Xenophyophores are giant protists that are confined to habitats deeper than 500 m and build agglutinated tests up to 10 cm or more in size (Fig. 12-1). According to recent molecular studies, at least two xenophyophore species are foraminiferans (Pawlowski et al. 2003; Lecroq et al. 2009a). They occur at bathyal, abyssal and hadal depths, but are most common where the particle flux to the sea floor is enhanced under productive regions, in canyons, on areas of raised topography such as seamounts and ridges, or on continental slopes (Tendal 1972; Levin 1994). Some species attach to hard substrates, but many live in soft sediments primarily as epifaunal forms, although there are some infaunal species. On seamounts and some slopes, the epifaunal species can be the most visually conspicuous and abundant large organisms on the ocean floor. Fist-sized tests of Reticulammina and Syringammina, which reach densities of 1–36 individuals per m2 on continental slopes and seamounts (Fig. 12-2), can represent an important source of habitat heterogeneity (Levin et al. 1986; Levin 1991; Levin & Gooday 1992; Hughes & Gooday 2004).
Figure 12-1. Xenophyophores from soft and hard substrate on eastern Pacific seamounts. (E) Galatheammina with an asteroid aboard.
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Figure 12-2. (A) Xenophyophores (Syringammina) at 1250 m, NW Atlantic margin; Photograph by B. Hecker. (B) Foraminifera (Bathysiphon filiformis) at 850 m on the margin off North Carolina, USA (C) Gromia sphaerica on the Oman margin; photograph by C. Smith and D. Hoover. (D) Xenophyophores (Reticulammina) from Nazare Canyon (4300 m Portuguese margin). (E) Xenophyophore Reticulamina sp. Porcupine Abyssal Plain, NE Atlantic (4850 m) with associated isopod. (F) Xenophyophore (Syringammina fragilissima) from Rockall Trough (950 m NE Atlantic).
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There are two xenophyophore orders, the Psamminida with rigid tests, and the Stannomida, characterised by proteinaceous threads that ramify the soft, flaccid test. The test morphologies range from spherical to plate-like or tubular, but more complex, branched, folded or reticulated morphotypes are also common among the psamminids. These complex forms in particular provide a variety of microhabitats for smaller organisms. Xenophyophore tests typically extend several centimeters above the surrounding level bottom, thereby providing their pseudopodia with access to enhanced water current velocities and enhancing their potential for suspension feeding and particle trapping. Documentation of 234Th inventories in tests 3–17 times above background sediment on seamounts, suggests that the baffle-shape of the psamminid tests entrains fine, organic-rich particles, and possibly larvae as well (Levin & Gooday 1992).
The internal organisation of xenophyophores includes branching, multinucleate cytoplasm enclosed within an organic tube (called the granellare system) and faecal pellets (stercomata) retained within the test as distinct masses (‘stercomare’) that are enclosed within an organic sheath to form the stercomare system (Tendal 1972). In many xenophyophores, the test interior is full of agglutinated particles, but more ‘advanced’ forms are hollow, apart from the stercomare and granellare. This test structure provides four distinct microhabitats that can be inhabited by foraminiferans and other taxa. Animals can live (i) within the remains of the organic tubes of the xenophyophore granellare system, (ii) within the branches of the test, but outside the granellare tubes, (iii) attached to the outer surface of the test, or (iv) in mud trapped between the test branches (Hughes & Gooday 2004).
Figure 12-3. Arborescent foraminifera. (A) Pelosina sp., Pakistan margin, Arabian Sea (1000 m). (B) Same site showing grape-like gromiids (Gromia pyriformis) attached to branches. (C) Pelosina sp. from Nazare Canyon, Portuguese margin (1415 m). (D) Pelosina sp. from North Carolina margin (850 m). E) Unidentified species attached to dropstone, BIOTRANS site (4550 m). (F) Arborammina hilaryi Madeira Abyssal Plain (4950 m).
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Figure 12-4. (A) The bryozoan Nolella intergrown with the komokiacean Lana sp.(NW African margin, 4450 m), (B) Gromiid Gromia sphaerica with network of foraminiferan Telammina on surface (1850 m, Pakistan margin). (C) Vanhoeffenella with nematode (3500 m, Weddell Sea). (D,E) Tubular foraminiferans with sipunculan worms [NE Atlantic: (D) Hyperammina sp. from 1857 m, Whittard Canyon; (E) Bathysiphon rusticus from 4000 m off NW Africa]. (F) Bathysiphon rusticus with ischnomesid isopod (4000 m off NW Africa).
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The tests of large, epifaunal xenophyophores, particularly those with complex, reticulated or folded morphologies, (Figs 12-1 and 12-2E) harbour many different kinds of metazoans and protozoans and appear to constitute faunal ‘hotspots’ within deep-sea sediments (Levin 1991, 1994). There is a positive relationship between test size and number of metazoan inhabitants in xenophyophores from Eastern Pacific seamounts, and it is on coarse substrates that their contribution to faunal heterogeneity is believed to be greatest (Levin & Thomas 1988).
Many taxa live within the interstices of xenophyophore tests (Table 12). Twenty-seven tests from Pacific seamounts yielded 153 macrofaunal and 333 meiofaunal individuals. The isopod Hebefustis sp., which occurred in ‘family’ groupings within tests but were not present outside the tests, is a possible obligate associate. In addition, densities of tanaids, isopods, ophiuroids, nematodes, harpacticoid copepods and ostracods (but not polychaetes) were enhanced in sediment beneath and around the seamount xenophyophore (Levin & Thomas 1988). Hughes & Gooday (2004) analysed rose-Bengal stained (i.e.‘live’) foraminifera associated with dead tests of the large xenophyophore Syringammina fragilissima in the Rockall Trough (NE Atlantic; 950 m water depth). This species builds a test with hollow branches that anastomose to form a complex, reticulated structure (Fig. 12-2F). Four tests yielded, in total, 3647 rose-Bengal-stained foraminiferal specimens representing 259 species, with 352–2238 specimens and 63–153 species found in each test. Many were common bathyal species that also occurred in the surrounding sediment. However, others, including the organic-walled monothalamous Cylindrogullmia sp. and the calcareous Chilostomella elongata, were more or less confined to the xenophyophores. The Syringammina tests also yielded between 175 and 1217 metazoans per test (total 2829) (Table 12). Nematodes, the dominant taxon, were identified to genus level (Van Gaever et al. 2004). Each test yielded 29–59 genera, significantly fewer than in the underlying or adjacent sediments. Among those present in the xenophyophores but rare in the adjacent sediment were Syringolaimus, Viscosia and Paracanthonchus. These are all large nematodes with prominent teeth, suggesting that they are predators. Other dominant taxa associated with Syringammina tests, such as Trefusia, Halalaimus and Acantholaimus, were also found in the sediments, albeit in lower relative abundances. The nematodes showed a high variability with different dominant genera (Syringolaimus, Trefusia and Halalaimus-Acantholaimus) present in each of the three tests. Thus, large xenophyophore tests can provide a microhabitat for particular nematode taxa that are less prominent, or even absent, in adjacent deep-sea sediments.
Table 12. Associations between protozoans and other organisms. Numbers indicate specimens of particular protozoan and metazoan taxa associated with the different species.
|Pacific speciesa||Syringamminab||Aschemonellac||othersd||tubular (inside)e||tubular (outside)f||Pelosinag||Vanhoeffenellah||Komokii||Gromia spp.j|
| bryozoans||–|| ||–||*||–||–||–||–||*||–|
| other peracarids||8||11||–||–||–||–||–||–||–||–|
| ophiuroids||40|| ||–||–||–||–||–||–||–||–|
| other taxa||4||4||–||–||–||–||–||–||–||–|
Other agglutinated foraminifera, particularly those with large tubular tests (e.g. Bathysiphon, Hyperammina, Rhabdammina, Pelosina), often harbour metazoans and other protists, while their exterior surfaces provide substrates for sessile organisms, notably other foraminifera, but also polychaetes (Table 12, Figs 12-3 and 12-4A,D–E). On some continental margins, tubes of Bathysiphon, Hyperammina and Rhabdammina, many of them dead, accumulate in large quantities at the sediment surface (Linke & Lutze 1993; Gooday et al. 1997). We speculate that these thanatocoenoses provide an important source of habitat structure for metazoans, particularly vermiform and sessile taxa. Smaller foraminifera can also provide habitat structure; for example, monothalamous tests of Vanhoeffenella gaussi are sometimes occupied by juvenile nematodes (Hope & Tchesunov 1999) (Fig. 12-4C). Even gromiids, close relatives of the foraminifera, can be colonised by other organisms, notably sessile foraminifera, despite the fact that they have smooth, organic test walls (Aranda da Silva & Gooday 2009; Fig. 12-3C). Komokiaceans can also harbour metazoans, including the ctenostome bryozoans, which intergrow with the tubules of these large foraminifera (Gooday & Cook 1984) (Fig. 12-3B).
Few experimental studies address the nature of interactions between large agglutinated protozoans and their metazoan and protozoan associates. Provision of substrate, enhanced food supply, refuge from predators, nursery habitat and breeding habitat have all been suggested as benefits to biota associated with large, agglutinated tests in the deep sea (Levin et al. 1986; Levin 1991). It is also possible that some foraminifera or animals present within or beneath tests were passively entrained from the overlying water as larvae or propagules.
Associations between large protists and microbiota may take many forms. Tendal (1972) proposed that xenophyophores garden bacteria within stercomes. Enhanced respiration rates (Deming unpublished in Levin & Gooday 1992), together with elevated bacterial fatty acids within xenophyophores (Laureillard et al. 2004), support this hypothesis. A recent molecular study suggests that komokiaceans are hotspots of microbial diversity. Lecroq et al. (2009b) detected DNA sequences attributable to Radiozoa, Haplosporidia, dinoflagellates, diatoms, fungi and Apusozoa associated with komokiacean foraminifera (Septuma, Normanina). They suggested that at least some of these organisms were inhabitants of the komokiaceans. Fungal sequences, for example, were confined to the komokiaceans and absent from the surrounding sediment.