp 2013). Then, they could be filled in some cases and be invisible in our observations. To conclude, we raise doubts as to the polyaxial nature of these spicules and warrant more observations at the interface between the tip of the tylostyles and their siliceous additions (spines and bulges). There are currently five known species of Discorhabdella from the Pacific coast of Panama, Western Mediterranean, the Azores and New Zealand (Table 1). Our new species differs from the other species by several characters: (1) presence of two types of pseudoastrose acanthostyles, one of which (pseudoaster) has entirely lost the shaft and is reduced to the inflated, spinose head, similar to an aster; (2) microscleres composed only of a single isochelae type, with sigma and oxydiscorhabd missing. The microsclere composition in Discorhabdella spp. is quite diverse, but only D. tuberosocapitatum (Topsent, 1890) has only isochelae. The isochelae of the new species clearly differ from those of D. tuberosocapitatum, which is from Macaronesia (N-E Atlantic), by a different shape, with teeth nearly joining and the shaft bearing a lamella. This type of isochelae shape is unknown in the other species of the genus.

FIGURE 3. Discorhabdella pseudaster n. sp. A, head of a subtylostyle, showing the axial canal. B, head of a pseudoastrose acanthotyle viewed by the top.

These isochelae, very unusual in Poecilosclerida, remind of the ‘palmate-anchorate-arcuate’ evolutionary sequence suggested by Maldonado & Uriz (1996) for aberrant chelae morphologies in Crambeidae genera Crambe and Discorhabdella. However, the isochelae of D. pseudaster n. sp., although possibly included in such a sequence, appear unique in Crambeidae, and more generally in Poecilosclerida. The most original character is the presence of a lamella on the shaft, a character rarely observed in isochelae. To our knowledge, this character is known only in the small isochelae of Hymenancora sirventi (Topsent, 1927) in Myxillidae. An interesting other example could be one isochela found by Hinde & Holmes (1892, p. 200, Pl. IX, 39) in sediment from the Late Eocene, and tentatively attributed to Melonanchora elliptica Carter, 1874. According to their description and drawing, this chela somewhat resembles those of the new species, although larger (66 µm) and bearing two

202 · Zootaxa 4466 (1) © 2018 Magnolia Press VACEL ET & CÁRDENAS lamellae instead of a single one. The presence of typical Discorhabdella spicules (tuberculate tylostyles and pseudoastrose acanthostyles) in these same Eocene sediments (Hinde & Holmes 1892; Łukowiak 2015) suggests that this chela may belong to this genus. The discovery of this 4 mm long new species emphasizes the need to carefully examine minute, inconspicuous, incrusting sponges on such rocky bathyal substrates, which certainly represent an underestimated source of biodiversity.

Acknowledgements

The sponge sample in this paper originates from the deep-sea cruise BIOMAGLO conducted jointly by French National Museum of Natural History (MNHN) as part of the Tropical Deep-Sea Benthos program, the French Research Institute for Exploitation of the Sea (IFREMER), the French Southern and Antarctic Lands (TAAF), the Departmental Council of Mayotte and the French Development Agency (AFD), with the financial support of the European Union. We are grateful to the crew of R/V Antéa, especially Cécile Debitus in charge of collecting and documenting sponge specimens, as well as the cruise leadersof BIOMAGLO: Laure Corbari, Karine Olu-Le Roy and Sarah Samadi. We also thank this team and Magalie Castelin for organizing the BIOMAGLO taxonomy workshop in Concarneau in April 2017, and inviting the authors, which led to the discovery of this new species. P. Cárdenas is supported by the European Union's Horizon 2020 research and innovation program through the SponGES project (grant agreement No. 679849). This document reflects only the authors’ view and the Executive Agency for Small and Medium-sized Enterprises (EASME) is not responsible for any use that may be made of the information it contains.

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