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Phylogeny and Ultrastructure of Miliammina fusca: Evidence for Secondary Loss of Calcification in a Miliolid Foraminifer
Abstract and Figures
The classification of the Foraminifera, a widely distributed group of largely marine protists, has traditionally been based on morphological characters. The most important of these are the composition and structure of the shell or "test." Here, we use both phylogenetic analysis of the genes for small subunit rRNA and beta-tubulin and ultrastructural analysis to document a reversion in wall type from more derived calcareous tests to an agglutinated test. These data indicate that the genus Miliammina, and possibly other members of the Rzehakinidae, should be placed in the Order Miliolida as opposed to their current assignment in Order Textulariida. We also address the effects this reversion may have had on the ability of rzehakinacids to effectively colonize marginal marine environments. Finally, the hypothesis that some multilocular agglutinated foraminiferans descended from calcareous lineages has implications for interpretation of the foraminiferal fossil record.
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Supplementary resource (1)
Nucleotide Sequence
November 2005
... It is also in accordance with macroscopic sediment observations in shallow cove sediment samples. This interpretation is consistent with the occurrence of other representatives of Miliammina in dysoxic settings (Hayward and Hollis, 1994;Tyszka, 1997;Habura et al., 2006). ...
... Adaptability to different habitats seems to be a characteristic of the Miliammina species more generally. Together with other members of the Rzehakinidae, they inhabit a wide spectrum of both open-and marginal-marine environments (Habura et al., 2006). They are common in salt marshes, mangrove swamps, and oligohaline estuaries (Sen Gupta, 1999), persist longer than other foraminifera in marine basins isolated from the sea (Lloyd and Evans, 2002), and dominate in a volcanic caldera less than a decade after significant eruptions (Finger and Lipps, 1981). ...
... They are common in salt marshes, mangrove swamps, and oligohaline estuaries (Sen Gupta, 1999), persist longer than other foraminifera in marine basins isolated from the sea (Lloyd and Evans, 2002), and dominate in a volcanic caldera less than a decade after significant eruptions (Finger and Lipps, 1981). Miliammina species have been also reported from mesohaline habitats (Hayward and Hollis, 1994;Lloyd and Evans, 2002;Habura et al., 2006). In Antarctic waters, M. arenacea is associated with corrosive high-salinity shelf water (Kennett, 1968;Milam and Anderson, 1981;Ishman and Sperling, 2002) and thrives in areas affected by Antarctic polynya (Capotondi et al., 2018). ...
Sub-Antarctic fjords are among the environments most affected by the recent climate change. In our dynamically changing world, it is essential to monitor changes in these vulnerable settings. Here, we present a baseline study of "living" (rose-bengal-stained) benthic foraminifera from fjords of South Georgia, including fjords with and without tidewater glaciers. Their distribution is analyzed in the light of new fjord water and sediment property data, including grain size and sorting, total organic carbon, total sulfur, and δ 13 C of bulk organic matter. Four well-defined foraminiferal assemblages are recognized. Miliammina earlandi dominates in the most restricted, near-shore and glacier-proximal habitats, Cassidulinoides aff. parkerianus in mid-fjord areas, and Globocassidulina aff. rossensis and an assemblage dominated by Ammobaculites rostratus, Reophax subfusiformis, and Astrononion echolsi are in the outer parts of the fjords. Miliammina earlandi can tolerate strong glacial influence, including high sedimentation rates in fjord heads and sediment anoxia, as inferred from sediment color and total organic carbon / sulfur ratios. This versatile species thrives both in the food-poor inner reaches of fjords that receive mainly refractory petrogenic organic matter from glacial meltwater and in shallow-water coves, where it benefits from an abundant supply of fresh, terrestrial, and marine organic matter. A smooth-walled variant of C. aff. parkerianus, apparently endemic to South Georgia, is the calcareous rotaliid best adapted to inner-fjord conditions characterized by moderate glacial influence and sedimentation rates and showing no preference for particular sedimentary redox conditions. The outer parts of fjords with clear, well-oxygenated bottom water are inhabited by G. aff. rossensis. Ammobaculites rostratus, R. subfusiformis, and A. echolsi dominate in the deepest-water settings, with water salinities ≥ 33.9 PSU and temperatures 0.2-1.4 • C, characteristic of winter water and Upper Circumpolar Deep Water. The inner-and mid-fjord foraminiferal assemblages seem specific to South Georgia, although with continued warming and deglaciation, they may become more widespread in the Southern Ocean.
... It is also in accordance with macroscopic sediment observations in shallow coves sediment samples. This interpretation is consistent with the occurrence of other representatives of Miliammina in dysoxic settings (Hayward and Hollis, 1994;Tyszka, 1997;Habura et al., 2006). ...
... Adaptability to different habitats seems to be a characteristic of Miliammina species more generally. Together with other members of the Rzehakinidae, they inhabit a wide spectrum of both open-and marginal-marine environments (Habura et al., 2006). They are common in salt marshes, mangrove swamps, oligohaline estuaries (Sen Gupta, 1999), persist longer than 455 other foraminifera in marine basins isolated from the sea (Lloyd and Evans, 2002), and dominated in a volcanic caldera less than a decade after significant eruptions (Finger and Lipps, 1981). ...
... They are common in salt marshes, mangrove swamps, oligohaline estuaries (Sen Gupta, 1999), persist longer than 455 other foraminifera in marine basins isolated from the sea (Lloyd and Evans, 2002), and dominated in a volcanic caldera less than a decade after significant eruptions (Finger and Lipps, 1981). Miliammina species have been also reported from mesohaline habitats (Hayward and Hollis, 1994;Lloyd and Evans, 2002;Habura et al., 2006). In Antarctic waters, M. arenacea is associated with corrosive High Salinity Shelf Water (Kennett, 1968;Milam and Anderson, 1981;Ishman and Sperling, 2002) and thrives in areas affected by Antarctic polynya (Capotondi et al., 2018). ...
Sub-Antarctic fjords are among the environments most affected by the recent climate change. In our dynamically changing world, it is essential to monitor changes in these vulnerable settings. Here, we present a baseline study of “living” (rose Bengal stained) benthic foraminifera from fjords of South Georgia, including fjords with and without tidewater glaciers. Their distribution is analyzed in the light of new fjord water and sediment property data, including grain size and sorting, total organic carbon, total sulfur, and δ13C of bulk organic matter. Four well-defined foraminiferal assemblages are recognized. Miliammina earlandi dominates in the most restricted, near-shore and glacier-proximal habitats, Cassidulinoides aff. parkerianus in mid-fjord areas, and Globocassidulina aff. rossensis and Reophax subfusiformis in the outer parts of fjords. Miliammina earlandi can tolerate strong glacial influence, including high sedimentation rates in fjord heads and sediment anoxia, as inferred from sediment color and total organic carbon/sulfur ratios. This versatile species thrives both in the food-poor inner reaches of fjords that receive mainly refractory petrogenic organic matter from glacial meltwater, and in shallow-water coves where it benefits from an abundant supply of fresh, terrestrial and marine organic matter. A smooth-walled variant of C. aff. parkerianus, apparently endemic to South Georgia, is the calcareous rotaliid best adapted to inner fjord conditions characterized by moderate glacial influence and sedimentation rates and showing no preference for particular sedimentary redox conditions. The outer parts of fjords with clear, slightly warmer bottom water, are inhabited by G. aff. rossensis. Reophax subfusiformis dominates in the deepest-water settings with water salinities ≥ 33.9 PSU and temperatures 0.2–1.4 °C, characteristic for Winter Water and Upper Circumpolar Deep Water. The inner- and mid-fjord foraminiferal assemblages seem specific to South Georgia, although with continued warming and deglaciation they may become more widespread in the Southern Ocean.
... However, the commonly accepted traditional wall structure characteristics of specific foraminiferal groups were largely defined based on low-resolution microscopy and/or on recrystallized fossil specimens with obscured test composition, which precluded any record of the original biocrystals (see discussion in Mikhalevich 2009;Dubicka and Gorzelak 2017). Moreover, more recent molecular studies of Foraminifera (Darling et al. 1997(Darling et al. , 2009Pawlowski 2000;Habura et al. 2006;Schweizer et al. 2008;Ujiié et al. 2008;Pawlowski et al. 2013;Holzmann and Pawlowski 2017) have revealed that the classical test structure-based higher-level classification of Foraminifera is rather speculative and, in several points, invalid. In a seminal work on Foraminifera classification based on molecular data, Pawlowski et al. (2013) established a higher-level (supraordinary) taxonomic system in which multi-chambered foraminifers (polythalamous) were grouped into two classes, Tubothalamea and Globothalamea, and mentioned that Lagenida probably constitutes a distinct class as well. ...
... Q. agglutinas, Rudoloculina hooperi) already published (Mikhalevich et al. 1986;Hottinger et al. 1993;Guilbault and Patterson 1998;Parker 2017;Dubicka et al. 2018), as well as that studied in this paper (Quinqueloculina arenata), has turned out to be composed of the same type of needle-shaped crystallites ( Fig. 7C 1 , C 2 ) as those found in entirely calcareous foraminiferal porcelain. Data from this test structure are consistent with the molecular studies of Fahrni et al. (1997) and Habura et al. (2006), which clearly show that agglutinated-porcelanous miliolid coiling taxa such as Miliammina, and possibly other members of Rzehakinidae, belong to the order Miliolida, as opposed to their former assignment in the order Lituolida ; for Lituolida definition see e.g., Loeblich and Tappan 1987;Sen Gupta 2003). The second order Spirillinida of the class Tubothalamea forms a sister clade to Miliolida according to molecular studies (Pawlowski et al. 2013). ...
Foraminiferal wall micro/ultra-structures of Recent and well-preserved Jurassic (Bathonian) foraminifers of distinct foraminiferal high-rank taxonomic groups, Globothalamea (Rotaliida, Robertinida, and Textulariida), Miliolida, Spirillinata and Lagenata, are presented. Both calcite-cemented agglutinated and entirely calcareous foraminiferal walls have been investigated. Original test ultra-structures of Jurassic foraminifers are given for the first time. “Monocrystalline” wall-type which characterizes the class Spirillinata is documented in high resolution imaging. Globothalamea, Lagenata, porcelaneous representatives of Tubothalamea and Spirillinata display four different major types of wall-structure which may be related to distinct calcification processes. It confirms that these distinct molecular groups evolved separately, probably from single-chambered monothalamids, and independently developed unique wall types. Studied Jurassic simple bilocular taxa, characterized by undivided spiralling or irregular tubes, are composed of miliolid-type needle-shaped crystallites. In turn, spirillinid “monocrystalline” test structure has only been recorded within more complex, multilocular taxa possessing secondary subdivided chambers: Jurassic Paalzowella and Recent Patellina. More integrated molecular and structural studies are needed in order to better understand taxonomic position and phylogeny of tubular taxa. Unilocular and multichambered Lagenata (Lagenidae and Nodosariidae, respectively) show identical test micro and ultra-structure which suggests their close phylogenetic relationship and questions most recent theories of their separate evolutionary history and origins. A comparison of Recent, Cretaceous, and Jurassic foraminiferal test structure indicates that test characteristics at particular higher-rank taxonomic levels change very little over time and thus can serve as good proxies for the taxonomic designations of fossil taxa, when their state of preservation is appropriate for microstructural observations.
... For the three orders with the highest diversity (i.e. Miliolida, Nodosariida and Rotaliida), evolution of families is indicated (based on Holzmann and Pawlowski, 2017;Habura et al., 2006;Hayward et al., 2022). For the other three orders, no attempt is made to indicate the diversity on family-level due to an absence of phylogenetic data and/or a detailed fossil record. ...
... For the three orders with the highest diversity (i.e. Miliolida, Nodosariida and Rotaliida), evolution of families is indicated (based on Holzmann and Pawlowski, 2017;Habura et al., 2006;Hayward et al., 2022). For the other three orders, no attempt is made to indicate the diversity on family-level due to an absence of phylogenetic data and/or a detailed fossil record. ...
Ongoing ocean acidification affects marine calcification, although the scope and magnitude of this impact is essentially unknown. Here, we investigate the evolutionary origin of shell building in foraminifera to understand the long-term interplay between ocean carbon chemistry and calcification. Our analysis of shell chemical composition reveals multiple, independent origins for foraminiferal calcification throughout the Phanerozoic. Differences between orders reflect the different physiological controls employed by foraminifera to take up Ca2+ and inorganic carbon from seawater for CaCO3 precipitation. With the long timespan involved, variability in seawater chemistry provided contrasting environments for calcification to arise, resulting in the diverse calcification strategies that exist today. This, in turn, explains the opposite responses of shell building to carbon perturbations. Our results call for adopting an evolutionary perspective when predicting the impact of perturbations on marine calcification and thereby, on the global carbon cycle.
... Traditionally, M. fusca is placed in the order Textulariida on the basis of the wall composition, which is agglutinated (Loeblich and Tappan, 1987). However, DNA analyses clearly show that this species groups with porcelaneous foraminifera and therefore belongs to the order Miliolida (Fahrni et al., 1997;Habura et al., 2006). ...
... Typical end-members along decreasing salinity gradients are a few agglutinated foraminifera, including Jadammina, Miliammina, Ammotium). Habura et al. [37] argue that the combination of reduced salinity and low pH conditions disfavor calcification in foraminiferans, as they are dependent on the local carbonate concentration [38], which generally decreases in low salinity environments (see also [39]). ...
Lagos Lagoon is among Africa’s largest estuarine ecosystems, bordered by one of the fastest growing megacities in the world and the ultimate repository of contaminants carried in industrial, municipal and agricultural wastes. The high levels of pollutants have progressively deteriorated the water quality, adversely affected lagoon ecosystems, impacted the livelihood of the coastal population and pose serious risks to human health. Benthic foraminifera are excellent proxies and sensitive bioindicators of environmental disturbances but comprehensive studies on the structure, distribution, diversity and impact of pollution upon foraminiferal communities have not yet been conducted in the Lagos Lagoon. To demonstrate the potential of foraminifera as proxies of environmental perturbations, benthic foraminifera were investigated on a lagoon-wide basis. Lagos Lagoon comprises areas that range from low levels of direct impact to those of severely affected by various forms of anthropogenic disturbance. The goals of this study are to analyze patterns of distribution and species richness, to document foraminiferal community structures, and to identify taxa that track documented records of pollution in Lagos Lagoon sediments. Heat maps were generated from abundance records for selected species to illustrate environmental preferences and relative resistance levels to individual forms of anthropogenic disturbance. Sediments were analyzed for a range of physicochemical properties, via a multi-parameter sensor probe-device, including temperature, pH, depth and total dissolved solids (TDS). Quantitative analysis of 24 sediment samples yielded a total 3872 individuals of benthic foraminifera that belong to 42 species and 25 genera. They comprise 10 porcellaneous, 22 hyaline perforate and 10 agglutinated species. Ammobaculites exiguus , Ammotium salsum , Ammonia aoteana , Ammonia convexa and Trochammina sp. 1 have been found to be the most abundant species. For the first time, the complete present-day foraminifera fauna is illustrated here via scanning electron microscopy. The features recorded allow to assess the spatial effects of pollution upon foraminiferal assemblages on a lagoon-wide basis. The data generated may ultimately form the basis to assess the progressive deterioration of Lagos Lagoon ecosystems from cores by using benthic foraminifera as bioindicators of environmental perturbation.
... The ITS region was used by de Vargas et al. (2001) for the first time, and later Tsuchiya et al. (2003) performed phylogenetic analysis of ITS rDNA. Protein-coding genes also have been used to identify foraminifers, namely actin (Keeling, 2001;Flakowski et al., 2005), RPB1 (Longet et al., 2003(Longet et al., , 2004Longet & Pawlowski, 2007), and αand β-tubulin (Habura et al., , 2006Takishita et al., 2005;Hou et al., 2013;Apotheloz-Perret-Gentil & Pawlowski, 2014). Secondary structure of the conserved regions of SSU RNA was also used for foraminiferal identification by Ertan et al. (2004) and Habura et al. (2004b). ...
Applications of molecular techniques have become integral to most fields of biological research, including evolutionary biology. Over the past two decades, studies of molecular genetics of foraminifers have emerged to enhance taxonomic identification with broad applications, including biodiversity, environmental assessments, and paleoceanographic studies. However, the results are widely scattered across the literature, thereby inhibiting advances in such research on foraminifers, especially regionally. In this review, we discuss the developments and contributions in the field of molecular genetics as applied to foraminifers, offering a guide to beginners in this area of research. Furthermore, this review highlights new opportunities for foraminiferal research that will pave the way for future studies in this field.
... These species included three agglutinated species (Miliammina fusca, Entzia macrescens, and Trochammina inflata) and two calcareous species (Helenina anderseni and Elphidium williamsoni; Fig. 1). We note that M. fusca is probably derived from calcareous ancestors (Habura et al., 2006). Most of our experiments used T. inflata because of the particular need for data on agglutinated species and because of its relatively large size and conspicuous motility. ...
Agglutinated foraminifera dominate in temperate salt marsh sediment, making them key indicators for monitoring sea level and environmental changes. Little is known about the biology of these benthic foraminifera because of difficulties in distinguishing live from dead specimens in laboratory cultures. We present data from 10 years of laboratory experiments using comparisons of the agglutinant trochamminids Trochammina inflata and Entzia macrescens and the miliolid Miliammina fusca with the calcareous rotalids Helenina anderseni and Elphidium williamsoni. Specimens were taken from a laboratory mesocosm representing Chezzetcook Inlet, a cool-temperate salt marsh in eastern Canada. We determined culture requirements for the agglutinated foraminifera in Petri dishes over 10–12 week periods. Five inexpensive, non-terminal ways of identifying live organisms were developed: spatial movement, detritus-gathering, attachment, clustering, and test opacity. Comparison with rose Bengal staining showed <10% diversion for calcareous species and T. inflata but M. fusca was over-counted by >30%. Terminal chambers of Trochammina inflata were examined by transmission electron microscopy to visualise food consumption and identify food in digestive vacuoles, both in specimens from mesocosm and in culture. Bacteria and unidentified detritus in the vacuoles establish that this agglutinated species is a saprophagous and bacterivorous detritivore. The adhesive secretions by these species apparently help them gather and possibly farm food while being relatively immobile in the sediments. Our observations of movement and feeding orientation in the agglutinants suggest links between form and function that underscore their value as ultra high resolution sea-level proxies. Mesocosm biomass and abundance counts show that foraminifera represent >50% of the meiofaunal biomass, emphasising their importance in the food web and energy-flow dynamics of temperate salt marsh systems.
Rudoloculina hooperi, a new miliolid from Holocene and modern shelf sediments of the northeastern Pacific Ocean, is characterized by chambers that are quadrate in cross-section and by a test wall with embedded agglutinated grains, some of which consist of miliolid-type shell material (subparallel calcite laths). The agglutinated grains are either calcareous and low in magnesium (Mg/Ca ≤ 0.01) or silicic. Rudoloculina hooperi has previously been mistakenly reported from the same region as Quinqueloculina agglutinata Cushman. The morphologically similar genus Cycloforina has been reported mostly from warmer waters, suggesting that R. hooperi is near the northern limit of its range in the Gulf of Alaska.
Late Osagean to Meramecian Platycrinites and Eucladocrinus from Illinois, Iowa, and Missouri are redescribed and redefined from study of type material. Three of the oldest species were incorrectly synonymized with P. sarae , and this correction leads to a realignment of species systematics within Platycrinites. Accordingly, six species of Platycrinites and one species of Eucladocrinus are considered valid in the Keokuk Limestone through St. Louis Limestone of the stratotype area. Valid species include Platycrinites saffordi (Hall), P. sarae (Hall), P. georgii (Hall), P. pumilus (Hall), P. brevinodus (Hall), P. niotensis (Meek and Worthen), and Eucladocrinus millebrachiatus Wahsmuth and Springer. Nomenclatoral changes include the following: 1) P. sarae is redescribed and all junior synonyms are removed; 2) P. georgii is a valid senior synonym of P. bonoensis (White), P. aeternalis (Miller), P. boonvillensis (Miller), and P. cauducus ; 3) P. pentagonus (Miller) is a junior synonym of P. niotensis ; 4) P. pumilus is a valid senior synonym of P. prattenanus (Meek and Worthen), and P. monroensis (Worthen); 5) P. bloomfieldensis (Miller) is designated as a nomen dubium; and 6) Eucladocrinus millebrachiatus immaturus is a junior synonym of E. millebrachiatus.
The evoluton of new species in Platycrinites was by a combination of cladogenesis and possibly anagenesis. Platycrinites sarae evolved from P. saffordi possibly through anagenesis, P. pumilus evolved from P. niotensis through cladogenesis, and P. hemisphaericus evolved through cladogenesis from P. brevinodus , although P. hemisphaericus does not occur in the geographic area of this study.
Volume 1 contains the text of the treatise, and volume 2, 847 plates. Of the 3620 validly proposed generic taxa of Foraminiferida considered 2455 genera are recognised, described and illustrated, 960 regarded as synonyms, 208 considered systematically unrecognisable, 16 too late for detailed inclusion. They are placed in 12 suborders, 74 superfamilies, 296 families, 302 subfamilies. A systematic index is included. The systematic arrangement of genera is alphabetical within the various subfamily or family categories, and the family group taxa within the suborders are arranged in order of presumed evolutionary sequence or increasing complexity. Descriptions are generally focused on test morphology, both external and internal, but some information concerning the living organism is summarized for the few that are known. Geologic range is given to the level of the geologic series of epoch, and known geographic occurrence and a limited amount of ecologic information is included. In view of the very large number of taxa considered, morphologic descriptions are as concise as possible, consistent with the inclusion of the available information. Morphologic terms used are defined in a glossary, in which reference also is given to other terms proposed by various writers. -from Authors
Based on the latest information available, total foraminiferal generic and family diversity through time is plotted by geologic stages, as is planktonic generic diversity. Phylogenetic diagrams are presented for the foraminiferal families within each suborder, and relationships of suborders postulated. Histograms are presented of generic diversity by geologic stage within each suborder. Increased diversification of planktonic taxa in the Mesozoic and Cenozoic has coincided with similar diversification of larger taxa of the Textulariina, Miliolina, and Rotaliina, and all have shown coincident times of extinction. Any marked environmental change in the photic zone or in shallow waters of the continental shelves may reverse the evolutionary pattern and lead to extinction of the specialized taxa. -from Authors
Molecular phylogenies of foraminifera are commonly inferred from the small subunit rRNA (SSU) genes, which can easily be obtained
from single cells isolated from environmental samples. The SSU phylogenies, however, are often biased by heterogeneity of
substitution rates, and their resolution of higher level relationships is often very low. The sequences of protein-coding
genes provide an important alternative source of phylogenetic information, yet their availability from foraminifera has been
limited until now. Here, we report the first extensive protein sequence data for foraminifera, which comprises 90 actin sequences
for 27 species representing five major foraminiferan groups. Our analysis enables grouping foraminiferan actins into two main
paralogs, ACT1 (actin type 1) and ACT2 (actin type 2), and several actin-deviating proteins. Phylogenetic analyses of ACT1
and ACT2 confirm the general structure of foraminiferan phylogenies inferred from SSU rDNA sequences. In particular, actin
phylogenies support (1) the paraphyly of monothalamous foraminifera, including the allogromiids, astrorhizids and athalamids;
(2) the independent divergence of miliolids and their close relationship to Miliammina; (3) the monophyly of rotalids; and (4) the rotaliid ancestry of globigerinids. Some foraminiferan taxa can be distinguished
in actin sequences by the presence of group-specific introns (rotaliids, allogromiids) or absence of any introns (soritids
ACT1).