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.

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.