Foraminifera

Foraminifera (/fəˌræməˈnɪfərə/; Latin for "hole bearers"; informally called "forams") are members of a phylum or class of amoeboid protists characterized by streaming granular ectoplasm for catching food and other uses; and commonly an external shell (called a "test") of diverse forms and materials. Tests of chitin (found in some simple genera, and Textularia in particular) are believed to be the most primitive type. Most foraminifera are marine, the majority of which live on or within the seafloor sediment (i.e., are benthic), while a smaller variety float in the water column at various depths (i.e., are planktonic). Fewer are known from freshwater or brackish conditions, and some very few (nonaquatic) soil species have been identified through molecular analysis of small subunit ribosomal DNA.[2][3]

Foraminifera
Temporal range: 542–0 Ma[1]
Ediacaran–Recent
Live Ammonia tepida (Rotaliida)
Scientific classification
Domain:
Eukaryota
(unranked):
SAR
(unranked):
Rhizaria
Phylum:
Retaria
Subphylum:
Foraminifera

d'Orbigny, 1826
Orders

Allogromiida
Carterinida
Fusulinida — extinct
Globigerinida
Involutinida — extinct
Lagenida
Miliolida
Robertinida
Rotaliida
Silicoloculinida
Spirillinida
Textulariida
incertae sedis
   Xenophyophorea
   Reticulomyxa

Foraminifera typically produce a test, or shell, which can have either one or multiple chambers, some becoming quite elaborate in structure.[4] These shells are commonly made of calcium carbonate (CaCO
3) or agglutinated sediment particles. Over 50,000 species are recognized, both living (10,000)[5] and fossil (40,000).[6][7] They are usually less than 1 mm in size, but some are much larger, the largest species reaching up to 20 cm.[8]

In modern scientific English, the term foraminifera is both singular and plural (irrespective of the word's Latin derivation), and is used to describe one or more specimens or taxa: its usage as singular or plural must be determined from context. Foraminifera is frequently used informally to describe the group, and in these cases is generally lowercase.[9]

Taxonomy

Alcide d'Orbigny, in his 1826 work, considered them to be a group of minute cephalopods and noted their odd morphology, interpreting the pseudopodia as tentacles and noting the highly reduced (in actuality, absent) head. [10] He named the group foraminifères, or "hole-bearers", as members of the group had holes in the divisions between compartments in their shells, in contrast to nautili or ammonites. [9]

The taxonomic position of the Foraminifera has varied since their recognition as protozoa (protists) by Schultze in 1854,[11] there referred to as an order, Foraminiferida. Loeblich and Tappan (1992) reranked Foraminifera as a class[12] as it is now commonly regarded.

The Foraminifera have typically been included in the Protozoa,[13][14][15] or in the similar Protoctista or Protist kingdom.[16][17] Compelling evidence, based primarily on molecular phylogenetics, exists for their belonging to a major group within the Protozoa known as the Rhizaria.[13] Prior to the recognition of evolutionary relationships among the members of the Rhizaria, the Foraminifera were generally grouped with other amoeboids as phylum Rhizopodea (or Sarcodina) in the class Granuloreticulosa.

The Rhizaria are problematic, as they are often called a "supergroup", rather than using an established taxonomic rank such as phylum. Cavalier-Smith defines the Rhizaria as an infra-kingdom within the kingdom Protozoa.[13]

Some taxonomies put the Foraminifera in a phylum of their own, putting them on par with the amoeboid Sarcodina in which they had been placed.

Although as yet unsupported by morphological correlates, molecular data strongly suggest the Foraminifera are closely related to the Cercozoa and Radiolaria, both of which also include amoeboids with complex shells; these three groups make up the Rhizaria.[14] However, the exact relationships of the forams to the other groups and to one another are still not entirely clear. Foraminifera are closely related to testate amoebae.[18]

Living Foraminifera

Modern Foraminifera are primarily marine organisms, but living individuals have been found in brackish, freshwater [20] and even terrestrial habitats.[3] The majority of the species are benthic, and a further 40 morphospecies are planktonic.[21] This count may, however, represent only a fraction of actual diversity, since many genetically distinct species may be morphologically indistinguishable.[22]

A number of forams have unicellular algae as endosymbionts, from diverse lineages such as the green algae, red algae, golden algae, diatoms, and dinoflagellates.[21] These mixotrophic foraminifers are particularly common in nutrient-poor oceanic waters.[23] Some forams are kleptoplastic, retaining chloroplasts from ingested algae to conduct photosynthesis.[24]

Biology
Schematic diagram of a live multilocular foraminifera. 1 - endoplasm, 2-ectoplasm, 3-chamber, 4-pores, 5-foramen, 6-food vacuole, 7-nucleus, 8-mitochondria, 9-granureticulose pseudopodia, 10-granules, 11- primary aperture, 12-food particle, 13-Golgi apparatus, 14-ribosomes.

The foraminiferal cell is divided into granular endoplasm and transparent ectoplasm from which a pseudopodial net may emerge through a single opening or through many perforations in the test. Individual pseudopods characteristically have small granules streaming in both directions.[20] The pseudopods are used for locomotion, anchoring, excretion, test construction and in capturing food, which consists of small organisms such as diatoms or bacteria.[21][25] Certain foraminifera prey upon small animals such as copepods or cumaceans; some forams even predate upon other forams, drilling holes into the tests of their prey.[26]

The generalized foraminiferal life-cycle involves an alternation between haploid and diploid generations, although they are mostly similar in form.[11][27] The haploid or gamont initially has a single nucleus, and divides to produce numerous gametes, which typically have two flagella. The diploid or schizont is multinucleate, and after meiosis divides to produce new gamonts. Multiple rounds of asexual reproduction between sexual generations are not uncommon in benthic forms.[20]

Certain benthic foraminifera have been found to be capable of surviving anoxic conditions for over 24 hours, indicating that they are capable of selective anaerobic respiration. This is interpreted as an adaptation to survive changing oxygenic conditions near the sediment-water interface. [28]

Tests
Foraminiferan tests (ventral view)
A variety of calcareous foram test morphologies
The miliolid foraminiferan Quinqueloculina from the North Sea

The form and composition of their tests are the primary means by which forams are identified and classified. Most secrete calcareous tests, composed of calcium carbonate.[20] Calcareous tests may be composed of either aragonite or calcite depending on species; among those with calcite tests, the test may contain either a high or low fraction of magnesium substitution.[29] In other forams, the tests may be composed of organic material, made from small pieces of sediment cemented together (agglutinated) by either proteins or calcium carbonate, and in one genus, of silica. Some studies suggest a high amount of homoplasy in foraminifera, and that neither agglutinated nor calcareous foraminifera form monophyletic groupings.[30]

The test contains an organic matrix, which can sometimes be recovered from fossil samples.[29]

Openings in the test that allow the cytoplasm to extend outside are called apertures. [31] The primary aperture, leading to the exterior, take many different shapes in different species, including but not limited to rounded, crescent-shaped, slit-shaped, hooded, radiate (star-shaped), dendritic (branching). Some foraminifera have "toothed", flanged, or lipped primary apertures. There may be only one primary aperture or multiple; when multiple are present, they may be clustered or equatorial. In addition to the primary aperture, many foraminifera have supplemental apertures. These may form as relict apertures (past primary apertures from an earlier growth stage) or as unique structures.

Test shape is highly variable among different foraminifera; they may be single-chambered (unilocular) or multi-chambered (multilocular). In multilocular forms, new chambers are added as the organism grows. A wide variety of test morphologies is found in both unilocular and multilocular forms, including spiraled, serial, and milioline, among others. [25]

Unlike other shell-secreting organisms, such as molluscs or corals, the tests of foraminifera are located inside the cell membrane, within the protoplasm. The organelles of the cell are located within the compartment(s) of the test, and the hole(s) of the test allow the transfer of material from the pseudopodia to the internal cell and back. [25]

Tests as fossils are known from as far back as the Ediacaran period, [32]and many marine sediments are composed primarily of them. For instance, the limestone that makes up the pyramids of Egypt is composed almost entirely of nummulitic benthic Foraminifera.[33] It is estimated that reef Foraminifera generate about 43 million tons of calcium carbonate per year.[34]

Thin section of a peneroplid foraminiferan from Holocene lagoonal sediment in Rice Bay, San Salvador Island, Bahamas. Scale bar 100 micrometres

Genetic studies have identified the naked amoeba Reticulomyxa and the peculiar xenophyophores as foraminiferans without tests. A few other amoeboids produce reticulose pseudopods, and were formerly classified with the forams as the Granuloreticulosa, but this is no longer considered a natural group, and most are now placed among the Cercozoa.[35]

Deep-sea species

Foraminifera are found in the deepest parts of the ocean such as the Mariana Trench, including the Challenger Deep, the deepest part known. At these depths, below the carbonate compensation depth, the calcium carbonate of the tests is soluble in water due to the extreme pressure. The Foraminifera found in the Challenger Deep thus have no carbonate test, but instead have one of organic material.[36]

Four species found in the Challenger Deep are unknown from any other place in the oceans, one of which is representative of an endemic genus unique to the region. They are Resigella laevis and R. bilocularis, Nodellum aculeata, and Conicotheca nigrans (the unique genus). All have tests that are mainly of transparent organic material which have small (about 100 nm) plates that appear to be clay.[36]

Evolutionary significance
Fossil nummulitid foraminiferans showing microspheric and megalospheric individuals; Eocene of the United Arab Emirates; scale in mm

Dying planktonic Foraminifera continuously rain down on the sea floor in vast numbers, their mineralized tests preserved as fossils in the accumulating sediment. Beginning in the 1960s, and largely under the auspices of the Deep Sea Drilling, Ocean Drilling, and International Ocean Drilling Programmes, as well as for the purposes of oil exploration, advanced deep-sea drilling techniques have been bringing up sediment cores bearing Foraminifera fossils.[37] The effectively unlimited supply of these fossil tests and the relatively high-precision age-control models available for cores has produced an exceptionally high-quality planktonic Foraminifera fossil record dating back to the mid-Jurassic, and presents an unparalleled record for scientists testing and documenting the evolutionary process.[37] The exceptional quality of the fossil record has allowed an impressively detailed picture of species inter-relationships to be developed on the basis of fossils, in many cases subsequently validated independently through molecular genetic studies on extant specimens[38] Larger benthic Foraminifera with complex shell structure react in a highly specific manner to the different benthic environments and, therefore, the composition of the assemblages and the distribution patterns of particular species reflect simultaneously bottom types and the light gradient. In the course of Earth history, larger Foraminifera are replaced frequently. In particular, associations of Foraminifera characterizing particular shallow water facies types are dying out and are replaced after a certain time interval by new associations with the same structure of shell morphology, emerging from a new evolutionary process of adaptation.[39] These evolutionary processes make the larger Foraminifera useful as index fossils for the Permian, Jurassic, Cretaceous and Cenozoic.

The earliest known definite foraminifera appear in the fossil record towards the very end of the Ediacaran; these forms all have agglutinated tests and are unilocular. These include forms like Platysolenites and Spirosolenites. [40][32] Molecular clocks indicate that the crown-group of foraminifera likely evolved during the Neoproterozoic or latest Mesoproterozoic; this timing is consistent with Neoproterozoic fossils of the closely-related filose amoebae. As fossils of foraminifera have not been found prior to the end of the Ediacaran, it is likely that most of these Proterozoic forms did not have hard-shelled tests.[41]

Uses

Because of their diversity, abundance, and complex morphology, fossil foraminiferal assemblages are useful for biostratigraphy, and can accurately give relative dates to sedimentary rocks, as was discovered by Alva C. Ellisor in 1920.[42] The oil industry relies heavily on microfossils such as forams to find potential hydrocarbon deposits.[43]

Ammonia beccarii, a benthic foram from the North Sea.

Calcareous fossil Foraminifera are formed from elements found in the ancient seas where they lived. Thus, they are very useful in paleoclimatology and paleoceanography. They can be used, as a climate proxy, to reconstruct past climate by examining the stable isotope ratios and trace element content of the shells (tests). Global temperature and ice volume can be revealed by the isotopes of oxygen, and the history of the carbon cycle and oceanic productivity by examining the stable isotope ratios of carbon;[44] see δ18O and δ13C. The concentration of trace elements, like magnesium (Mg),[45] lithium (Li)[46] and boron (B),[47] also hold a wealth of information about global temperature cycles, continental weathering, and the role of the ocean in the global carbon cycle. Geographic patterns seen in the fossil records of planktonic forams are also used to reconstruct ancient ocean currents. Because certain types of Foraminifera are found only in certain environments, they can be used to figure out the kind of environment under which ancient marine sediments were deposited. For the same reasons they make useful biostratigraphic markers, living foraminiferal assemblages have been used as bioindicators in coastal environments, including indicators of coral reef health. Because calcium carbonate is susceptible to dissolution in acidic conditions, Foraminifera may be particularly affected by changing climate and ocean acidification.

Foraminifera Baculogypsina sphaerulata of Hatoma Island, Japan. Field width 5.22 mm

Foraminifera have many uses in petroleum exploration and are used routinely to interpret the ages and paleoenvironments of sedimentary strata in oil wells.[48] Agglutinated fossil Foraminifera buried deeply in sedimentary basins can be used to estimate thermal maturity, which is a key factor for petroleum generation. The Foraminiferal Colouration Index [49] (FCI) is used to quantify colour changes and estimate burial temperature. FCI data is particularly useful in the early stages of petroleum generation (about 100 °C).

Foraminifera can also be used in archaeology in the provenancing of some stone raw material types. Some stone types, such as limestone, are commonly found to contain fossilised Foraminifera. The types and concentrations of these fossils within a sample of stone can be used to match that sample to a source known to contain the same "fossil signature".

  • Foraminifera of Pag Island, Adriatic Sea -60 m, field width 5.5 mm
  • Foraminifera of Pag Island, Adriatic Sea -60 m, field width 5.5 mm
  • Foraminifera of Pag Island, Adriatic Sea -60 m, field width 5.5 mm
  • Foraminifera of Pag Island, Adriatic Sea -60 m, field width 5.5 mm
  • Foraminifera of Indian Ocean, south-eastern coast of Bali, field width 5.5 mm
  • Foraminifera of Indian Ocean, south-eastern coast of Bali, field width 5.5 mm
  • Foraminifera of Indian Ocean, south-eastern coast of Bali, field width 5.5 mm
  • Foraminifera in Ngapali, Myanmar, field width 5.22 mm
  • Foraminifera Heterostegina depressa, field width 4.4 mm

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