Foraminifera

Astrammina rara, from micro*scope.

Belongs within: Sar.
Contains: Ammoscalariida, Hippocrepinida, Psammosphaerida, Parathuramminida, Allogromiidae, Globothalamea, Dendrophryida, Xenophyophorea, Nodosariana, Tubothalamea, Astrorhizoidea, Lagynidae.

The Foraminifera are a diverse group of aquatic, mostly marine, amoeboid organisms with granular cytoplasm forming slender anastomosing pseudopodia. Most Foraminifera construct some form of resistant test, and as a result they have an extensive fossil record. There are, however, some basal forms such as Reticulomyxa filosa that lack a test. If present, the test may be composed of foreign particles (such as sand grains) glued together with a cement, or it may be secreted directly by the foram itself. Classifications of forams have been heavily influenced by whether the test is agglutinated or secreted, and whether it is divided into multiple, discrete chambers, but it has become clear as our understanding of foram evolution has improved that both these features evolved on multiple occasions (Pawlowski et al. 2013). Multi-chambered tests are found within the Lagenida, Fusulinida, Tubothalamea and Globothalamea. Calcareous tests have also arisen independently within the Lagenida, Tubothalamea and Globothalamea.

Basal, unilocular forams may have a membranous or pseudochitinous test, or one composed of agglutinated sand grains and/or other foreign particles, and have been divided respectively between the Lagynacea and Ammodiscacea on the basis of this feature (Loeblich & Tappan 1964a). Once again, however, the different conditions are not phylogenetically distinct and the classification of many basal forams remains uncertain. Various basal forams may be free-living or attached to the substrate, and the test may be dominated by a single central chamber or elongate and/or branching.

Living with poo: a new xenophyophore
Published 8 July 2009
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 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).
Systematics of Foraminifera

Characters (from Loeblich & Tappan 1964a, as Foraminiferida + Granuloreticulosia): Cytoplasm minutely granular; pseudopodia delicate and reticulate. Protoplasmic body usually protected by test composed of one or more interconnected chambers; wall may be imperforate, finely or coarsely perforate, and may be chitinous, or composed of agglutinated particles or secreted material (rarely silica or aragonite, more commonly calcite), may have canal system of varying complexity; commonly with one or more large openings or apertures in addition to smaller wall perforations which may be present; pseudopodia protruding from apertures and perforations. Reproduction characterised by alternation of sexual and asexual generations, though one generation may be secondarily repressed; gametes commonly flagellate with two or three flagella, more rarely amoeboid.

<==Foraminifera (see below for synonymy)
    |--Astrammina Rhumbler in Wiesner 1931PH03, LT64a [incl. Armorella Heron-Allen & Earland 1932LT64a]
    |    |--*A. rara Rhumbler in Wiesner 1931LT64a
    |    |--A. limicolaG96
    |    |--A. sphaerica (Heron-Allen & Earland 1932) [=*Armorella sphaerica]LT64a
    |    `--A. triangularisPH03
    `--+--AllogromiidaM13
       |    |  i. s.: Niveus Altin et al. 2009M13
       |    |         Edaphoallogromia Pawlowski & Holzmann 2002M13
       |    |         Xiphophaga Goldstein et al. 2010M13
       |    |--AllogromiidaePHT13
       |    |--Argillotuba Avnimelech 1952LT64a [ArgillotubidaeM13, Argillotubinae]
       |    |    `--*A. vermiformis (Goës 1896) [=Astrorhiza vermiformis]LT64a
       |    |--Shepheardella Siddall 1880LT64a (see below for synonymy)
       |    |    |--*S. taeniformis Siddall 1880 [=*Arshepheardellum taeniforme]LT64a
       |    |    `--*Tinogullmia’ hyalina Nyholm 1954LT64a
       |    `--LabyrinthochitinidaeM13
       |         |--Labyrinthochitinia Bykova 1961LT64a
       |         |    `--*L. tastikoliensis Bykova 1961LT64a
       |         `--Chitinolagena Bykova 1961M13, LT64a
       |              `--*C. gutta Bykova 1961LT64a
       `--+--+--Cribrothalammina albaPHT13
          |  `--Reticulomyxa Nauss 1949PHT13, AS12 [Athalamea, Reticulomyxida]
          |       `--R. filosaPH03
          `--+--+--+--GlobothalameaPHT13
             |  |  `--+--DendrophryidaPHT13
             |  |     `--+--XenophyophoreaPHT13
             |  |        `--Shinkaiya lindsayiPHT13
             |  `--+--NodosarianaM13
             |     `--+--TubothalameaPHT13
             |        `--+--AstrorhizoideaPHT13
             |           `--Micrometula Nyholm 1952PHT13, LT64a
             |                `--*M. hyalostriata Nyholm 1952LT64a
             `--+--+--VellariaPHT13
                |  `--Psammophaga simploraPHT13, PH03
                `--LagynidaM13
                     |--LagynidaePHT13
                     |--BlysmasphaeridaeM13
                     `--Maylisoria Bykova 1961LT64a (see below for synonymy)
                          `--*M. pseudoscheda Bykova 1961LT64a
Foraminifera incertae sedis:
  Spheroidinellopsis seminulinaKS02
  Radicula Christiansen 1958LT64a
    `--*R. limosa Christiansen 1958LT64a
  Globospirillina Antonova 1964BL79
    `--G. claraBL79
  Mormosina kijastschensisBL79
  Ellesmerella Mamet & Roux in Mamet et al. 1987VH01
  Orobias Eichwald 1860 (n. d.)LT64b
    `--*O. aequalis Eichwald 1860LT64b
  Schizocladus [Schizocladea]C-S03
  PlanocassidulinaH03
    |--P. norcrossi (Cushman 1933) (see below for synonymy)H03
    |--P. sublimbata (Asano & Nakamura 1937) [=Cassidulina sublimbata]H03
    `--P. yabei (Asano & Nakamura 1937) [=Cassidulina yabei]H03
  Loxoendothyra parakosvensisE03
  Radiosphaera basilicaE03
  ‘Paralagena’ Sabirov 1986 non Dall 1904MSV00
  Septatounayella rauseraeZP86
  Eodiscus guangdongensisZP86
  Shouguania annectenaZP86
  Rosita fornicataG-B87
  Praeorbulina curvaH90
  Neolenticulina peregrinaJW99
  Rutherfordoides tenuisJW99
  ‘Nautilus’ umbilicatus Linnaeus 1758S64
  Cinibides thiaraB49
  DicarinellaM08
    |--D. asymmetrica [incl. Globotruncana ventricosa carinata, G. fundiconulosa, G. lobata]M08
    |--D. concavataM08
    `--D. primitivaM08
  Radotruncana calcarataM08
  Contusotruncana fornicataM08
  Spiroplectinella semicomplanataM08
  Marginula breoniF71
  Adherentina Spandel 1909 (n. d.)LT64b
    `--*A. rhenana Spandel 1909LT64b
  Aeolides de Montfort 1808 (n. d.)LT64b
    `--*A. squammatus de Montfort 1808LT64b
  Arthrocena Modeer 1791 (n. d.)LT64b
  Aspidodexia Ehrenberg 1872 (n. d.)LT64b
    `--*A. lineolata Ehrenberg 1872LT64b
  ‘Auriculina’ Costa 1856 nec Grateloup 1838 nec Gray 1847 (n. d.)LT64b
    `--*A. crenata Costa 1856LT64b
  ‘Buliminopsis’ Rzehak 1895 non Heude 1890 (n. d.)LT64b
    `--*B. conulus Rzehak 1895LT64b
  Calatharia Zalessky 1926LT64b
    `--*C. perforata Zalessky 1926LT64b
  Cameroconus Meunier 1888 (n. d.)LT64b
    `--*C. marmoris Meunier 1888LT64bCanopus’ de Montfort 1808 non Fabricius 1803 (n. d.)LT64b
    `--*C. fabeolatus de Montfort 1808LT64b
  ‘Cantharus’ de Montfort 1808 non Röding 1798 (n. d.)LT64b
    `--*C. calceolatus de Montfort 1808LT64b
  Canthropes de Montfort 1808 (n. d.) [=Cantharipes Agassiz 1846, Canthropus Pallas in Oken 1815]LT64b
    `--*C. galet de Montfort 1808LT64b
  Cepinula Schafhäutl 1851 (n. d.)LT64b
  Cerataria Zalessky 1926 (n. d.)LT64b
    `--*C. pulchella Zalessky 1926LT64b
  Chelibs de Montfort 1808 (n. d.) [=Celibs Sherborn 1893]LT64b
    `--*C. gradatus de Montfort 1808LT64b
  Cidarollus de Montfort 1808 (n. d.)LT64b
    `--*C. plicatus de Montfort 1808LT64b
  Cimelidium Ehrenberg 1858 (n. d.)LT64b
    `--*C. homeri (Ehrenberg 1858) [=Guttulina homeri]LT64b
  Clypeocyclina Silvestri 1908 (n. d.)LT64b
  Colpopleura Ehrenberg 1844 (n. d.)LT64b
    `--*C. ocellata (Ehrenberg 1838) [=Rotalia ocellata]LT64b
  Cortalus de Montfort 1808 (n. d.)LT64b
    `--*C. pagodus de Montfort 1808LT64b
  Craterularia Rhumbler 1911 (n. d.)LT64b
  Crustula Allix in Lecointre & Allix 1913 (n. d.)LT64b
    `--*C. complanata Allix in Lecointre & Allix 1913LT64b
  Cyclopavonina Silvestri 1937 (n. d.)LT64b
    `--*C. cyclica Silvestri 1937LT64b
  Cylindria de Gregorio 1930 (n. d.)LT64b
    `--*C. minuta de Gregorio 1930LT64b
  Dexiopora Ehrenberg 1861 (n. d.)LT64b
    `--*D. megapora Ehrenberg 1861LT64b
  Dorbignyaea Deshayes 1830 (n. d.)LT64b
  ‘Dujardinia’ Gray 1858 non Quatrefages 1844 (n. d.)LT64b
    `--*D. mediterranea Gray 1858LT64b
  Elliptina Harting 1852 (n. d.)LT64b
    |--E. inflataLT64b
    `--E. truncataLT64b
  Epistominites Zalessky 1926 (n. d.)LT64b
    `--*E. formosulus Zalessky 1926LT64b
  Glandiolus de Montfort 1808 (n. d.)LT64b
    `--*G. gradatus de Montfort 1808LT64b
  Hedbergina Brönnimann & brown 1956 (n. d.)LT64b
    `--*H. seminolensis (Harlton 1927) [=Globigerina seminolensis]LT64b
  Hemistegina Kaufmann 1867 (n. d.)LT64b
    `--*H. rotula Kaufmann 1867LT64b
  Hemisterea Ehrenberg 1872 (n. d.)LT64b
    `--*H. nautilus Ehrenberg 1872LT64b
  Hemisticta Ehrenberg 1872 (n. d.)LT64b
    `--*H. amplificata Ehrenberg 1872LT64b
  ‘Heterostomum’ Ehrenberg 1854 non Diesing 1850 (n. d.)LT64b
    `--*H. cyclostomum Ehrenberg 1854LT64b
  Lagenopsis de Gregorio 1930 (n. d.)LT64b
    `--*L. maliarda de Gregorio 1930LT64b
  Lekithiammina de Folin 1887 (n. d.)LT64b
    `--*L. aculeata de Folin 1887LT64b
  ‘Lepista’ Zalessky 1926 (n. d.) nec Wallengren 1863 nec (Fr.) Sm. 1870 (ICBN)LT64b
    `--*L. ornata Zalessky 1926LT64b
  ‘Lobularia’ Costa 1839 non Lamarck 1816 (n. d.)LT64b
    `--*L. vesiculosa Costa 1839LT64b
  Lyrina Zborzewski 1834LT64b
    `--*L. fischeri Zborzewski 1834LT64b
  ‘Mesopora’ Ehrenberg 1854 non Wesmael 1852LT64b
    `--*M. chloris Ehrenberg 1854LT64b
  Metarotaliella Grell 1962 (n. d.)LT64b
    `--*M. parva Grell 1962LT64b
  Mirfa de Gregorio 1890LT64b
    `--*M. subtetraedra de Gregorio 1890LT64b
  Mirga de Gregorio 1930 (n. d.)LT64b
    `--*M. permiana (de Gregorio 1930) [=Orbulina (*Mirga) permiana]LT64b
  Molnaria Zalessky 1926 (n. d.)LT64b
    `--*M. spinulata Zalessky 1926LT64b
  ‘Monocystis’ Ehrenberg 1854 non Stein 1848 (n. d.)LT64b
    `--*M. arcella (Ehrenberg 1854) [=Miliola (*Monocystis) arcella]LT64b
  Nummulitella Dorren 1948 (n. d.)LT64b
    `--*N. polystylata Dorren 1948LT64b
  Oncobotrys Ehrenberg 1856 (n. d.)LT64b
    `--*O. buccinum Ehrenberg 1856LT64b
  Ozawaina Lee 1927 (n. d.)LT64b
    `--*O. antiquior (Rouillier & Vosinsky 1849)LT64b (see below for synonymy)
  Orthocerina d’Orbigny in de la Sagra 1839 (n. d.)LT64b
    |--*O. quadrilatera (d’Orbigny in de la Sagra 1839) [=Nodosaria (*Orthocerina) quadrilatera]LT64b
    |--O. clavulus [=Nodosaria (Orthocerina) clavulus]LT64b
    `--O. murchisoniLT64b
  Otostomum Ehrenberg 1872 (n. d.)LT64b
    `--*O. strophoconus Ehrenberg 1872LT64b
  ‘Pectinaria’ Zalessky 1926 non Lamarck 1818 (n. d.)LT64b
    `--*P. costata Zalessky 1926LT64b
  Physomphalus Ehrenberg 1856 (n. d.)LT64b
    `--*P. porosus Ehrenberg 1856LT64b
  Pleurostomina Costa 1862 (n. d.)LT64b
    `--*P. bimucronata Costa 1862LT64b
  Pleurotrema Ehrenberg 1840 (n. d.)LT64b
    `--*P. calcarina Ehrenberg 1840LT64b
  Pseudastrorhizula Wetzel 1940 (n. d.)LT64b
    `--*P. eisenacki Wetzel 1940LT64b
  Pteroptyx Ehrenberg 1873 (n. d.)LT64b
    `--*P. vespertilio Ehrenberg 1873LT64b
  ‘Renulina’ Blake 1876 (n. d.) non Lamarck 1804LT64b
    `--*R. sorbyana Blake 1876LT64b
  Rhabdella d’Archiac & Haime 1853 (n. d.)LT64b
    `--*R. malcolmi d’Archiac & Haime 1853LT64b
  Rhynchoplecta Ehrenberg 1854 (n. d.)LT64b
    `--*R. punctata Ehrenberg 1854LT64b
  Rotalites Lamarck 1801 (n. d.)LT64b
    `--*R. tuberculosa Lamarck 1801LT64b
  Semseya Franzenau 1893 (n. d.)LT64b
    `--*S. lamellata Franzenau 1863LT64b
  Siderospira Ehrenberg 1845 (n. d.)LT64b
    `--*S. indica (Ehrenberg 1845) [=Siderolina indica]LT64b
  Spiroplectina Schubert 1902 (n. d.)LT64b
  Spiropleurites Ehrenberg 1854 (n. d.)LT64b
  Synspira Ehrenberg 1854 (n. d.)LT64b
    `--*S. triquetra Ehrenberg 1854LT64b
  Trioxeia de Folin 1888 (n. d.)LT64b
    `--*T. edwardsi de Folin 1888LT64b
  Upsonella Moore 1959 (n. d.)LT64b
    `--*U. typus Moore 1959LT64b
  Volutaria Zalessky 1926 (n. d.)LT64b
    `--*V. potoniei Zalessky 1926LT64b
  Volvotextularia Termier & Termier 1950 (n. d.)LT64b
    `--*V. polymorpha Termier & Termier 1950LT64b
  Parredicta poriferaLJ98
  AmmoscalariidaM13
  Cylindrogullmia albaPH03
  Toxisarcon synsuicidicaPH03
  GloiogullmiaPH03
  HippocrepinidaM13
  Neocatena Özdikmen 2009 [=Catena Schroder, Medioli & Scott 1989 non Richter 1975]M13
  PsammosphaeridaM13
  ParathuramminidaM13
  Jarvisella karamatensisB-F08
  Distichoplax Pia 1934B-F08, H75
    `--D. biserialisB-F08
  AcrulamminaJB12
  Pseudotaberina malabaricaM12
  Silicotuba Vyalov 1966 [Silicotubidae]HW93
  Planorbulinopsis parasita Banner 1971C94

Foraminifera [Allogromidiaceae, Allogromiidea, Allogromiidia, Allogromiina, Allogromioidea, Ammoasconidae, Ammodinetta, Ammodiscacea, Arastrorhiznia, Archimonothalamia, Arenacea, Arenacidae, Arforaminifera, Arreticularia, Arrhabdamidia, Arrhabdamnia, Ascoforaminifera, Asiphoidea, Astrorhizacea, Astrorhizata, Astrorhizicae, Astrorhizana, Astrorhizidaceae, Astrorhizidea, Astrorhizina, Astrorhizinae, Ataxophragmiacea, Ataxophragmioidea, Delosinacea, Earlandiacea, Foraminiferae, Foraminiferiae, Foraminiferida, Granuloreticulosea, Haplophragmiacea, Lagynacea, Lagynana, Lagynidea, Lituolacea, Lituolicae, Lituolidaceae, Lituolidea, Lituolina, Loftusiacea, Metammida, Monosomatia, Monostegua, Monothalamea, Monothalamia, Monothalamida, Nodosariata, Nodosinellacea, Perforata, Polysomatia, Polythalamea, Polythalamiis, Protammida, Psammatostichostegia, Reticulariida, Rhabdamminae, Rhabdamminina, Saccorhizidae, Serpuleidae, Siphonoforaminifera, Textulariacea, Textulariaceae, Textularida, Textularidae, Textularidea, Textularidia, Textulariidea, Textulariina, Thalamia, Thalamophora, Tubulata]

Maylisoria Bykova 1961LT64a [incl. Alexandrella Bykova 1958 (n. n.) nec Chevreux 1911 nec Tonnoir 1926 nec Schweyer 1939LT64a; MaylisoriidaeM13]

*Ozawaina antiquior (Rouillier & Vosinsky 1849)LT64b [=Nummulina antiquiorC40, Fusulinella (*Ozawaina) antiquiorLT64b, Orobias antiquiorC40]

Planocassidulina norcrossi (Cushman 1933) [=Cassidulina norcrossi; incl. C. kasiwazakiensis Husezima & Maruhasi 1944, C. nakamurai Uchio 1951]H03

Shepheardella Siddall 1880LT64a [=Arshepheardellum Rhumbler 1913LT64a, Shepheardia (l. c.)LT64a; incl. Tinogullmia Nyholm 1954LT64a; ShepheardellidaeM13]

*Type species of generic name indicated

References

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[B-F08] BouDagher-Fadel, M. K. 2008. The Cenozoic larger benthic foraminifera: the Palaeogene. Developments in Palaeontology and Stratigraphy 21: 297–418.

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