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A short history of freshwater foraminiferal research

Foraminifera are unicellular eukaryotes characterized by the presence of granuloreti-culopodia and the possession of a membranous, agglutinated, or calcareous test, which is either monothalamous (single-chambered) or polythalamous (multi-chambered) (Loeblich and Tappan 1987). Within monothalamids some species like Reticulomyxa filosa are amoeboid naked forms.

Gromia brunneri Blanc
Gromia brunneri Blanc

Until 1859, foraminifera were only known from marine habitats, but that year Claparède and Lachmann described a monothalamid foraminifer, Lieberkuehnia wageneri, sampled from an unknown water body in Berlin. It had a smooth flexible test with an entosolenian tube that separated the main cytoplasm mass from the pseudopodial peduncle. In 1886 Henri Blanc, a Swiss scientist, described another freshwater foraminifer, Gromia brunneri, which he had collected from the bottom of Lake Geneva. This single-chambered species had an agglutinated test, an organic layer covered and/or embedded with foreign, mainly non-organic, particles.

In subsequent years, Eugène Penard, another Swiss protozoologist, described four similar species Gromia gemma and G. squamosa (1899), G. linearis (1902) and G. saxicola (1905) from the same lake. He also described G. nigricans (1902), which he found not far from Lake Geneva in Mategnin and a marsh near Rouelbeau. Penard made permanent preparations of these foraminifera, which are still preserved and available in the Penard Collection of the Natural History Museum of Geneva (Switzerland).

In 1904, Ludwig Rhumbler erected the subfamily Allogromiinae for monothalamous foraminifera characterized by a more or less flexible organic test wall commonly with one or rarely two terminal apertures at either end of the test. He included all described freshwater species in this taxon. In a recent higher ranked classification of foraminifera based on molecular phylogenies (Pawlowski et al. 2013), monothalamous foraminifera were considered as a paraphyletic group that contains agglutinated and organic walled species as well as “naked” amoeboid species and environmental clades with unknown morphological affinities.

Gromia squamosa
Gromia squamosa

Traditionally the organic-walled foraminifera are called allogromiids. Most of them are distributed over a wide range of marine and brackish habitats (Gooday 2002). Freshwater allogromiids with an agglutinated test were originally placed in the genus Gromia by their discoverers, but as its type species G. oviformis is a filose marine species, Rhumbler (1904) transferred three species (G. squamosa, G. nigricans and G. linearis) to Rhynchogromia Rhumbler 1894. He further erected a new genus, Diplogromia, for the other two species having a double test wall: G. brunneri and G. gemma, although without designing a type species for the genus.

Eugene Penard
Eugene Penard

De Saedeleer (1934) revised Rhumbler’s classification leaving D. gemma in its genus and creating a new genus Allelogromia for the Rhynchogromia species with G. brunneri as type species. Deflandre (1953) erected the genus Penardogromia for G. linearis, with the argument that it had a homogenous agglutinated test with calcareous particles.

Loeblich and Tappan (1960) argued that the classification of De Saedeleer was un-acceptable, because G. brunneri had been fixed as the type of Diplogromia by subsequent designation of Cushman (1928). They created the genus Saedeleeria for G. gemma, transferring G. squamosa and G. nigricans also to Diplogromia, but without giving any supporting explanations. Another agglutinated allogromiid, Penardogromia palustris, was described by Thomas (1961) from a freshwater marsh near Bordeaux (France).

Beside these descriptions there have been some scattered records of agglutinated freshwater allogromiids over the years (Grospietsch 1958; Hoogenraad and De Groot, 1940; Siemensma 1982; Wailes 1915; Meisterfeld pers. comm.; Clauss, unpublished) and some photomicrographs available online (Revello 2015; Protist Information Server 2016).

Gromia terricola Leidy 1879
Gromia terricola

Joseph Leidy (1879) was the first who described an allogromiid foraminifer, Gromia terricola, from a terrestrial habit. He found this non-agglutinated species “among moist moss in the crevices of pavements, in shaded places, in the city of Philadelphia”. A similar terrestrial organic walled allogromiid Edaphoallogromia australica has been described by Meisterfeld et al. (2001).

Apart from all these agglutinated and organic-walled species, some naked amoeboid freshwater species belonging to the family Reticulomyxidae have been described. The best known of these species is Reticulomyxa filosa (Nauss 1949), long time considered as an amoebozoan, until its foraminiferal affinity was demonstrated by molecular study (Pawlowski et al. 1999). Since then two new species of Reticulomyxidae were described: Haplomyxa saranae (Dellinger et al. 2014) and Dracomyxa pallida (Wylezich et al. 2014). In an attempt to rediscover the allogromiids described by Penard and Blanc, Holzmann and Pawlowski (2002) examined samples from Lake Geneva. They did not succeed in finding any specimens by microscopic observations. However, several foraminiferal DNA sequences were obtained from the same sediment samples that built a monophyletic clade with the marine genera Ovammina and Cribrothalammina at its base. In a later report, numerous environmental rDNA sequences revealed the existence of a large number of freshwater monothalamids branching in several clades. However, none of these clades (except clade 2 that comprises the family Reticulomyxidae) could be linked to known freshwater allogromiids (Holzmann et al. 2003). Further studies based on environmental DNA surveys showed that foraminifera are also a ubiquitous component of soil samples (Geisen et al. 2015; Lejzerowicz et al. 2010).

In 2017, Siemensma et al. described two new agglutinated freshwater species (Lacogromia cassipara  and Limnogromia sinensis. They compared both new species with those described by Blanc, Penard and Thomas, with reference to the slides of the Penard Collection in Geneva and revised the taxonomy of agglutinated freshwater foraminifera.

Rhumbler
(1904)
DeSaedeleer
(1934)
Deflandre
(1953)
Loeblich and Tappan (1960) Siemensma et al. (2017)
Rhynchogromia Allelogromia Allelogromia Saedeleeria Lacogromia
– linearis – brunneri – brunneri – gemma – cassipara
– nigricans – nigricans – nigricans – brunneri
– squamosa – squamosa – squamosa – squamosa
– linearis – palustris
Diplogromia Diplogromia Diplogromia Diplogromia Limnogromia
– brunneri – gemma – gemma – squamosa – sinensis
– gemma – nigricans – nigricans
– linearis
Penardogromia Penardogromia – saxicola
– linearis – linearis
– palustris (1961)
G. saxicola1 G. saxicola1 G. saxicola1

1 Not mentioned by the author(s)

From Siemensma et al. 2017

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