Xenophyophorea

Introduction

Single-celled organisms are generally required to maintain microscopic sizes. Xenophyophores, immobile shell-making mud-stickers, however, brazenly ignore all requirements of general microbial decency by attaining sizes not merely macroscopic, but positively enormous (at least by unicell standards). One of the largest species, Stannophyllum venosum Haeckel 1889, is a broad flat form up to 25 cm across, although only about a millimetre thick.  Tendal 1972).

Despite such impressive dimensions, mention of them is likely to garner blank looks from most of the general public, and even from many biologists who probably should know better. This is because xenophyophores are restricted to the deep sea, not usually regarded as a prime holiday destination. Those that are occasionally pulled up from below are probably not recognised. Like benthic Steptoes, xenophyophores surround themselves with all sorts of junk they find lying around, which they use to make their shells, stuck together with a cement of polysaccharides. Id. Foraminiferan and radiolarian shells, sponge spicules, mineral grains – all are potential building materials (though individual species are often quite picky with regard to exactly what they use, and some species eschew foreign particles altogether). The particles used are referred to as xenophyae. When the fragile test is brought up, these particles tend to all fall apart, and are hence not recognised as having once been part of a larger whole.

Image: Syringammina from the web page of J. Alan Hughes.

© 2004 Christopher Taylor CT041222

Description

The xenophyophore cell itself is organised as a series of branching tubes, which in the eternal quest for excess jargon, are referred to as granellare. The cell is multinucleate, with nuclei evenly distributed throughout the cytoplasm. The other obvious feature of the cell is the presence of numerous crystals (called granellae) of barite (BaSO₄) probably secreted by the xenophyophore itself. The point of all this is unknown (Hopwood et al., 1997), though it may be to remove toxic barium solutions ingested while feeding. Tendal (1972).

Xenophyophores also produce long branching strings of faecal matter (stercomare) that are retained in the test. In some species this can make up a significant part of the test, and those species that do not collect xenophyae live out their lives in a home made entirely of their own shit.

Xenophyophores live attached to the sea-bottom, mostly above the surface except the infaunal Occultammina. They are probably suspension or filter feeders, with some extraction of food particles from the surrounding mud. Levin 1994); Riemann et al. (1993). It has been suggested that they garden microbes in the stercomare for food, but there are no actual data to support this. Xenophyophores appear to be a significant part of the benthic ecology, with large numbers of organisms living on, in and around the microenvironments created by test aggregations. Levin (1994). Beyond the production of biflagellate gametes, the reproduction of xenophyophores is still obscure, and the details have not been established by Peeping Tom biologists. Tendal (1972).

© 2004 Christopher Taylor CT041222

Phylogeny

The affinities of xenophyophores have generally been obscure. A large number of species were originally described by Haeckel as sponges. Other workers at the same time regarded them as agglutinated foraminifers. Other suggested relatives were slime moulds or testate amoebae currently included in Cercozoa. Tendal (1972). A recent molecular phylogeny including a single xenophyophore, Syringammina corbicula, found it nested with a fair degree of support among basal Foraminifera, amongst a clade of sessile species with agglutinated tests such as Rhizammina. Pawlowski et al. (2003).

It would be expected that organisms the size of xenophyophores would have an extensive fossil record. So far, though, they've got squat. This is probably due to the same problems as with recognising modern examples – like a political coalition party, xenophyophore tests are constructed of many disparate elements welded together for protection, often without anything to obviously connect them.

Levin (1994) describes a number of attempts to recognise fossil xenophyophores. Similarities have been noted between the pattern formed on the sediment surface by the infaunal Occultammina and the form of graphoglyptid 'traces' like Paleodictyon – suggesting that some of these may be fossil xenophyophores rather than animal feeding traces. However, graphoglyptids do not show evidence of xenophyae, and are often a lot more regular and symmetrical than expected for xenophyophores.

Maybury & Evans (1994) suggested that some Carboniferous fossils previously identified as phylloid 'algae' (alga – term often used by Palaeozoic palaeontologists to refer to any sessile organism that can't be made to fit anywhere else) might be xenophyophores, citing similar in structure and form, and a higher concentration of barium in the fossils than the surrounding matrix. Torres (1997) disputed this, suggesting that the similarity of structure, when looked at closely, wasn't all that obvious, and also highlighting Maybury and Evans' own caveat that the barium concentration might be the result of barium replacing calcium in preservation.

So to date, the xenophyophore fossil record is marked by a lot of wishful thinking, but few definite results – another opportunity for the coalition party analogy?

© 2004 Christopher Taylor CT041222

Systematics

The Xenophyophorea, like many Eukarya, have gone by a variety of names: Arxenophyria, Domatocoela, Psamminidea, Psammininae, Xenophiophorae, Xenophyophora, Xenophyophoria, Xenophyophorida, and Xenophyophoridae.  They are rather unevenly divided between two easily distinguishable groups (Tendal, 1972). No attempt has been made to reconstruct the phylogeny of Xenophyophorea, and each of the constituent families (which are essentially form-taxa) may or may not be monophyletic. In particular, linellae are a feature unique to Stannomida among all eukaryotes, and so probably an apomorphy of them. As Psamminida are defined by the absence of linellae, it is entirely possible that it could turn out to be paraphyletic with regard to Stannomida.

S. coralloides Haeckel 1889 [= Stannoplegma coralloides]  

Xenophyophorea incertae sedis: Ammoclathrinidae. This family was described in 1889 by Haeckel (as Ammoconidae, but as this was based on a preoccupied genus name, a replacement name was supplied by Tendal, 1972) as sponges in his 'Deep-Sea Keratosa'. Ammoclathrinidae are composed of tubules that are single or branched with free or anastomosing branches. Tube walls have simple pores and are constructed of radiolarian and foraminiferan tests, sand grains and/or fragments of sponge spicules, connected by a cement of some kind. The total body is up to 20 mm in diameter. Haeckel's material is missing, and was probably destroyed over the course of his investigations. No specimens have been recorded since. The nature of Ammoclathrinidae is therefore unknown. The other 'Deep-Sea Keratosa' now comprise the xenophyophores, and the tubular form and construction from foreign particles of Ammoclathrinidae are reminiscent of xenophyophores. However, after dissolving away the calcareous material of the test of members of all three genera with acid, Haeckel recorded the presence of a possible epithelium of small granular cells, as well as small stellate cells and larger amoeboid cells. If multicellular, Ammoclathrinidae would be unlikely to be xenophyophores. For now, I include Ammoclathrinidae tentatively in the Xenophyophorea. In doing so, I am assuming that Haeckel mistook parts of a multinuclear plasmodium for separate cells, perhaps as a result of preparation effects of the acid.

Systematics References:  Gooday 1991), Gooday (1996), Gooday & Tendal 1996), Levin (1994), Riemann et al. 1993), Tendal (1972).