P.P Shirshov Institute of Oceanology
Two groups of deep-sea protists (unicellular eukaryotes) include species of megafaunal size, the gromiids and xenophyophores, both of which are members of the 'supergroup' Rhizaria. Another group, the komokiaceans, are mainly of macrofaunal size and rarely if ever visible in seafloor photographs.
This group of amoeboid protists is characterised by a relatively simple single-chambered organic test, resembling those of 'allogromiid' foraminifera. Within the Rhizaria, molecular data clearly distinguishes them from the foraminifera. However, there has been considerable debate about their relationship to other rhizarians (Rothe et al., 2009). The most recent classification places them within the Cercozoa (Adl et al., 2012). All gromiids are currently accommodated within Gromia, but additional genera may be required as knowledge of the group increases. Gromiids differ from foraminifera in having generally branching, rather than anastomosing, pseudopodia, and in their test wall structure, which includes a distinctive layer of 'honeycombe membranes' visible only by transmission electron microscopy (Hedley and Wakefield 1969). The test has an oral capsule, an often prominent mound-like or nipple-like structure through which the pseudopodia emerge (Hedley 1960; Rothe et al., 2010). This is the main feature visible with a light microscope that distinguishes dead or preserved gromiids from organic-walled monothalamous foraminifera ('allogromiids'). Some species are also considerably larger (>1 cm) than any 'allogromiids'.
For many years, gromiids were believed to be confined to coastal and sublittoral settings and were generally identified as Gromia oviformis Dujardin 1835. The first deep-sea species was discovered in the Arabian Sea in 1994 (Gooday et al., 2000). Since then, it has become apparent that the group is common and diverse in the deep sea, particularly on bathyal continental slopes (Gooday and Bowser 2005; Aranda da Silva et al., 2006, 2009; Matz et al., 2008; Rothe et al., 2009, 2010). The vast majority of these species are undescribed. They are distinguished mainly by their test morphology; common morphotypes range from spherical, grape-shaped, pear-shaped and oval to more elongate and sometimes very elongate, sausage-shaped forms (Aranda da Silva et al., 2006; Rothe et al., 2010). In some of the elongated species, the proximal part of the test is inflated (bulbous) compared to the distal part. There is usually a single aperture (oral capsule) but multiple apertures are present in a few species. Other features that can be used to distinguish species include the thickness of the test wall (and in a few cases its surface ornamentation) and the size and morphology of the oral capsule (Rothe et al., 2010). Many are too small (a few millimetres in length) to be seen in seafloor photographs. Gromia spherica, a spherical species that can reach a diameter of several centimetres, is the only species likely to be clearly visible (Gooday et al., 2000; Matz et al., 2008). Objects resembling G. spherica appear in a few photographs from the CCFZ. Some larger elongate morphotypes with maximum dimensions of > 1 cm are discernible in seafloor images from the Arabian Sea (Gooday et al., 2000) but have yet to be recognised in the CCFZ.
Reticulate morphotype 8. Reticulammina sp. 2
Plate-like morphotype 5
Other forms morphotypes
These giant protists have tests reaching dimensions of 10-15 cm or more. The first species were described in the late 19th Century (Brady 1883; Haeckel 1889), since when they have been variously classified as foraminifera, sponges, or members of a distinct protistan group (Tendal 1972). However, recent molecular analyses place at least some species firmly within the radiation of monothalamous foraminifera (Pawlowski et al., 2003, 2013; Lecroq et al., 2009; Gooday et al., 2011). Most xenophyophores have tests consisting of agglutinated particles, termed 'xenophyae'. These are often the shells of planktonic foraminifera, radiolarians or other biogenic particles (e.g. sponge spicules) or mineral grains. When xenophyophore tests are broken open, they exhibit a number of distinctive internal features. The cell body (the cytoplasm) is enclosed within an organic tube, these two elements together comprising the 'granellare' system. The cytoplasm is multinucleate and contains numerous mineral particles, usually crystals of barite (Hopwood et al., 1996) although other heavy minerals, notably rutile, dominate in at least one species (Rothe et al., 2011). Stercomata, small pellets of waste material (mainly clay particles), accumulate in large masses enclosed within an organic sheath. These lumpy or string-like masses are termed 'stercomare'; they are dark in colour. in contrast to the pale whitish or yellowish granellare branches. The interior of xenophyophore tests therefore often has a very distinctive appearance, unlike that of other foraminifera.
Following Tendal (1972), we recognise two main xenophyophore groups. In stannomids (order Stannomida of Tendal 1972; 16 species in 2 genera), the tree- or plate-like test is typically soft and flexible, although possibly more rigid in some species, and ramified by proteinaceous fibres called linellae. In psamminids (order Psamminida in Tendal 1972; 46 species in 16 genera), the test is generally rigid and encompasses a wide variety of morphotypes, including irregular lumps, spheres, simple plates, contorted plates, hemispherical structures consisting of reticulated plates, simple tubular structures and structures composed of reticulated tubes. Family-level groups within the psamminids are distinguished mainly by the way in which the xenophyae are distributed between the outer part and the interior of the test (Tendal, 1972). The family Psammetidae includes the simplest types. The test is massive and the xenophyae are arranged haphazardly to form a solid structure with no specialised surface layer or large openings. In the family Psamminidae, the test usually forms a solid, sometimes fragile, structure with the external xenophyae forming a surface layer and the interior occupied by a looser mass of internal xenophyae as well as granellare and stercomare. In the family Syringamminidae, the fragile test is composed of agglutinated tubes in which the xenophyae are restricted to the test wall, so that the interior contains only stercomare and granellare. Finally, members of the family Cerelasmidae have a fragile, relatively soft test organised as a system of anastomosing branches with varying quantities of xenophyae arranged with no obvious order and embedded in fine-grained ‘cement’.
As they are in some other abyssal areas (Tendal and Gooday, 1981; Gooday et al., 2011), xenophyophores are among the most common megafaunal organisms visible in seafloor photographs taken in the CCFZ (Kamenskaya et al., 2013). Certain species and genera can be identified with some confidence. The identification of distinctive, tree-like tests, often attached to nodules, as Spiculammina delicata has been confirmed by the collection of specimens (Kamenskaya 2005). Hemisphaerical morphotypes with a reticulated surface structure consisting of meshwork of bar-like elements that delimit open spaces can be assigned to the genus Syringammina. Morphologically very similar forms have been collected and described as Syringammina species in the SW Pacific and NE Atlantic (e.g. Tendal and Lewis 1978; Richardson 2001). Hemisphaerical morphotypes consisting of plate-like elements that tend to anastomose are very similar to some species of Reticulammina collected from east Pacific seamounts (Levin and Thomas 1988) and the Portuguese margin (Gooday et al., 2011). An erect, fairly flat, plate-like morphotype with a curved margin has been collected; the test structure suggests a placement in the genus Psammina (Kamenskaya et al., 2013, Fig. 6b).
In the absence of a characteristic test morphology or of collected specimens, it is more difficult to place morphotypes into genera or families since identification depends on test structure, particularly the degree of development of a distinct surface layer of xenophyae. This applies particularly to the wide variety of basically plate-like morphotypes, which are common in the CCFZ. These include forms in which the plates are contorted or have side branches, or have complex morphologies comprising crenulated plate-like elements that don't anastomose. These could represent Psammina or Galatheammina, or more likely one or more undescribed genera. The genus Psammina is currently defined as having a discoidal test composed of two firmly cemented plates of external xenophyae, with the internal xenophyae forming pillar-like structures between the plates, and with large 'pores' (apertures?) opening around the margin (Tendal, 1972). Most of CCFZ forms are not simple plates, and so placement in Psammina would require a redefinition of this genus, or more likely the establishment of one or more new genera. Galatheammina is not well-defined morphologically. The genus currently encompasses lumpy, plate-like and branched (tetrahedral) morphotypes that have a similar test construction and lack the more distinctive morphologies of Psammina and Reticulammina (Tendal 1972; Gooday and Tendal 1988). It would probably be impossible to assign xenophyophores to this genus based only on seafloor photographs, except perhaps in the case of the tetrahedrally-shaped G. tetraedra (Tendal 1972).
Hemispherical structures from ~7,800 m in the New Britain Trench with smooth or somewhat uneven surfaces were identified by Tendal (in Lemche et al., 1976) as species of Psammetta (family Psammettidae). He also compared more irregular ('lumpy, more or less oblong...rounded') structures at this and other hadal sites in the western Pacific to xenophyophores in the family Cerelasmidae. Around half of the structures were surrounded by a star-shaped pattern of radiating lines that Tendal interpreted as pseudopodia or their traces. Such features have not been observed around xenophyophores in seafloor photographs from the CCFZ, or any other deep-sea area. They were not evident in a time-lapse photographic record of xenophyophore in the abyssal NE Atlantic (Gooday et al., 1993).
Stannomid xenophyophores are particularly common in the eastern Pacific (Tendal 1972, 1996), and will undoubtedly be collected in the CCFZ, but their identification in bottom photographs is problematical. Members of this group have a test that is flexible to varying degrees. Tendal (1972) presents arguments for believing that the most common species, Stannophyllum zonarium, is too soft to stand upright and probably lies flat on or just below the seabed. Tendal (in Lemche et al., 1976) identifies flat-lying, rounded 'flake- or plate-like structures' at >8000 m in the Palau Trench as a similar species, Stannophyllum mollum. He goes on to point out resemblances between structures comprising a basal plate and upstanding side plates or excrescencies from the abyssal NW Pacific and Stannophyllum granularium. Tendal (in Lemche 1976) also tentatively identifies branched organisms seen in photographs from hadal depths in the western Pacific as species of Stannoma. Some of these structures (particularly those identified as Stannoma cf. dendroides) could also be interpreted as Spiculammina.
In summary, xenophyophores are common and diverse in the CCFZ, occurring both on soft sediments and attached to nodules. At least 25 morphotypes have been recognised in photographs and additional species are identified in the literature on the basis of collected specimens. A few morphotypes can be identified with some certainty to genus, or even species from photographs. In most cases, however, identification to genus or family depends on test features that are only discernible in collected specimens.
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