Evolution and Geological Significance of Larger Benthic Foraminifera

Second Edition

Marcelle K. Boudagher-Fadel

Biology and Evolutionary History of Larger Benthic Foraminifera

1.1 Biological Classification of Foraminifera

1.1.1 Introduction

Foraminifera are unicellular eukaryotes characterized by streaming granular ectoplasm usually supported by an endoskeleton or “test” made of various materials. They are considered to fall within the phylum Retaria, which in turn is within the infrakingdom Rhizaria (Ruggiero et al., 2015). Their cellular cytoplasm is organised into a complex structure by internal membranes, and contains a nucleus (Plate 1.1, Figs. 1–2), mitochondria, chloroplasts (when present) and Golgi bodies (Plate 1.1, Figs. 3–5; Plate 1.2). In foraminifera, the cytoplasm is subdivided into the endoplasm, in which the nucleus (or nuclei, as many foraminifera are multinucleate) and other organelles are concentrated, and ectoplasm, which contains microtubules and mitochondria (Hemleben et al., 1977; Anderson et al., 1979; Alexander, 1985). Foraminifera are characterised by specialized pseudopodia (temporary organic projections) known as granuloreticulopodia (also called rhizopodia), which are thread-like, granular, branched and anastomosing filaments that emerge from the cell body (Fig. 1.1). The unique ability of the foraminiferal ectoplasm to assemble and disassemble microtubules allows them rapidly to extend or retract their rhizopodia (Bowser and Travis, 2002). The functions of the rhizopodia include movement, feeding, and construction of the test.

Fig. 1.1.
Larger foraminifera Heterostegina depressa with thread-like, granular, branched and anastomosing filaments that emerge from the cell body (courtesy of Prof Röttger).

Both living and fossil foraminifera come in a wide variety of shapes and sizes. Academically, the study of their preserved tests is referred to as micropalaeontology, and although their typical size is sub-millimetric, they have occurred in the geological past with sizes up to ~150mm. In addition, they occur in many different environments, from freshwater to the deep sea, and from near surface to the ocean floor. Their remains are extremely abundant in most marine sediments and they live in nearly all marine to brackish habitats (Fig. 1.2).

Fig. 1.2.
The ecological distribution of foraminifera.

Foraminifera that dwell in freshwater do not produce tests (Pawlowski et al., 2003), however most marine foraminiferal species grow an elaborate test or endoskeleton made of a series of chambers (Fig. 1.3).

Fig. 1.3.
The different shapes of foraminiferal test; a = axis of the test; u = umbilicus.

These single-celled organisms have inhabited the oceans for more than 500 million years. The complexity of their fossilised test structures (and their evolution in time) is the basis of their geological usefulness. The earliest known foraminifera, mostly forms that had an organic wall or produced a test by agglutinating particles within an organic or mineralized matrix, appeared in the Cambrian, and were common in the Early Paleozoic (Platon et al., 2001). Forms with calcareous tests appeared by the Early Carboniferous, becoming diverse and abundant, with the evolutionary development of taxa with relatively large and complicated test architecture by the Late Paleozoic. Their long, diverse and well-documented evolutionary record makes Foraminifera of outstanding value in zonal stratigraphy, and in paleoenvironmental, palaeobiological and palaeoceanographic interpretation and analysis.

Fig. 1.4.
An enlargement of the surface of a Heterostegina shell showing two types of holes. 1) the many small pores which are characteristic of all foraminifera. They do not form open connections between the test lumen and the sea water, but are closed by a membrane. Only small molecules like nutrition salts may penetrate, which are important for the nutrition of the algal endosymbionts. 2) the larger openings on the lateral test surface are openings of the canal system of the chamber walls and chamberlet walls (shown in Fig. 1.17) with the outside world. In Heterostegina depressa, and other nummulitids, the protoplasm emerges through these openings and forms a thin veil covering the test surface in living specimens, which is also responsible for the secretion of the elastic inanimate protective sheath with radiating processes that covers the test, attaching it to the algal or rock surface. This function is described and illustrated by Röttger (1983). The apertures in the last chamber are masked in Heterostegina.

Fossil and living foraminifera have been known and studied for centuries. They were noted by Herodotus (in his Histories written in the 5th century BC) as occurring in the limestone of the Egyptian pyramids, which in fact contain fossils of the larger benthic Foraminifera Nummulites. The name Foraminifera derives from the apertures and the “foramen” connecting successive chambers seen in their tests. The test surfaces of many foraminiferal species are covered with microscopic holes (foramen), normally visible at about x40 magnification (Fig. 1.4). Among the earliest workers who described and drew foraminiferal tests were Anthony van Leeuwenhoek in 1600, and Robert Hooke in 1665, but an accurate description of foraminiferal architecture was not given until the 19th century (Carpenter et al., 1862).

The first attempts to taxonomically classify Foraminifera placed them within the genus Nautilus, a member of the phylum Mollusca. In 1781, Spengler was among the first to note that foraminiferal chambers are in fact divided by septa. In 1826, d’Orbigny, having made the same observation, named the group Foraminifères. In 1835, Foraminifera were recognised by Dujardin as protozoa, and shortly afterwards d’Orbigny produced the first classification of foraminifera, which was based on test morphology. Modern workers normally use the structure and composition of the test wall as a basis of primary classification, and this approach will be followed in this book.

Despite the diversity and usefulness of the foraminifera, the phylogenetic relationship of Foraminifera to other eukaryotes has only recently emerged. Early genetic work on the origin of the Foraminifera postulated that the foraminiferal taxa are a divergent “alveolate” lineage, within the major eukaryotic radiation (Wray et al., 1995; Baldauf, 2003). Subsequently, many researchers have tried to determine the origin of the foraminifera, but molecular data from Foraminifera generated conflicting conclusions.

Molecular phylogenetic trees have assigned most of the characterised eukaryotes to one of eight major groups. Baldauf (2003) tried to resolve the relationships among these groups to find “the deep roots of the eukaryotes”. He placed them in the “Cercozoa” group. Cercozoans are amoebae, with filose pseudopodia, often living within tests, some of which can be very elaborate. The phylum Cercozoa was originally erected by Cavalier-Smith (1998) to accommodate the euglyphid filose amoebae, along with the heterotrophic cercomonadids and thaumatomonad flagellates, which were shown to be related by Cavalier-Smith and Chao (1997).

However, the origins of both Cercozoa and Foraminifera have been evolutionary puzzles because foraminiferal ribosomal RNA gene sequences are generally divergent, and show dramatic fluctuations in evolutionary rates that conflict with fossil evidence. Ribosomal RNA gene trees have suggested that Foraminifera are closely related to slime moulds and amoebae (Pawlowski et al., 1994), or alternatively used to suggest that they are an extremely ancient eukaryotic lineage (Pawlowski et al., 1996). In 2003, Archibald et al. found that cercozoan and foraminiferal polyubiquitin genes (76 amino acid proteins) contain a shared derived character, a unique insertion, which implies that Foraminifera and Cercozoa indeed share a common ancestor. Archibald et al. (2003) proposed a cercozoan-foraminiferan supergroup to unite these two large and diverse eukaryotic groups. In recent molecular phylogenetic studies, Nikolaev et al. (2004) adopted the name “Rhizaria” (proposed first by Cavalier-Smith, (2002), which refers to the root-like filose or reticulose pseudopodia) and included the Retaria, Cercozoa and Foraminifera within this supergroup. While additional protein data, and future molecular studies on Rhizaria, Retaria, Cercozoa and Foraminifera, are necessary to provide a better insight into the evolution of the pseudopodial divisions, the placement of the Foraminifera within the Rhizaria appears to be well supported (Pawlowski and Burki, 2009; Ruggiero et al., 2015; Burki et al., 2016) (see Fig. 1.5).

Fig. 1.5.
A consensus phylogeny of eukaryotes from Burki et al., (2016).

Similarly, the higher taxonomy of the Foraminifera is still unsettled. Although proposed as the Class Foraminifères by d’Orbigny (1826), throughout most of the 20th century the group was considered as the Order Foraminiferida, and the major subdivisions were considered to be suborders. In 1992, Loeblich and Tappan recommended Lee’s (1990) re-elevation of the Order Foraminiferida to Class Foraminifera, thereby elevating the suborders to orders. Sen Gupta (1999), Platon et al. (2001) adopted the class-level designation with some modifications at the order-level that have been largely supported by molecular phylogenies (Mikhalevich, 2000, 2004; Pawlowski and Burki, 2009; Groussin et al., 2011). Most recently Ruggiero et al. (2015) suggested a subphylum status for the Foraminifera.

Recognizing that the classification of Foraminifera is still in flux, in this edition (in contrast to BouDagher-Fadel (2008)) we accept the elevation of the Order Foraminiferida to Class Foraminifera, and the concomitant elevating of the previously recognized suborders to the ordinal level.

1.1.2 Larger Benthic Foraminifera

Foraminifera are separated into two groups following their life strategy, namely the planktonic and the benthic foraminifera. Fewer than 100 extant species of foraminifera are planktonic, though they occur worldwide in broad latitudinal and temperature belts. They drift in the pelagic waters of the open ocean as part of the marine zooplankton (see Fig. 1.6). Their wide distribution and rapid evolution reflect their successful colonization of the pelagic realm. When this wide geographical range, achieved through the Late Mesozoic and in the Cenozoic, is combined with a short stratigraphic time range due to their rapid evolutionary characteristic, they make excellent index fossils at family, generic and species levels (see BouDagher-Fadel, 2013, 2015).

Fig. 1.6.
(A) Globigerinoides sacculifer (Brady), a spinose species with symbionts carried out by rhizopodial streaming on the spines (courtesy of Dr Kate Darling); (B) Neogloboquadrina dutertrei (d’Orbigny), a non-spinose species (courtesy of Dr Kate Darling). See BouDagher-Fadel, 2015 for a detailed study of the planktonic foraminifera mode of life, classification and distribution.

The benthic foraminifera, however, are far more diverse, with estimates of roughly 10,000 extant species. Benthic foraminifera live, attached to a substrate or free of any attachment, at all ocean depths, and include an informal group of foraminifera with complicated internal structures known as “larger benthic foraminifera”. It is these forms that are the principle subject of this book.

The larger benthic foraminifera are not necessarily morphologically bigger than other benthic foraminifera, although many are, but they are characterised by having internally complicated tests. While one can identify most small benthic foraminifera from their external morphology, one must study thin sections to identify many of the larger benthic foraminifera, using features of their internal test architecture (Fig. 1.7).

Fig. 1.7.
Examples of two dimensional sections through the three-dimensional test of a larger, three layered foraminifera. A) Sections through a milioline test (modified from Reichel, 1964). B) Three-dimensional view of Lepidocyclina sp., showing the distinction between equatorial or main chamberlet cycles and lateral chambers (modified from Vlerk and Umbgrove, 1927).

Larger benthic foraminifera develop characteristically complicated endoskeletons, which permit the taxa to be accurately identified, even when they are randomly thin-sectioned. The tests of dead, larger foraminifera can dominate carbonate sediments, and foraminiferal-limestones are extensively developed in the Upper Paleozoic, the Mesozoic (especially the Upper Cretaceous) and in the Cenozoic (see Fig. 1.8).

Fig. 1.8.
A. Eocene limestone containing fossil porcelaneous foraminifera; a) Alveolina sp., b) Orbitolites sp., c) Quinqueloculina sp., from France. B. Miocene limestone dominated by Lepidocyclina spp. from Indonesia, courtesy of Peter Lunt.

Following recent taxonomic studies and reassessments of classifications, we recognise 14 different large benthic foraminiferal orders (Fig. 1.9). The orders with larger foraminiferal lineages that are discussed in detail in this volume are the:

  • Parathuramminida

  • Moravamminida

  • Archaediscida

  • Earlandiida

  • Palaeotextulariida

  • Tetrataxida

  • Tournayellida

  • Endothyrida

  • Fusulinida

  • Lagenida

  • Involutinida

  • Miliolida

  • Textulariida

  • Rotaliida.

Throughout this book standard nomenclature is followed, so orders are expressed via the suffix “–ida”, or generically as “–ides” (e.g. Miliolida or miliolides). The suffix of “–oidea” is used to denote superfamilies, rather than the older suffix “-acea” following the recommendation of the International Commission on Zoological Nomenclature (see the ‘International Code of Zoological Nomenclature’, 1999, p. 32, Article 29.2). Families are designated via the suffix “–idae”. In this book, the suffix “–ids” is used to indicate a generic superfamily or family member (e.g. Fusulinoidea/ Fusulinidae or fusulinids).

Fig. 1.9
The geological range of the larger foraminifera orders and some selected, important families.

The study of living larger foraminifera shows that they occur abundantly in the shelf regions of most tropical and subtropical shallow marine, especially in carbonate-rich, environments. Indeed, they seem to have done so ever since the first larger foraminifera emerged during the Carboniferous. Again, from the study of extant forms, it seems that many larger foraminifera enclose photosynthetic symbionts, which appear to be essential to the development of most of the lineages with morphologically larger forms (Hallock, 1985; BouDagher-Fadel et al., 2000; BouDagher-Fadel, 2008).

From their structural complexity, and because of the diversity of the shelf environments that they inhabited, fossil larger foraminifera provide unique information on palaeoenvironments and biostratigraphy of shelf limestones around the world. Generally, in such environments, calcareous nannofossils are unavailable because of the shallowness of the marine environment and because of the recrystallisation of the calcite in the limestone matrices. Furthermore, macrofossils are relatively rare in these habitats. By the late 1920s, the larger foraminifera had become the preferred fossil group for biostratigraphy in several oil-rich regions including the Indonesian area, parts of Russia, and in the United States, especially western Texas. Larger foraminifera had the advantage that they were more abundant than molluscs, and additionally a scheme was developed that utilised assemblage zones, rather than percentages of forms to be found. Using molluscs to identify and correlate sections required extensive knowledge of both living and fossil species. The larger foraminiferal assemblage zones could be identified by the presence of a few key taxa, usually with use of a hand lens in the field. Some groups of larger foraminifera provide excellent biostratigraphic markers, sometimes the only ones which can be used to date carbonate successions (e.g. the fusulinids and schwagerinids in the Upper Paleozoic (Fig. 1.10A; 1.10B), orbitoidoids in the Middle to Upper Cretaceous (Fig. 1.10C), nummulitids in the Paleogene (Fig. 1.10D), and lepidocyclinids (Fig. 1.10E) and miogypsinids in the Oligocene and Neogene (Fig. 1.10F)). Provincialism was often a problem in these groups, but this is now well understood, so that biozonal schemes applicable to certain time intervals in defined bioprovinces have recently been erected and successfully applied (BouDagher -Fadel and Price, 2010a, b, 2014; BouDagher et al., 2015).

Fig. 1.10
Examples of larger foraminifera which provide excellent biostratigraphic markers, A) Fusulina; B) Schwagerina; C) Lepidorbitoides; D) Nummulites; E) Lepidocyclina; F) Miogypsina.

Larger foraminifera are an ideal “group” of organisms to use in the study of general evolutionary theory. Their fossil record is so rich in individual fossils that assemblage concepts can be used, and both horizontal and vertical variation can be studied in the stratigraphic record. Their preference for certain marine environments is well understood and documented. Because representatives of most of the orders are still extant, it is also possible to infer their reproductive strategy, which as will be seen later, is quite complex.

This book does not attempt to present a comprehensive or extensive listing of all genera and species of larger foraminifera, but rather focuses on the taxonomy, phylogeny and biostratigraphic applications of the most important forms. For an almost comprehensive list, the reader can refer to Loeblich and Tappan (1988). In addition, for brevity, the complete references to genera and species are not given and again the reader can refer to Loeblich and Tappan (1988) and the contemporary, on-line literature. Finally, the reader can refer to Hottinger (2006) for an exhaustive set of definitions of terms used in the taxonomic description of the larger foraminifera, many of which, but inevitably not all, are also explained below.

1.1.3 Trimorphic life cycle in larger benthic foraminifera

Larger foraminifera may reproduce asexually by multiple fission, producing many hundreds of offspring, and at other times they reproduce sexually, many by broadcasting gametes. Röttger (1983) described the asexual reproduction of Heterostegina. He stated that the protoplasmic body leaves the test through an internally developed canal system. The spherical daughter cells are colourless and are without a calcareous test (Fig. 1.11; Plate 1.3, Fig. 3). A small part of the symbiont-containing residual protoplasm is then apportioned to each daughter cell. At this stage the test is formed and consist of two chambers, which as the juvenile grows are followed by the addition of further chambers. The growth rate of the calcareous tests of foraminifera is light-dependent (Röttger, 1983).

Fig. 1.11.
Schematic figures (in the centre) showing a trimorphic life-cycle of the larger benthic foraminifera Amphistegina gibbosa from Dettmering et al. (1998). The upper part shows the dimorphic life cycle, consisting of an alternation between a haploid, megalospheric gamont with its gametes, and the microspheric diploid agamont with its offspring produced by multiple fission. The lower part represents the megalospheric generation in a trimorphic cycle reproduced by cyclic schizogony, inserted between agamont and schizont. The photographs of living Heterostegina depressa (courtesy of Prof R. Röttger) show an alternation of generations in which a 2-4mm sized gamont (megalospheric generation) (on the left) alternates with an 1-2cm-sized agamont (microspheric generation) (on the right). During multiple fission of the agamont, the symbionts-containing protoplasm (top right) flows out of the calcareous test and then divides into 1000 to 3000 daughter individuals, the young gamonts. In addition to gamont and agamont forms another generation, which looks like a gamont of Heterostegina depressa, but which reproduces asexually (Röttger, 1990).

In other taxa, the process has some small differences. For example, in the species Amphistegina spp., the cytoplasm exits through the aperture (see Fig. 1.12). In the soritid foraminifera, the partitions of the final chambers are dissolved to form a brood chamber in which the daughter cells form (Röttger, 1984; 1990). After asexual multiple fission, the empty parent test becomes a lifeless grain of sediment.

Fig. 1.12.
Amphistegina: A) an axial section of a fossil specimen of Amphistegina; B) A live specimen showing the cytoplasm exiting through the aperture.

Larger foraminifera are dimorphic (having two forms), which is the result of the heterophasic alternation of generations between a haploid, uninucleate gamont (the sexual generation which produces gametes) and a diploid, multinucleate agamont (the asexual generation which produces daughter individuals by multiple fission) (Schaudinn, 1895; Röttger, 1990). The dimorphic forms usually exhibit different morphological characters; the two forms are called:

  • The asexual microspheric (or B-) form, which is larger, with numerous chambers, but with a small proloculus (first chamber, see Plate 1.3 and Fig. 1.11). It is this asexual generation which produces daughter individuals by multiple fission, and

  • the megalospheric (or A-) form, which is smaller with fewer chambers, but with a large proloculus. It is this sexual generation which usually produces gametes (see Fig. 1.11).

However, in addition to these two generations, a third generation is documented by many authors, where the agamont produces megalospheric schizonts instead of gamonts (see Fig. 1.11). This life cycle was first discovered by Rhumbler (1909), and since then has been recognised by many authors (Leutenegger, 1977; Röttger, 1990; Dettmering et al., 1998; Harney et al., 1998). Röttger (1990) cultivated Heterostegina depressa (Plate 1.3, Fig. 1) in the laboratory and was able to confirm the trimorphic cycle. Dettmering et al. (1998) and Harney et al. (1998) suggested that the trimorphic cycle can account for the abundance of the megalospheric generation in many populations. The schizonts, which are produced by asexual reproduction, in contrast to zygotes, which are too small to carry symbionts, begin their ontogeny as large symbiont-bearing cells. Harney et al. (1998) also suggested that the trimorphic cycle provides tremendous colonization potential, allowing foraminifera to rapidly increase their population densities sufficient to successfully sexually reproduce by gamete broadcasting, while at the same time promoting genetic divergence by amplifying the colonizing genotypes, all of which could promote relatively rapid rates of evolution.