Porcelain Fans

Mature specimen of Rhapydionina deserta, from Loeblich & Tappan (1964).

Calcareous foraminiferans have been featured on this site before: planktic floaters, living stars, microscopic jelly moulds and gigantic reef-formers. All these forms have belonged to the group of calcareous forams known as the rotaliids. Today's subject is another group of forams, the Rhapydionininae, belonging to a different calcareous group, the Miliolida. Miliolids may have shell walls made of calcite like the rotaliids, but differ in the wall structure: while the walls of rotaliids are glass-like and porous, those of miliolids are structured like porcelain. Phylogenetic studies of forams have not placed the miliolids close to the rotaliids, and the two groups seem to have evolved their secreted shells independently (Sen Gupta 2002).

Rhipidionina liburnica, from Loeblich & Tappan (1964).

The Rhapydionininae were defined by Loeblich & Tappan (1964) as a group of miliolids with a conical test composed of broad chambers stacked one on top of another (the overall shape being kind of like a fan or an ice-cream cone), with each of these chambers subdivided by internal septa into multiple chamberlets (the difference between a 'chamber' and a 'chamberlet' being that the latter are not completely divided from each other by the walls). The opening of the test took the form of a sieve-like array of pores at the top end. However, subsequent researchers have discovered that Loeblich & Tappan's definition was inadequate. Rhapydioninines start life growing as a flat spiral, with growth becoming linearised at maturity. However, it turns out that not all Rhapydionininae become linear; some retain their juvenile coiling into maturity (Vicedo et al. 2011). At least some species are believed to have both a linear megalospheric form and a coiled microspheric form. To explain, forams can be divided between microspheric forms, in which the first chambers of a new test are much smaller, and megalospheric forms with larger initial chambers. In those relatively few forams whose life cycles have been studied in detail, these two forms correspond to an alternation of generations, with a mostly microspheric asexually-reproducing generation giving rise to the generally megalospheric sexually-reproducing phase. Loeblich & Tappan's (1964) concept of rhapydionines, therefore, would have potentially placed members of a single species into separate families.

Diagram of internal structure of two adult chambers of Cuvillierinella, from Vicedo et al. (2011). Key to abbreviations: ap f = apertural face, c chl = cortical chamberlets, flo = floor, m chl = medullar chamberlet, prp = preseptal space, rpi = residual pillars, s = septum, sl = septulum.

Rhapydionines are best known as fossils, with a definite range from the Upper Cretaceous to the mid-Eocene (Loeblich & Tappan 1984). Believe it or not, whether there are still rhapydioninines in the world is something of an open question. Loeblich & Tappan (1964) listed two Recent genera in the Rhapydionininae, each represented by only a single known specimen. Ripacubana conica was originally described from sand deposits in Cuba; however, Loeblich & Tappan (1964) suggested that Ripacubana may actually represent what has been referred to as a 'zombie taxon'. Some of you may be familiar with the palaeontological concept of a 'Lazarus taxon', where a species disappears from the fossil record only to reappear at a later date. What has actually happened in these cases is that the species had only become locally extinct, but survived in some other locality that has not been preserved, subsequently recolonising its old range. A 'zombie taxon', however, is one that has genuinely become extinct at the earlier date, but its fossilised remains have since been transported into a younger sediment deposit, giving the impression that it survived later than it did*. In the case of Ripacubana, it is difficult to know just how long a foram shell buried in sand has been lying there.

*Identifications of Lazarus taxa also have to be on the look-out for 'Elvis taxa': where the more recent population does not in fact represent the same species, but a different species that has convergently evolved similar features.

Craterites rectus, from Loeblich & Tappan (1964).

Loeblich & Tappan (1964) did not express the same reservations about Craterites rectus, described from a beach on Lord Howe Island east of Australia. Craterites was later separated as its own subfamily by Loeblich & Tappan (1984) on the basis of its being attached to the substrate, and so differing from other free-living Rhapydionininae. Nevertheless, they kept the two subfamilies together as the family Rhapydioninidae, so Craterites may still be the only known survivor of the rhapydioninine lineage. However, with only one known specimen, the details of the internal structure of Craterites remain unknown.

REFERENCES

Loeblich, A. R., Jr & H. Tappan. 1964. Treatise on Invertebrate Paleontology pt C. Protista 2. Sarcodina, chiefly "thecamoebians" and Foraminiferida, vol. 1. The Geological Society of America and The University of Kansas Press.

Loeblich, A. R., Jr & H. Tappan. 1984. Suprageneric classification of the Foraminiferida (Protozoa). Micropaleontology 30 (1): 1-70.

Sen Gupta, B. K. 2002. Modern Foraminifera. Springer.

Vicedo, V., G. Frijia, M. Parente & E. Caus. 2011. The Late Cretaceous genera Cuvillierinella, Cyclopseudedomia, and Rhapydionina (Rhapydioninidae, Foraminiferida) in shallow-water carbonates of Pylos (Peloponnese, Greece). Journal of Foraminiferal Research 41 (2): 167-181.

Acervulinids: Reef Forams

Regular readers of this site will know that, contrary to common belief, not all representatives of the vaguely defined category of organisms known as 'protozoa' are too small to be seen with the naked eye. Some are very visible indeed, and many of the more visible forms can be found among the shell-constructing amoeboids known as Foraminifera. One group of giant forams, the xenophyophores, has become fairly famous in internet circles as one of the contenders for the title of 'largest single cell', though, as noted in the post linked to, the question is kind of a pointless one with regard to forams. Besides, as described later in this post, xenophyophores may not have even have always been the largest forams.

Encrusting nodules of Acervulina inhaerens from Rhodes, from M. Hesemann.

The Acervulinidae are a family of reef-inhabiting forams belonging among the rotaliids. Juvenile chambers of newly growing acervulinids are arranged in a flat spiral, but chambers of mature specimens may be arranged in one to several layers. The chambers do not have regular apertures, and instead their walls are only pierced by coarse pores (Perrin 1994). Genera and species of acervulinids are distinguished by the presence, arrangement and shapes of layers and chambers, but defining distinctions appropriately is challenging. Acervulinids do not have a determinate 'adult morphology'; instead, the final adult appearance can be affected by factors such as substrate relief and water movement. Properly identifying acervulinids therefore requires identification of features independent of these external factors.

Living crust of Gypsina plana, photographed by Hal Ray Tichenor.
Acervulinids can be abundant on tropical coral reefs, and may play a not insiginificant role in reef formation as binding organisms. They tend to be particularly prominent in deeper parts of the reef, as they can tolerate lower light levels than other organisms such as coralline algae; in shallower parts of the reef, they are found in more cryptic locations among the coral. Acervulinids may be free-living, or they may be directly attached to their substrate. Like the star-shaped calcarinids, their primary food source is benthic diatoms (that they may or may not live with symbiotically), and the abrupt disappearance of the modern Acervulina inhaerens below depths of 130 m probably corresponds to the lower limit of that food source (Bosellini & Papazzoni 2003).

Fossilised nodules from a Solenomeris reef, photographed by Stefano Dominici. Note that Stefano identifies these as Acervulina; due to the complications in distinguishing acervulinid taxa, it remains contentious whether Solenomeris and Acervulina can be reliably separated.

Attached acervulinids may form either nodules or spreading crusts, depending on species and/or growth conditions (Perrin 1994). Such nodules or crusts may have diameters in the millimetre range, but some living species may be within the decimetre range. The most dramatic expression of acervulinid potential, however, was known from the Tethyan region during the Eocene period (the Tethys, for those unfamiliar with it, was the sea that connected the Atlantic and Indian Oceans north of Africa, before the northward movement of that continent closed off the Mediterranean at the eastern end). Here was found Solenomeris ogormani, initially interpreted as a red alga but since reidentified as an acervulinid. Solenomeris was primarily an encrusting form, but large growths would also produce tightly packed branches one or two centimetres in diameter. Over time, Solenomeris formed massive metre-sized domes, and these domes together would form entire reefs stretching over multiple kilometres: reefs formed not of coral, or of algae, but purely of forams!

REFERENCES

Bosellini, F. R., & C. A. Papazzoni. 2003. Palaeoecological significance of coral−encrusting foraminiferan associations: a case−study from the Upper Eocene of northern Italy. Acta Palaeontologica Polonica 48 (2): 279-292.

Perrin, C. 1994. Morphology of encrusting and free living acervulinid Foraminifera: Acervulina, Gypsina and Solenomeris. Palaeontology 37 (2): 425-458.

The Osangulariidae: Deep-Water Trochospires

Dorsal (spiral side), lateral and ventral (umbilical side) views of an Osangularia specimen, from here.

For today's post, I'm presenting for your consideration the Osangulariidae, a family within the rotaliid Foraminifera (see here for my post introducing the Rotaliida). These are benthic forams, mostly found in intermediate waters within the top few centimetres of sea floor sediment (Kaiho 1998). The Osangulariidae were first established as a distinct family of Foraminifera by Loeblich & Tappan (1964) to include trochospiral forams with bilamellar walls, with an important distinguishing feature separating osangulariids from related families being their granular rather than radial test wall structure. However, Loeblich & Tappan were criticised by Kaiho (1998) for their utilisation of this character. In developing a more lineage-based classification of the osangulariids and related taxa, Kaiho concluded that "radial-granular texture has no taxonomic significance in the suprageneric classification of calcareous trochospiral benthic foraminifera". Instead, Kaiho defined the Osangulariidae as trochospiral forams with an aperture on the umbilical side of the test, an angular periphery and strongly oblique sutures on the spiral side.

The Coniacian (Late Cretaceous) Globorotalites multisepta, from Loeblich & Tappan (1964).

The Osangulariidae first appeared in the Early Cretaceous, during the Aptian epoch. Kaiho (1998) recognised two subfamilies within the Osangulariidae, the Osangulariinae and the Globorotalitinae (not to be confused with the Globorotaliinae), regarding the slightly earlier-appearing Globorotalitinae as probably ancestral to the Osangulariinae. The Globorotalitinae possessed a test with a strongly inflated umbilical side, and can basically be described as looking like a jelly mould. Osangulariids of the globorotalitine type became extinct during the Palaeocene.

Nuttallides rugosus, from Todd 1965.

The Osangulariinae, on the other hand, have survived to the present day. Their most obvious distinction from the Globorotalitinae is the reduction of the umbilical side of the test, so that osangulariines tend to be more discus-shaped than jelly-mould-shaped. The earliest osangulariine genus, Protosangularia, appeared in the Aptian and survived until the Cenomanian in the early Late Cretaceous. At the end of the Cenomanian, a major anoxic event took place in the ocean followed by a reduction in world ocean temperatures. After this, Protosangularia was replaced by a number of other osangulariine genera appearing from the Turonian to the early Campanian (Kaiho 1998). Two of these genera, Osangularia and Nuttallides, are the family's modern representatives.

REFERENCES

Kaiho, K. 1998. Phylogeny of deep-sea calcareous trochospiral benthic Foraminifera: evolution and diversification. Micropaleontology 44 (3): 291-311.

Loeblich, A. R., Jr & H. Tappan. 1964. Treatise on Invertebrate Paleontology pt C. Protista 2. Sarcodina. Chiefly "thecamoebians" and Foraminiferida vol. 2. The Geological Society of America and The University of Kansas Press.

The Rotaliida: Building a Wall

Tests of Elphidium crispum, photographed by Spike Walker.

The foraminifers have been featured on this site a number of times before, when various members of this diverse group of unicellular organisms have been introduced. Today, I thought I'd take a look at the broader classification of forams through the lens of one of their major subgroups, the rotaliidans.

The earliest classifications of forams divided them on the basis of the number and arrangement of chambers within the test, but over time the composition of the test walls came to be also recognised as an important feature (Haynes 1990). This reached an apotheosis of sorts in the Treatise on Invertebrate Paleontology classification of Loeblich and Tappan (1964), in which the forams were divided between five suborders primarily on the basis of test composition. These were the Allogromiina (with membranous or chitinous tests), Textulariina (with agglutinated tests) and three suborders with calcareous tests but differing wall structures: the microgranular Fusulinina, the porcelaneous, imperforate Miliolina and the hyaline, perforate Rotaliina (other authors would treat these groups as orders, with the suffix -ida instead of -ina). However, later authors (including Loeblich and Tappan themselves) regarded this classification as somewhat oversimplified, and divided groups such as the planktonic rather than benthic Globigerinida, the aragonitic rather than calcitic Robertinida, the Lagenida with monolamellar rather than bilamellar walls, and the high-spired or serial rather than planispiral Buliminida from the Rotaliida proper (Haynes 1990). However, many of the subdivisions within forams remained somewhat artificial, and potentially did not reflect true evolutionary relationships.

Bulimina marginata, photographed by Fabrizio Frontalini.

Molecular phylogenetics of forams got off to a fairly rocky start. For various reasons, extraction of reliably genetic samples from forams is a difficult process (for instance, their tendency to live in symbiotic associations makes contamination a continuing issue). However, studies have progressed to the point where a broad outline is beginning to emerge. One significant agreement between studies has been the monophyly of forams with a perforate calcareous test (Flakowski et al. 2005; Schweizer et al. 2008). The 'Globigerinida' and 'Buliminida' have both been shown to fall within this clade, and should probably not be distinguished from the Rotaliida. No representatives of the Lagenida or Robertinida appear to have been analysed molecularly; the lagenidans may be an independent lineage, while the robertinidans may be closely related to the Rotaliida (Sen Gupta 2002).

Suggested relationships of major foraminiferan groups from Sen Gupta (2002). This arrangement, which is somewhat concordant with available molecular data, proposes two separate lineages of multi-chambered forams, with calcareous members in each.

Within the Rotaliida, the most extensive molecular analysis has been that of Schweizer et al. (2008), whose results support a division between three main clades. Though reasonably well supported molecularly, these clades do not correspond to morphological divisions: the 'Buliminida', for instance, are divided between at least two clades. The planktonic forms may also be polyphyletic within the Rotaliida, though analyses have been inconsistent on their exact position in the clade (and Schweizer et al. do not include any globigerinidans in their analysis). Not all molecular results clash with the morphology, though: the Nummulitidae, a group of giant discus-shaped forams that get up to five centimetres in diameter, are one of a number of families that remain supported by either data source.

Internal chambers of Nummulites gizehensis, from the Natural History Museum. This species is most famous for being the major component of the limestone used in the construction of the pyramids of Giza.

REFERENCES

Flakowski, J., I. Bolivar, J. Fahrni & J. Pawlowski. 2005. Actin phylogeny of Foraminifera. Journal of Foraminiferal Research 35 (2): 93-102.

Haynes, J. R. 1990. The classification of the Foraminifera—a review of historical and philosophical perspectives. Palaeontology 33 (3): 503-528.

Loeblich, A. R., Jr & H. Tappan. 1964. Treatise on Invertebrate Paleontology pt C. Protista 2. Sarcodina, chiefly "thecamoebians" and Foraminiferida, 2 vols. The Geological Society of America and The University of Kansas Press.

Schweizer, M., J. Pawlowski, T. J. Kouwenhoven, J. Guiard & B. van der Zwaan. 2008. Molecular phylogeny of Rotaliida (Foraminifera) based on complete small subunit rDNA sequences. Marine Micropaleontology 66: 233-246.

Sen Gupta, B. K. 2002. Modern Foraminifera. Springer.

If a Komokiacean Turns Up in a Phylogeny, Will Anybody Notice?

It's possible that only one reader will care about this. But this is one minor detail that I came across while researching yesterday's post.

Komokiacea are large deep-sea branching protists that are expected, but not conclusively demonstrated, to belong or be related to Foraminifera. Attempts to extract molecular data for komokiaceans have, to date, failed miserably (Lecroq et al., 2009). Or have they?

In a paper written by Gooday et al. (1997), my attention was caught by the offhand comment: "We include Rhizammina algaeformis Brady 1879 [another deep-sea branching foram] within the Komokiacea on the basis of its 'softpart' organization". This relationship, it turns out, had originally been proposed by Cartwright et al. (1989). If this assignment is correct then komokiaceans have been appearing in molecular phylogenies for some years and nobody has been paying a blind bit of notice! Even more interestingly, Pawlowski et al. (2003) placed Rhizammina as sister to the xenophyophore Syringammina. Xenophyophores resemble komokiaceans both in being large branchers and in the sequestration of stercomata (faecal pellets) within their structure. A close relationship between the two groups would be quite credible. However, no other authors to date appear to have commented on Cartwright et al.'s reclassification of Rhizammina so I have no idea whether it's regarded as credible.

Discuss.

REFERENCES

Cartwright, N. G., A. J. Gooday & A. R. Jones. 1989. The morphology, internal organization, and taxonomic position of Rhizammina algaeformis Brady, a large, agglutinated, deep-sea foraminifer. Journal of Foraminiferal Research 19 (2): 115-125.

Gooday, A. J., R. Shires & A. R. Jones. 1997. Large, deep-sea agglutinated Foraminifera; two differing kinds of organization and their possible ecological significance. Journal of Foraminiferal Research 27 (4): 278-291.

Lecroq, B., A. J. Gooday, T. Cedhagen, A. Sabbatini & J. Pawlowski. 2009. Molecular analyses reveal high levels of eukaryotic richness associated with enigmatic deep-sea protists (Komokiacea). Marine Biodiversity 39: 45-55.

Pawlowski, J., M. Holzmann, J. Fahrni & S. L. Richardson. 2003. Small subunit ribosomal DNA suggests that the xenophyophorean Syringammina corbicula is a foraminiferan. Journal of Eukaryotic Microbiology 50: 483-487.

Three Random Foram Genera (Taxon of the Week: Pelosininae)

In an earlier post, I introduced you to the agglutinated forams of the family 'Saccamminidae'. As explained in that post, 'Saccamminidae' is undoubtedly a polyphyletic assemblage of forams of very simple morphology. In the influential, and outdated, classification of Cushman (1940), 'saccamminids' were divided between four subfamilies for which odds are that each of those subfamilies are as polyphyletic as the whole. Let's take a look at the members of one of those subfamilies and see where they are now.


Pelosina variabilis. Photo by Jan Pawlowski.

The subfamily Pelosininae, as recognised by Cushman (1940), included the genera Pelosina, Technitella and Pilulina. The distinguishing characteristics of this subfamily were that its members had free, unattached tests with a single chamber, at least one aperture and walls composed of fine particles. All three also live in the deep sea and include relatively large species for forams (up to 60 mm in height in Pelosina). In the classification of Kaminksi (2004), none of these genera were closely associated. In the case of Pelosina, Cushman was not even correct about the few defining features of the subfamily because this genus does live attached to the sediment by root-like structures (Rützler & Richardson 1996). Pelosina species are one of a number of tree-like forams that form a significant component of the deep-sea benthic community.


Technitella legumen. Image from here.

Technitella, in contrast, is an elongate, somewhat sausage-like form. The name of the genus ("little workman") refers to its elegantly constructed test, constructed from carefully selected materials. Heron-Allen & Earland (1909) described one species, T. thompsoni, which uses nothing but brittle star plates while T. legumen prefers sponge spicules, arranged in two layers with the spicules in each layer at right angles to each other to strengthen the test. Heron-Allen and Earland mused that "Probably we should be considered as imposing too weighty a postulate upon the members of the Club if we ventured to suggest that these rudimentary organisms were gifted with any aesthetic sense... it would appear that this "primordial, protoplasmic, atomic globule" is by no means so elementary an organism as naturalists are inclined to believe".


Lectotype and paralectotype of Pilulina jeffreysii. Photo by Andrew Henderson.

Finally, Pilulina constructs a globular test of felted sponge spicules with an elongate aperture like the mouth on a stick-figure's face. Of the three genera, only Pelosina and Pilulina have appeared in molecular phylogenetic analyses and the two do not appear to be associated, sitting instead in separate parts of the saccamminid cloud (e.g., Lecroq et al., 2009). Mikhalevich & Voronova (1999) argued that Pelosina is in fact a xenophyophore and placed it in the order Stannomida with the genera Stannoma and Stannophyllum. This was based on the supposed presence of linellae, a structure only otherwise found in stannomids. No molecular analysis has indicated an association between Pelosina and other xenophyophores. However, no other stannomid has appeared in these analyses, so just because Pelosina is not directly related to xenophyophores may not necessarily mean that it is not directly related to stannomids.

REFERENCES

Cushman, J. A. 1940. Foraminifera: their classification and economic use, 3rd ed. Harvard University Press: Cambridge (Massachusetts).

Heron-Allen, E., & A. Earland. 1909. On a new species of Technitella from the North Sea, with some observations upon selective power as exercised by certain species of arenaceous Foraminifera. Journal of the Quekett Microscopical Club, second series 10: 403-412.

Kaminski, M. A. 2004. The Year 2000 classification of the agglutinated Foraminifera. In: Bubík, M. & M. A. Kaminski (eds) Proceedings of the Sixth International Workshop on Agglutinated Foraminifera. Grzybowski Foundation Special Publication 8: 237-255.

Lecroq, B., A. J. Gooday, T. Cedhagen, A. Sabbatini & J. Pawlowski. 2009. Molecular analyses reveal high levels of eukaryotic richness associated with enigmatic deep-sea protists (Komokiacea). Marine Biodiversity 39: 45-55.

Mikhalevich, V. I., & M. N. Voronova. 1999. O sistematicheskom polozhenii roda Pelosina (Xenophyophoria, Protista, inc. sedis). Zoologicheskii Zhurnal 78 (2): 133-141.

Rützler, K., & S. Richardson. 1996. The Caribbean spicule tree: a sponge-imitating foraminifer (Astrorhizidae). Bulletin de l'Institut Royal des Sciences Naturelles de Belgique 66 (Suppl.): 143-151.

Floating Forams (Taxon of the Week: Globorotaliidae)

The planktic foraminiferan Globorotalia ungulata. Photo by Kenneth Finger.

Foraminifera have previously been covered at Catalogue of Organisms here and here. In those posts, the families covered were benthic forams while the family I'm covering today, Globorotaliidae, contains plaktonic forams.

The benthic vs planktonic division is generally treated as the basic starting point by foram workers. This is not because of any fundamental taxonomic distinction; benthic forams are considerably more diverse than planktonic species and, while past authors have treated planktonic forams as a single order Globigerinida, recent studies are often more consistent with a polyphyletic origin for planktonic lineages (Ujiié et al., 2008). It has even been shown that some individual foram species may alternative between benthic and planktonic stages (Darling et al., 2009). Planktonic forams also have much less history than benthic forams - while the earliest forams deep in the Palaeozoic were benthic, planktonic forms didn't appear until the Triassic (and didn't really become abundant until much later). However, the two groups do have very different ecologies and practical significance. While benthic species may be very localised, planktonic foram species are usually very widespread and abundant. About one-third of the world's ocean floor is covered with "Globigerina ooze", a thick deposit of the shells of dead planktonic forams. This great abundance and distribution, together with a high species turnover rate compared to benthic taxa, has made planktonic forams perhaps the most significant group of organisms of all for marine biostratigraphy.


Live specimen of Globorotalia menardii (Globorotaliidae; left) compared to Globigerinoides sacculifer (Globigerinidae; right). Photos by Colomban de Vargas.

The Globorotaliidae are a family of planktonic forams whose first definite appearance was in the Oligocene (de Vargas et al., 1997) assignations of earlier taxa to the globorotaliids are more contentious). Globorotaliids are distinguished from the other major family of planktonic forams, the Globigerinidae, by their different form (flattened rather than globular) and their smooth shell (globigerinids are spinose and honeycombed). While globigerinids feed on zooplankton as well as phytoplankton, globorotaliids are more specific feeders on phytoplankton. Ochrophyte endosymbionts have also been recorded in globorotaliids though the exact species involved does not appear to have been determined (Gastrich, 1988).

Blow (1979) recognised two subfamilies in the Globorotaliidae, the Globorotaliinae and Pulleniatininae; other authors may recognise them as separate families. In both subfamilies, the initial growth form is trochospiral (chambers arranged like the whorls of a top shell). In Globorotaliinae, it remains so throughout the life span; in Pulleniatininae, the earlier trochospiral stage is followed by a later streptospiral stage (each individual chamber occupies half a whorl and grows over the earlier chambers).


External and X-ray view of Pulleniatina obliquiloculata to show the change in spiral direction during growth. Photos from e-Foram Stock.

REFERENCES

Blow, W. H. 1979. The Cainozoic Globigerinida: A study of the morphology, taxonomy, evolutionary relationships and the stratigraphical distribution of some Globigerinida (mostly Globigerinacea). E. J. Brill: Leiden.

Darling, K. F., E. Thomas, S. A. Kasemann, H. A. Seears, C. W. Smart & C. M. Wade. 2009. Surviving mass extinction by bridging the benthic/planktic divide. Proceedings of the National Academy of Sciences of the USA 106 (31): 12629-12633.

Gastrich, M. D. 1988. Ultrastructure of a new intracellular symbiotic alga found within planktonic foraminifera. Journal of Phycology 23 (4): 623-632.

Ujiié, Y., K. Kimoto & J. Pawlowski. 2008. Molecular evidence for an independent origin of modern triserial planktonic foraminifera from benthic ancestors. Marine Micropaleontology 69 (3-4): 334-340.

Vargas, C. de, L. Zaninetti, H. Hilbrecht & J. Pawlowski. 1997. Phylogeny and rates of molecular evolution of planktonic foraminifera: SSU rDNA Sequences compared to the fossil record. Journal of Molecular Evolution 45 (3): 285-294.

Star Sands (Taxon of the Week: Calcarinidae)

Star-shaped forams, Calcarina sp., on an algal substrate. Photo from here.

About a month ago, I presented my first post on the marine shell-bearing protists known as foraminiferans. That post was on forams that constructed their shell by gluing together sand but I mentioned that there were other families that secreted their shells themselves. Some of these families can reach sizes large enough to be seen with the naked eye (over a millimetre and sometimes well over a centimetre in diameter); the Indo-Pacific calcareous Calcarinidae are one of these larger families. Such large forams live in association with endosymbiotic algae and have been given the evocative name of 'living sands' (Lee, 1995).

Among the living sands, the shape of Calcarinidae is distinctive. Their basic form is trochoid (i.e. shaped like a top shell, a Trochus) and similar to species of the related family Rotaliidae (Cushman, 1940) but extra shell material and chambers are laid down over and around the central trochoid structure. Large blunt external spines radiate from the sides of the foram, often giving the whole a star-like appearance when viewed from above. A system of canals runs between the chambers and along the spines allowing for the passage of cytoplasm between the chambers and the outside world. The chosen symbionts of calcarinids are diatoms which are held in special vacuoles inside the chambers. Symbiotic forams do still feed on other micro-organisms as well as deriving nutrients from their endosymbionts (Lee, 1995) but laboratory studies have shown that calcarinids are capable of living solely on nutrients derived from their diatoms in the absence of another food supply (Röttger & Krüger, 1990). If the algal symbionts are killed, the forams cannot live long without them though they may replace them if the opportunity arises in time (Lee, 1995).


Living specimen of Baculogypsina sphaerulata with cytoplasm emerging from the spines. Figure from Röttger & Krüger (1990); size is 2 mm across.

Calcarinids can make up a significant part of coastal calcareous deposits in the Indo-Pacific region; one of the most fun expressions of this abundance was made by Lee (1995) who commented that calcarinid deposits in one part of Japan were "so abundant that they can be scraped together by hand to build sand castles". Because of their dependence on their diatom symbionts, calcarinids are only found in shallow waters, mostly preferring high energy environments (Lobegeier, 2002). Many calcarinids live as epiphytes on macroalgae and seagrasses where they attach themselves to their substrate by means of cytoplasm extended through the spine canals (Röttger & Krüger, 1990); among filamentous algae the spines themselves may form a mechanical anchor among tangled filaments (Lobegeier, 2002).

REFERENCES

Cushman, J. A. 1940. Foraminifera: their classification and economic use, 3rd ed. Harvard University Press: Cambridge (Massachusetts).

Lee, J. T. 1995. Living sands. BioScience 45 (4): 252-261.

Lobegeier, M. K. 2002. Benthic foraminifera of the family Calcarinidae from Green Island Reef, Great Barrier Reef province. Journal of Foraminiferal Research 32 (3): 201-216.

Röttger, R., & R. Krüger. 1990. Observations on the biology of Calcarinidae (Foraminiferida). Marine Biology 106 (3): 419-425.

A Small Bag of Grains (Taxon of the Week: Saccamminidae)

Tests of the agglutinating foram Saccammina sphaerica. Scale bar = 500 μm. These are the lectotype and paralectotype of this species held by the British Natural History Museum.

Foraminifera are one of the best-known of protist groups and may make up more than half of the benthic biomass in some marine habitats, particularly in the deep sea (Gooday et al., 2001). Forams are amoeboids with filose pseudopodia that branch and rejoin each other to form a net for the collection of food particles. The great majority of forams are marine, and most (but not all) forams produce some sort of protective test or shell with the filopodia extending from openings or pores in the test. Because of this test, forams are one of the few protist groups with an extensive fossil record. Indeed, their use in biostratigraphic studies (and leading surveyors to small treats such as oil deposits) has lead to forams being better known from a palaeontological than a Recent perspective and the structure and morphology of the test has long been a major factor in distinguishing and classifying forams.

Forams may secrete their own tests (usually chitinous or calcareous) or they may construct a test from sand grains and/or other foreign particles (these are known as agglutinating forams). A distinction is also commonly made between monothalamous forms, in which the test is not divided into chambers (at least, not by complete septa), and polythalamous forms, in which the test is divided by septa into a number of chambers. However, molecular phylogenetic studies of recent forams have shown that monothalamous forams are paraphyletic while polythalamous forms are potentially polyphyletic (Flakowski et al., 2005). Also, while monothalamous taxa may produce chitinous or agglutinated tests, the type of test produced does not appear to correspond with phylogenetic position (Pawlowski et al., 2002).

Despite this, foram researchers continue to use the old test-based classification for the simple reason that no-one has yet come up with a better alternative (and doing so would not be easy). The Saccamminidae as generally recognised are a large family of agglutinating forams with generally a single chamber (or sometimes a bunch of similar chambers loosely attached to each other), usually with a single aperture. They may be globular or more elongate in shape. Some saccamminids are quite catholic in their choice of building materials but others may be more fussy. Perhaps the ultimate in fussiness is expressed by Technitella thompsoni which builds its test with nothing but the ambulacral plates of brittle stars (Cushman, 1940).


The 'silver saccamminid', an as-yet unidentified species that has appeared in a number of phylogenetic studies. Photo by Jan Pawlowski.

As with other monothalamous groups, molecular phylogenetic studies have indicated that "saccamminids" are polyphyletic with representative species scattered in various positions among the basal part of the foram tree (Cedhagen et al., 2009; Gooday & Pawlowski, 2004). Despite a fossil record extending back to the Cambrian (with putative 'saccamminids' at least as far back as the Silurian) and a significant abundance in the modern marine benthos, agglutinating forams are not as well-studied as calcareous taxa and monothalamous forms are particularly poorly so. For a start, they are often extremely small. Ecological studies have found the majority of 'saccamminid' specimens to be much less than 100 μm in diameter (Gooday et al., 2001) though Pilulina jeffreysii reaches more than 4 mm (Cedhagen et al., 2009). Also problematic, particularly for palaeontological studies, is that agglutinating foram tests are often difficult to distinguish from their surrounding environment because they are, after all, made from their surrounding environment. Perhaps the best demonstration of this issue is that the Stannomidae, despite being the largest of all forams and reaching over a foot in size, have no recognised fossil history at all.

REFERENCES

Cedhagen, T., A. J. Gooday & J. Pawlowski. 2009. A new genus and two new species of saccamminid foraminiferans (Protista, Rhizaria) from the deep Southern Ocean. Zootaxa 2096: 9-22.

Cushman, J. A. 1940. Foraminifera: their classification and economic use, 3rd ed. Harvard University Press: Cambridge (Massachusetts).

Flakowski, J., I. Bolivar, J. Fahrni & J. Pawlowski. 2005. Actin phylogeny of Foraminifera. Journal of Foraminiferal Research 35 (2): 93-102.

Gooday, A. J., H. Kitazato, S. Hori & T. Toyofuku. 2001. Monothalamous soft-shelled Foraminifera at an abyssal site in the North Pacific: a preliminary report. Journal of Oceanography 57: 377-384.

Gooday, A. J., & J. Pawlowski. 2004. Conqueria laevis gen. and sp. nov., a new soft-walled, monothalamous foraminiferan from the deep Weddell Sea. Journal of the Marine Biological Association of the UK 84 (5): 919-924.

Pawlowski, J., M. Holzmann, C. Berney, J. Fahrni, T. Cedhagen & S. S. Bowser. 2002. Phylogeny of allogromiid Foraminifera inferred from SSU rRNA gene sequences. Journal of Foraminiferal Research 32 (4): 334-343.

Living with Poo - A New Xenophyophore

Scattered individuals of the xenophyophore Reticulammina labyrinthica. Image from Ocean Planet.

And if you don't know what a xenophyophore is, then shame on you! Xenophyophores are sessile deep-sea protists that often reach comparatively gigantic sizes. One species, Stannophyllum venosum (which looks something like half a plate sitting on its edge), can be nearly a foot across (Tendal, 1972). Images from deep-sea submersibles have shown that xenos can be spectacularly abundant, carpeting the ocean floor in some places.

Xenophyophores are sometimes referred to as the largest unicellular organisms, but as I've mentioned before, that's arguably not entirely appropriate. Rather, xenophyophores have a coenocytic or hyphal organisation, with numerous nuclei scattered throughout long branching cytoplasmic tubes. The name "xenophyophore" means "bearer of foreign objects", and refers to the external test of the organism, which it constructs by cementing together objects it collects from the sediment around it - sand grains , for instance, or shells of other organisms - using a polysaccharide cement. The xenos also sequester their faecal pellets, which they may also integrate into their skeleton. Different species of xeno can be distinguished by the nature and arrangement of the foreign particles in the test (they are often quite picky about what they use), and the proportion of foreign particles to cement or faecal pellets. The species Cerelasma massa, for instance, differs from other xenos in using no foreign particles whatsoever, but only cement and its own faecal pellets - hence also being a contender for the title of most disgusting organism in existence. Species that use a high proportion of foreign particles in their construction are generally quite rigid, while those using more cement are softer.


The new xenophyophore species Shinkaiya lindsayi. In the long section, the central white strands are the xenophyophore's cytoplasm, while the black strands are strings of faecal pellets. Figure from Lecroq et al. (2009).

Yesterday saw the publication of a new xenophyophore species, Shinkaiya lindsayi (the genus is named, offhand, after the submersible that was used to collect the type specimen) by Lecroq et al. (2009). One of the most significant features of the new paper is that it includes a molecular phylogenetic analysis of the new species. Xenophyophores have been sequenced on one occasion before, by Pawlowski et al. (2003), who placed the species Syringammina corbicula among basal Foraminifera. It is good to see that Lecroq et al. place Shinkaiya as the sister to Syringammina, and the two together fit in the same position among forams originally found by Pawlowski et al.. The closest relative to xenophyophores identified is a foram called Rhizammina, which is also sessile, constructs a test of foreign matter, and even sequesters faecal pellets in a similar manner to xenophyophores.

This is a noteworthy achievement - these are not easy organisms to sequence. Not only is there a shortage of accessible material, but xenos and forams both tend to have large numbers of bacteria and other micro-organisms living around them, just aching to contaminate DNA samples (the very first molecular phylogenetic analysis of a foram, for instance, suggested a close relationship between forams and dinoflagelates, only to have it later shown that the sequence analysed belonged not to the foram but to parasitic micro-organisms living in the foram*). So the fact that Lecroq et al.'s results are not only well-supported, but make a lot of intuitive sense morphologically, makes this a very nice study indeed.

*Still, if the recently suggested SAR clade is correct, there is a certain irony to this - forams may be somewhat related to dinoflagellates after all.


Haeckel's (1889) illustrations of species of Stannophyllum, including the gigantic S. venosum at the bottom. Stannophyllum belongs to a family of xenophyophores called stannomids that differ from other xenos such as Shinkaiya (called psammetids) in having reinforcing threads (probably made of mucopolysaccharides) running through their tests. Stannomids are more plate-like, upright and flexible than the lumpy psammetids. Image via here (Haeckel referred to xenophyophores as "Deep-Sea Keratosa", as he was under the impression that they were sponges).

REFERENCES

Haeckel E. 1889. Report on the Deep-Sea Keratosa. Report on the Scientific Results of the Voyage of H. M. S. Challenger during the years 1873–76. Zoology 32 (part 82): 1–92.

Lecroq, B., A. J. Gooday, M. Tsuchiya & J. Pawlowski. 2009. A new genus of xenophyophores (Foraminifera) from Japan Trench: morphological description, molecular phylogeny and elemental analysis. Zoological Journal of the Linnean Society 156: 455-464.

Pawlowski, J., M. Holzmann, J. Fahrni & S. L. Richardson. 2003. Small subunit ribosomal DNA suggests that the xenophyophorean Syringammina corbicula is a foraminiferan. Journal of Eukaryotic Microbiology 50: 483-487.

Tendal, O. S. 1972. A monograph of the Xenophyophoria (Rhizopodea, Protozoa). Galathea Report 12: 7-99.