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Xenophyophores (Rhizaria, Foraminifera) Protist, Vol. 169, 926–957, December 2018 http://www.elsevier.de/protis Published online date 5 October 2018 ORIGINAL PAPER Xenophyophores (Rhizaria, Foraminifera) from the Eastern Clarion-Clipperton Zone (equatorial Pacific): the Genus Psammina a,1 b a c Andrew J. Gooday , Maria Holzmann , Aurélie Goineau , Olga Kamenskaya , d e a,2 b Vyacheslav F. Melnik , Richard B. Pearce , Alexandra A.-T. Weber , and Jan Pawlowski a National Oceanography Centre, Southampton, University of Southampton Waterfront Campus, European Way, Southampton SO14 3ZH, UK b University of Geneva, Department of Genetics and Evolution, Quai Ernest Ansermet 30, 1211 Geneva 4, Switzerland c Shirshov Institute of Oceanology Russian Academy of Sciences, Nakhimovsky Prosp. 36, 117997 Moscow, Russia d Joint Stock Company Yuzhmorgeologiya, Krymskaya St., 20, 353461 Gelendzhik, Russia e Ocean and Earth Science, University of Southampton, National Oceanography Centre Southampton, Waterfront Campus, European Way, Southampton SO14 3ZH, UK Submitted May 9, 2018; Accepted September 24, 2018 Monitoring Editor: Laure Guillou Xenophyophores are important megafaunal organisms in the abyssal Clarion-Clipperton Zone (CCZ; equatorial Pacific), a region hosting commercially significant deposits of polymetallic nodules. Previ- ous studies assigned those with attached, fan-like tests to Psammina limbata, a species described from the central CCZ based on morphology. Here, we redescribe the holotype of P. limbata and then show that limbata-like morphotypes collected in the eastern CCZ include three genetically distinct species. Psammina aff. limbata is closest morphologically to P. limbata. The others are described as P. micro- granulata sp. nov. and P. rotunda sp. nov. These fan-shaped species form a well-supported clade with P. tortilis sp. nov., a morphologically variable species exhibiting features typical of both Psammina and Semipsammina. A second clade containing Psammina sp. 3, and two species questionably assigned to Galatheammina branches at the base of this group. The genus Psammina includes another 9 described species for which there are no genetic data, leaving open the question of whether Psammina as a whole is monophyletic. Our study increases the number of xenophyophore species described from the east- ern CCZ from 8 to 11, with a further 25 morphotypes currently undescribed. Many additional species of these giant foraminifera undoubtedly await discovery in abyssal settings. © 2018 The Author(s). Published by Elsevier GmbH. This is an open access article under the CC BY- NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Key words: Agglutinated foraminifera; monothalamids; new species; SSU rDNA sequences; deep-sea mining; polymetallic nodules. Introduction 1 Corresponding author; fax +44 23 80596247 2 Present address: Marine Invertebrates, Sciences, Museum The Clarion-Clipperton Zone (CCZ) in the east- Victoria, GPO Box 666, Melbourne, Victoria 3000, Australia ern equatorial Pacific has long been known as e-mail [email protected] (A.J. Gooday). https://doi.org/10.1016/j.protis.2018.09.003 1434-4610/© 2018 The Author(s). Published by Elsevier GmbH. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Xenophyophores (Rhizaria, Foraminifera) from the Eastern Clarion-Clipperton Zone 927 an area where xenophyophores (large agglutinated applied to xenophyophores. foraminifera) are common and relatively diverse Supergroup Rhizaria Cavalier–Smith 2002 (Schulze 1907; Tendal 1972, 1996). In recent years, a considerable research effort has focused Foraminifera D’Orbigny 1826 on this region, which hosts vast, commercially ‘Monothalamids’ important deposits of polymetallic nodules. Sam- Clade C pling in several of the areas licensed for nodule prospecting by the International Seabed Author- Xenophyophoroidea Tendal 1972 ity has revealed the presence of many additional xenophyophore species (Gooday et al. 2017a). A Genus Psammina Haeckel 1889 number of these have been formally described, some from the Russian license area in the central Type species: Psammina nummulina Haeckel 1889 CCZ (Kamenskaya 2005; Kamenskaya et al. 2015, 2017), others from the United Kingdom 1 (UK- Diagnosis: Test free or attached, fragile, brittle, 1) and Ocean Mineral Singapore (OMS) license basically plate-like, and fan-shaped or rounded areas at the eastern end of the CCZ (Gooday et al. with basal stalk attached to substrate, or dis- 2017b,c). One such species is Psammina limbata coidal without stalk, or folded into more complex Kamenskaya, Gooday & Tendal 2015, established shape. Circular apertures (‘pores’) or lattice-like by Kamenskaya et al. (2015) based on a single mesh of spicules developed along margin in some specimen from the Russian area, for which no species. External xenophyae firmly cemented to genetic data are available. The specimen had a form upper and lower plates; internal xenophyae semicircular test with a distinctive pale rim and was relatively sparse, sometimes forming pillar-like, bar- found attached to a nodule by a short basal stalk. like, or partition-like structures between plates. Pale According to Gooday et al. (2017a) this species is rim often present in fan-shaped species. Granellare fairly common in the UK-1 and OMS areas. How- branches and well-developed stercomare strings ever, a subsequent reassessment of the genetic run between plates (Modified after Gooday and data from these two areas has revealed that mate- Tendal 2000). rial assigned to P. limbata encompasses at least Remarks: Following Gooday and Tendal (1988, three distinct species. The one that is most similar 2000), Tendal (1996) and Kamenskaya et al. (2015, to P. limbata is assigned tentatively to this species 2017), Psammina is interpreted to encompass as P. aff. limbata, the other two were undescribed. plate-like xenophyophores in which the test is They cluster with a fourth Psammina species, also folded, undulating or stalked, in addition to the undescribed, that is morphologically distinct. typical, more or less discoidal forms originally The present study has the following main objec- described by Haeckel (1889) and included in this tives. 1) To redescribe P. limbata based on genus by Tendal (1972). As discussed below, it photographs of the freshly-collected holotype and is likely that this heterogeneous assemblage of a re-examination of its remaining fragment. 2) To species is polyphyletic. describe (as P. aff. limbata) sequenced and unse- quenced specimens from the UK-1 and OMS areas that we consider most similar to P. limbata. 3) To for- Psammina limbata Kamenskaya, Gooday mally describe the three new Psammina species (P. & Tendal 2015 microgranulata sp. nov., P. rotunda sp. nov., P. tor- tilis sp. nov.). Two unsequenced specimens of P. Figures 1, 2; Supplementary Material Figure S1A,B aff. limbata were included in a recent study of the Psammina sp. Kamenskaya, Melnik, Gooday, 2013, internal structure of several xenophyophores using pp. 391–392, Fig. 6b Micro-CT 3D imaging (Gooday et al. 2018). Psammina limbata Kamenskaya, Gooday, Tendal, 2015, pp. 585–588, Fig. 4 Results Material. Unique holotype collected in the Russian ◦ ◦ exploration claim area: 13.28 N, 134.45 W; depth Systematics 4,724 m (Kamenskaya et al., 2015). Diagnosis: Flattened, plate-like, rigid, semi-circular See Tendal (1972) and Gooday et al. (2017b) test attached to nodule surface by basal stalk for definitions of the special morphological terms and root-like structures. Outer test layer relatively 928 A.J. Gooday et al. Figure 1. Psammina limbata Kamenskaya, Gooday, Tendal 2015; holotype from Russian license area. A: Attached to a nodule, as originally collected; view of concave side. B: Detached from nodule, convex side. Scale bars: 1 cm. thin and fragile, composed of radiolarian skeletons wards (i.e., away from the concave face of the test) and sponge spicule fragments, with some min- and arose from the base of an abraided ridge-like eral grains. Weakly developed concentric zonation feature that extended down most of the vertical sometimes visible. Curved outer margin distinctly axis on the convex side of the plate (Fig. 1B). An lighter than other parts of test and consisting mainly extensive system of more or less twisted roots-like of sponge spicules. Interior with prominent strings bars was developed on either side of the base of of granellare and masses of stercomare interwoven the test (Fig. 1A). Most of them extended down- with loosely agglutinated spicule fragments; ster- wards and outwards towards the sloping nodule comare and granellare absent from pale margin surface, sometimes splitting into short branches at (modified slightly from Kamenskaya et al. 2015). their extremities. However, these ‘roots’ terminated just above the nodule surface, which was covered Additional observations on the holotype with a thin layer of sediment. The original description was based on the holo- In Figure 1B, which shows the convex side of type (housed in the Zoological Museum of the the test after removal from the nodule, the height Moscow State University, registration number F- exceeds the width resulting in a somewhat elon- 18), the only specimen available to Kamenskaya gated shape, and the lower margin of the test forms et al. (2015). This was originally attached to a poly- a concave arc. Based on the remaining part of the metallic nodule. It now consists of one half of the holotype (Fig. 2A, B), the test measured 26.5 mm plate-like test, the other half having been used for high from the top of this arc to the upper mar- scanning electron microscopy (SEM). The follow- gin of the test and 30.0 mm from the base of the ing points supplement the original description. They plate to the upper margin. The width of the test are based on photographs of the freshly collected measured in a straight line from side to side of specimen (Fig. 1; Supplementary Material Fig. S1), the plate was ∼29 mm (Fig. 1B). However, when and a re-examination of the remaining part of the measured around the curvature of the plate it was holotype (Fig.
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