SE Asian Cenozoic Larger Foraminifera: Taxonomic Questions, Apparent Radiation and Abrupt Extinctions

0. INTRODUCTION

The distribution of larger foraminifera in time is important as the identification of a continuous range with evolution and extinction datums is a key test of species concepts. With good age control on the sample sites, the evolution of novel characters, or the large scale trends in evolutionary series, can be compared over a wide area to shed new light on speciation and radiation. Historically important sites have been re-studied and data have been corrected to modern time scales. This has been merged with data from some new locations to give a nearly complete view of the evolution of larger foraminifera in SE Asia since the Middle Eocene. This article reviews the published and proprietary data on the larger foraminifera of SE Asia, especially the dating of sample sites.

1. SE ASIAN LARGER FORAMINIFERA

The Cenozoic larger foraminifera of SE Asia lived through the closure of the Mediterranean to Indo-Pacific seaway, as firstly India collided with Asia, and then the western part was isolated as the Mediterranean Sea when the Arabian plates collided with the Eurasian land-mass. Finally, SE Asia collided with the Philippine and Australian plates. What has become known as the Indo-Pacific realm is the area around SE Asia, with tropical to subtropical carbonate facies deposited in the latitudes between Japan and North Australia. This realm extends to isolated reefal bodies into the western Pacific (Cole, 1963, 1960, 1957a, b, 1954). The underlying geology centered on a continental mass called Sundaland (Figs. 1a, 1b) that had a complex tectonic history involving episodic subsidence, transgression, and relative sea-level rise from Mid Eocene to Early Miocene times (Lunt and Woodroof, 2021). This transgression made Sundaland an excellent place for carbonate sediments to be deposited and preserved, while passive continental margins were being subject to gradual eustatic sea-level fall (Haq and Al-Qahtani, 2005). The later Early Miocene to recent collision of the Australian and Philippine plates was mild compared to the Alpine Orogeny affecting the Mediterranean and Middle Eastern, so the stratigraphic record is much less faulted.

Figure  1.  (a) Map of sites in South East Asia mentioned in the text, centered on the continental plate of Sundaland; (b) regional map of South East Asia and the West Pacific Ocean showing sites mentioned in the text and the faunal provinces of Pleistocene to recent high energy carbonate sands. Some sites dominated by Schlumbergerella have minor Baculogyspinoides (based on Bromfield and Renema, 2011; Renema, 2002; Renema and Troelstra, 2001).

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Larger foraminifera have a long history of study in SE Asia and an unfortunate legacy of taxonomic problems at the species level. With definitions going back to the early 19th century, there are a host of poorly illustrated species names based on external features that are largely of ecophenotypic origin. In dimorphic taxa, the haploid and diploid generations (also known as the megalospheric and microspheric, or A and B forms) were often given separate names. It was only with the work of Tan (1932) and van der Vlerk (1959) that it was realized there was a common trend for gradual evolution (argued to be in very small saltation steps by Tan) which was observed in the gradually reducing juvenile stage of the test, a character which had not been observed in any detail by earlier workers. The international code for zoological nomenclature (ICZN) typological approach does not easily accommodate gradually evolving species and the status of species names in many larger foraminifera remains a difficult issue.

This review takes a practical approach and examines the lineages, which are distinct clades established by intense sampling of often continuous sections around SE Asia. These lineages can be grouped by evolutionary style. Larger foraminifera evolved through peramorphosis (see Table 1), and the classic genera show this style very clearly; which is why they are famously large (to several centimetres). In carbonate facies, there are also many associated taxa, such as Amphistegina and Sphaerogypsina that have only mildly peramorphic tests and are typically only about a millimeter in size. It is the strongly peramorphic forms that display orthoselection trends. They are also the forms that were major rock-forming organisms—not just through their increased size, but also their great abundance.

Table  1.  Glossary of specialist terminology

Anagensis: The evolutionary process that sees change from an ancestor to a descendant without branching. This contrasts with cladogenesis where there are branching and survival of two different descendants
Gerontic: The late adult life stage, in metazoans often associated with physical decline after losing the ability to reproduce, but in other organisms that reproduce just before death, the gerontic stage may have no link to a less viable morphotype
Heterochrony: Evolution of a morphotype by changing the time of onset or offset of different life stages (embryonic, juvenile, adult), often for different parts of the body at different rates
Orthoselection: A term proposed by Levit and Olsson (2006) to replace orthogenesis as the latter term ("straight creation") was synonymous with directed evolution. Levit and Olssen wanted a neutral term emphasising only the trend produced by prolonged and consistent selection force
Peramorphism: Peramorphic organisms develop enhanced adult morphologies, by rapid acceleration through the juvenile stage and extension of the adult stage by increased life span, perhaps with emphasized gerontic morphologies not seen in the ancestral forms

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2. INTRODUCTION TO THE LETTER STAGES

The evolution and extinction of larger foraminifera were the foundation of biostratigraphy in SE Asia through the Letter Stages. These were replacements for European Epochs and were based on generic level taxonomy, intensely studied in the first half of the 20th century on numerous outcrops in Java and Kalimantan (East Borneo). In 1965, Adams studied the exceptional and unbroken outcrop from Middle Eocene to basal Miocene in the Melinau Gorge, and in 1970, he wrote the most widely cited review of the Letter Stages since the summary of Rutten in van Bemmelen (1949). In 1984, Adams reviewed the data for Neogene biostratigraphy and the Letter Stages. In 2004, Lunt and Allan used planktonic foraminifera, nannofossils and strontium dating to better correlate the Letter Stages with standard time scales that had been improved by ODP/ IODP drilling and improved planktonic zonation schemes and time scales (Gradstein et al., 2004; Berggren et al., 1995, 1985). In addition, the application of ⁴⁰Ar/³⁹Ar dating and magnetic stratigraphy in the 1990's found errors in the correlation and calibration of previous Cenozoic time scales (Berggren and Prothero, 1992; Prothero and Swisher, 1992; Swisher and Prothero, 1990). Consequently early 1990's or older times scales have to be investigated and upgraded to modern time scales that have been stable since Gradstein et al. (2004). A modern summary of the Letter Stages in SE Asia was presented by van Gorsel et al. (2014).

The Letter Stages are observed in SE Asian sediments (based on fossil content, like the original terms Eocene, Oligocene, Miocene and Pliocene that they replaced) whereas the stages are defined on European stratotypes that can only be inferred. It is therefore preferable to discuss Letter Stages as the primary chronostratigraphic units, and only convert these to the European Stages through a standard time scale.

3. LIFE HISTORY STRATEGIES

Since at least Hallock et al. (1991), it has been thought that the life history strategies of larger foraminifera are linked to their adaptation to oligotrophic conditions. These life histories, which lead to a highly specialized test morphology, have then been subject to natural selection. The principle that life histories are subject to selection was highlighted by MacArthur and Wilson (1967) in their r/K selection theory that established a simple mathematical formula predicting evolution would move in one of two directions based on the selection of opposing population dynamics (where r is the maximum growth rate and K is the carrying capacity of the local environment). This theory has been criticized as too simple for many types of animals (Stearns, 1992) but it appears to remain valid for the protozoan larger foraminifera. The oligotrophic conditions of a tropical reef lead to niche stability as, while other factors may vary, the continuous bottleneck of nutrient-starved conditions continually selects forms with the optimal ability to survive this crucial restriction. This therefore favors highly specialized forms that are able to live at the carrying capacity of the environment (K-selection).

It is empirically observed that selection of highly optimized larger foraminifera has led to the development of six characters that are repeatedly seen in the fossil record.

(a) A tendency to large size.

(b) A tendency to reduce the juvenile stage, and to increase not only the proportion, but the duration of the adult stage.

(c) A tendency to have increased numbers of chambers or chamberlets.

(d) A tendency to acquire "lateral chamberlets" or cubiculae.

(e) A tendency to radial symmetry.

(f) A tendency towards increased size differentiation between the macrospheric or A generation (assumed to be haploid from extant foraminifera) and the microspheric or B generation, i.e., increased dimorphism.

The mechanism for evolution is dominantly heterochrony through the emphasis of the specialized adult test (peramorphism). All six characters listed above can be trends driven by heterochony, based on gradual shifts in the timing of different life stages. Consequently, the larger foraminifera are naturally prone to gradualism. This gradual evolution is remarkably slow, with rare exceptions such as the rapid evolution of the highly peramorphic test of Eulepidina prior to its migration out of central America (van der Vlerk, 1959). A combination of slow, gradual evolution and the trends listed above has led to application of the term orthogenesis or directed evolution. However, there is no known force guiding evolution other than K-selection pressure, and hence the term orthoselection is a clearer description (Levit and Olsson, 2006). The result can be summarized as the natural selection of protists that tend towards large, increasingly subdivided tests, with internal circulation based on stolon systems or nummulitic cords, highly optimized to a very specific, stable niche, in which they can be an abundant rock forming fossil. The outstanding mystery is how the process can be drawn-out over so many millions of years.

4. CLASSIFYING LARGER FORAMINIFERA

4.1 The Species Problem in SE Asian Larger Foraminifera

There are a large number of legally available names for SE Asian larger foraminifera. A response of adult test shape to the environmental energy has produced one type of physical diversity (Hallock and Glenn, 1986), whilst the slow, heterochronous process of evolution has produced another. Externally distinct test types are often classed as genera, but it is unusual to have species with a distinct morphology and a discrete and contiguous stratigraphic range indicative of an evolution and extinction datum. However, two examples of this are the larger foraminifera Lepidocyclina ferreroi and Cycloclypeus annulatus.

The taxonomic problems in larger foraminifera also extend to the genera. There are lineages with multiple intermediate forms that range over many millions of years, and which include many generic or sub-generic names such as Neorotalia-Miogypsinoides-[Miogypsinella, Miogypsinodella]-Miogypsina and Lepidosemicyclina; as well as Lepidocyclina (Nephrolepidina), Lepidocyclina (Multilepidina), Lepidocyclina (Trybliolepidina). Some workers (e.g., Adams, 1984) placed Eulepidina in a subgenus rank Lepidocyclina (Eulepidina). On purely morphological criteria this seems reasonable, but knowledge of the stratigraphic ranges of these forms changes our views. In the Neorotalia to Lepidosemicyclina example, good age dating shows a continuous morphoseries where there was peramorphic addition of several new features within a single lineage. In contrast, the Lepidocyclinids have peramorphism of one lineage, plus age data showing that the Eulepidina forms are a much older clade that had separated before the group migrated out of Central America.

The excellent stratigraphic record of larger foraminifera also means the unusual property of iterative evolution can be demonstrated. This is clearly seen in the development of Tansinhokella/Spiroclypeus which is recorded in both European and SE Asian assemblages during the Late Eocene (Less and Özcan, 2008). These forms are missing from Early Oligocene assemblages, but the gradual re-evolution of Heterostegina (Vlerkina) into Tansinhokella and then Spiroclypeus sensu stricto was documented in NE Java by Muhar (1957) and was repeated in the same area with planktonic and strontium age dating by Lunt and Renema (2014). It is interesting that the Eocene evolution of Tansinhokella from a Heterostegina ancestor just reached the Spiroclypeus form in S. granulosus from the Priabonian (Col de Priabona) in Italy over a period of nearly four million years. In the Oligocene of SE Asia, the repeated evolution of Heterostegina (Vlerkina) to Tansinhokella then Spiroclypeus again took about four million years (Lunt and Renema, 2014)

The sum of all these issues means that the application of the ICZN rules and the Linnaean system based on a defining type specimen, and an assumption that species are morphologically distinct, is not optimal for larger foraminifera. It is argued below that if we maintain the Linnean approach this will require us to have a much simpler taxonomy with fewer names, and become taxonomic "lumpers", simply because splitting species becomes un-defendable under ICZN rules.

4.2 Choosing an Appropriate Scale of Observation

If we assume that all species are morphologically distinct and can be classified by a typological approach (assuming adequate quality of preservation), then we can proceed with the classic method of observations beginning at the individual outcrops, and build an evolutionary history from the local to the general. However, if we suspect a mixture of anagenesis within a lineage that is also prone to ecophenotypic variation as well as occasional cladogenesis, then we must adopt a different scale of observation to identify each property. In this revised approach, the stratigraphic continuity of a morphotype becomes a key test of which features have an evolution and an extinction datum, and which features are probably a response to environmental or other influences. Such a test of context is established in metazoan paleontology where sexual dimorphs are required to have the same ages of evolution and extinction.

The summaries shown in Figs. 2, 3 and 4 show morphological trends in Oligo-Miocene larger foraminifera, emphasising the features that early workers noted to have biostratigraphic importance, namely the heterochronic changes in the embryonic and juvenile stages. The ecophenotypic variation of shape and external morphology is noted above, and was also emphasized as a non-evolutionary variable in a detailed study of Cycloclypeus by Laagland (1990).

Figure  2.  Lineages and biometric characters of nepionic chambers in Miogypsinids and Lepidocyclinids. Species of Miogypsina and Miogypsinoides based on Drooger (1993, Fig. 64); Raju (1974, Fig. 37) calibrated to outcrops samples based on van Vessem (1978, Fig. 60) and Lunt (2013). Species of Lepidocyclina from various sources but biometrics calibrated to planktonic zones in Ho (1973), van Vessem (1978), van der Vlerk and Postuma (1967), Lunt and Allan (2004), and Lunt (2013). Note the embryonic chambers of Miogypsinids and Lepidocyclinids are not shown at the same scale.

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Figure  3.  Summary of biometric trends in factor A of Lepidocyclina from well constrained study sections in SE Asia plus one point from the Mediterranean. Well names refer to samples in the study of Ho (1973).

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Figure  4.  Summary of reduction of the juvenile stage in Cycloclypeus in the Indo-Pacific as reflected in the heterochronous reduction of the ancestral heterostegine whorls (pink shading), with notes on well-dated Oligocene to basal Miocene samples in the Mediterranean. The first two chamber are the embryont (no colour). The nepionic (juvenile stage) chambers are from the third chamber to the last heterostegine chamber. All examples have multiple, adult, annular whorls of the cyclocleipid form, but only the first of these is shown on these sketches (green shading).

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It is important to note that heterochronous evolution of the life stages is not precisely linear. Many workers such as Drooger and Raju (1978), Laagland (1990), Chaproniere (1980) and many others have noted that local populations can have a modal value for a biometric character, with low population deviation, but adjacent samples have variation in the same parameter outside the standard deviation or nearby samples, and sometimes in reverse to the general long-term trend up-section. This variance limits the precision of the biometric technique for high resolution biostratigraphy, but it does not invalidate the overall, larger scale trend that is repeatedly observed at multiple sites, over a wide area.

It can be interpreted that while a long-term orthoselection pressure is evident on these peramorphic lineages, there is interference from other factors. For instance, Fermont (1977), Laagland (1990) and Drooger (1993) all report variation in embryont size relative to water depth (see below). Such local variation could produce slight, short term phenotypic responses to the embryonic and juvenile stages in some populations that temporarily overprint the orthoselection pressure. In other words, even though the orthoselection pressure is weak, it has been present for the long term and eventually dominates over short term ecophenotypic variation that lacks a consistent selection pressure.

Figure 2 shows a summary for the Miogypsinids and Lepidocyclinids with the general trends of lineages based on published sources. The evolutionary development of Miogypsinoides to Miogypsina and then Lepidosemicyclina, and the lineage of Lepidocyclina (Neprolepidina) to L. (Trybliolepidina) with a L. (Multilepidina) clade are not generally contested. This diagram differs from previous publications as it shows the biometric parameters and times of cladogensis fixed to well constrained age data from new outcrop and oil company exploration reports (detailed in Lunt, 2013; Lunt and Allan, 2004) and standardized on a modern time scale.

Figure 3 shows a detailed plot for Lepidocyclina factor A, the degree of enclosure of the protoconch by the deuteroconch (van der Vlerk, 1963) from mostly SE Asian sources but with some Mediterranean data. At any time, there is up to 5% variation in factor A, suggesting a biostratigraphic resolution not better than about 4 Ma. The overall trend is the same in both the Mediterranean and the Indo-Pacific, suggesting a single, geographically widespread population subject to the same orthoselection pressure. To argue for genetically separate lineages in different geographies raises the question as to why the local lineages then kept pace with each other over a long period. If they were truly separate, it is more likely the two heterochronic evolutionary trends would diverge. When there was true cladogenesis (e.g., Miogypsina from Miogypsinoides), the rates of heterochronic change then varied between genetically isolated lineages (Fig. 2). By the later part of the Early Miocene, Miogypsinoides had a reduced juvenile spire of five or six chambers, but there was faster acceleration through juvenile stages in Miogypsina, and the juvenile spiral had shrunk to achieve bispiral nepionic forms by lowest Tf.

In the Mediterranean, populations of Lepidocyclina with factor A of 40% coincide with the Miogypsinoides to Miogypsina evolution datum, as well as the evolution datum of Globigerinoides and the extinction of Helicosphaera recta in Cyprus(Lunt, 1984, nannofossils by O. Varol). The evolution of Miogypsina is also close to the lowest Paragloborotalia kugleri proxy for base Miocene in Libya (Abdulsamad and Barbieri, 1999), appears at the Te4 to 5 boundary (base Miocene) in India (Raju, 1974), and in the Java Sea where Lepidocyclina again has a factor A of 40% (Lunt and Renema, 2014; van Vessem, 1978; van der Vlerk and Postuma, 1967). In North Luconia, the base Miogypsina datum is associated with Lepidocyclina with 40% enclosure (Ho, 1973), and a similar value is observed at the Oligo-Miocene boundary around the northern coasts of Australia and New Zealand (Chaproniere, 1980). Shortly after this, the synchronous appearance of bispiral Miogypsina is seen in basal Lower Tf, upper Zone N5, in both the Mediterranean and SE Asia.

The genus Cycloclypeus has been studied biometrically in both SE Asia and the Mediterranean (Laagland, 1990; Tan, 1932) and very simple biostratigraphic relationships at a larger scale can be correlated across the entire ocean (Fig. 4). The oldest records of this genus in Europe (e.g., Özcan et al., 2009) are of a few specimens of Zone O2 age, but in SE Asia, there is a single Zone O1 site (Cimanggu, Tan, 1932, dated as c. 32–33 Ma on strontium isotopes and planktonic foraminifera; Lunt, 2013), which has been used to tentatively suggest that Cycloclypeus migrated out of SE Asia to the west (Renema, 2015). The numerous Mediterranean sites studied by Laagland (1990; Spain, Italy, and Israel) had planktonic biostratigraphy to date Cycloclypeus-rich samples as old as uppermost Td to Te1 (Lepidocyclinids, Nummulitids and O4-O5/NP24 planktonic fossils; so about 28 to 29.5 Ma), to as young as later Te4 (Miogypsinoides bantamensis and Paragloborotalia kugleri, Zone M1, c. 24 Ma). In both SE Asian and European data sets, the number of nepionic chambers decreases from 28 to 21 in the older Oligocene records, to typically 19–17 chambers near the Oligo-Miocene boundary (Te4-5, Zone M1). On top of this basic correlation, there was the appearance of a form with a protoconch diameter half that of the ancestral forms (Cycloclypeus. eidae) that appeared abruptly in SE Asia within Te1 times (between Tan's Ciapus sites as young as O4, Lunt, 2013 and Sample 2k/09/24 of Lunt and Renema, 2014, Zone O5, c. 28–28.5 Ma). This distinct form is absent in the oldest of Laagland's Td-Te1/O4-5 faunas, but is present in his Zone O6 and younger samples. These C. eidae types have similar numbers of nepionic stages to the co-existing C. koolhoven-droogeri-mediterraneus forms with large embryonts (cf. Fig. 4 of Renema, 2015), and their status as a separate evolutionary lineage is unclear. During the Late Oligocene and Early Miocene times, these C. eidae forms showed a gradual tendency to evolve a larger protoconch (Renema, 2015; Laagland, 1990), until they cannot be distinguished from the C. mediterraneus forms. Laagland's study demonstrated that there was a clear evolutionary trend in the reduction of nepionic stages through time, but there was considerable local and apparently random biometric variation in populations of the same age (see his data re-plotted in Renema, 2015). In other words, there is much small scale variation within a longer term trend. Just as Tan's (1932) concept of small saltatory steps in nepionic evolution of Cycloclypeus has been disregarded as over-emphasis of statistically insignificant variation, some modern suggestions of lineages and species can be questioned in the same way. The larger scale data seems to show simple trends that have properties in time linked to evolution and extinction datums, and simple anagenic trends in-between, suggesting a single evolutionary lineage. So far the appearance of the C. koolhoveni, C. eidae, C. annulatus and C. carpenteri forms is the only division of the genus Cycloclypeus that have survived such testing (Renema, 2015).

In light of these observations calibrated in time, it is suggested that a corollary of ranking the biometric measurement of peramorphic properties so highly is that it emphasiszes natural evolutionary patterns, but also it suggests less provinciality than the large number of available regional species names for each lineage might suggest.

4.3 Comparing Neogene Larger Foraminifera to Nummulites

This view of larger foraminiferal lineages with low species diversity seems to contrast with the summaries for the Paleocene and Eocene Nummulites of western Tethys (e.g., Schaub, 1981; approximately 130 species, updated and annotated for the Indo-Pacific by Renema, 2002). In these schemes, there are only a handful of major lineages, but these branches have diversified through time, resulting in multiple concurrent species, each given a short range.

This is proposed here to be a framing bias in how taxonomy is applied, based on species concepts and an absence in the ICZN method for defining species boundaries. In the shallow benthic zone [SBZ] scheme (Serra-Kiel et al., 1998), based on Nummulites, the SBZ 17-18 boundary does not stand out any more than any other of the other zonal boundaries, and each zonal boundary is implied to have been a time of extinction and evolution (Fig. 5).

Figure  5.  Comparison of a high resolution species approach (left) and a lineage morphology approach (right). The latter display of species shows apparently lower zonal resolution but a better portrayal of the paleontological history of the Nummulitids in the Middle and Later Eocene, especially the two main extinction events at top Letter Stage Ta and top Tb.

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In contrast, the summary by Eames in Morley Davies et al. (1971) presented an alternative view of the evolution of the Nummulites that is arguably more natural than a tabulation of Linnean binomials. This observes a well-known radiation of many Nummulitids following the six trends in larger foraminifera listed above, driven by peramorphism to an acme in the late Middle Eocene, then collapsed at a mass extinction and a return to assemblages dominated by simple Nummulites and the ancestral Palaeonummulites (e.g., Racey, 1995).

In the Middle Eocene the larger foraminifera were a far more important rock building organism, prior to the expansion of scleractinian corals (Perrin, 2002). It is therefore possible that there was greater diversity and consequently more sub- lineages and species of Nummulites than observed in the Miocene Lepidocyclinids and Miogypsinids. However, the contrast shown in Fig. 5 emphasizes an approach to taxonomy where long-term evolutionary trends can be better used as a framework to rank the morphological criteria chosen by stratigraphic continuity to define species. Unfortunately, the Paleogene carbonate record in SE Asia is very limited due to non- deposition. The Mediterranean and Middle East have many outcrops but these have been subject to deformation and faulting during the Alpine Orogeny. Both areas are handicapped by the inability of strontium dating to offer independent age control, as the sea-water calibration curve has a negligible gradient until virtually the Eocene-Oligocene boundary.

5. MIGRATION EVENTS

Migration needs to be considered in evolutionary studies of larger foraminifera for two reasons. Firstly, there have been proposals that depth migration over time leads to a morphological selection through an ecophenotypic response. Secondly, there has been an assumption that larger foraminifera migrate slowly across the Mediterranean to Indo-Pacific Ocean. This latter point implies that geographically separate lineages are potentially allopatric isolates that could be the source of cladogenic speciation. The validity of these ideas is challenged.

5.1 Migration with Depth/Environment

In living Operculina in the Gulf of Aqaba Fermont (1977) found a tendency towards increased protoconch size with habitat depth. He also proposed a similar trend in a fossil species of Discocyclina (Fermont, 1982). Hallock (1985) suggested that this was an ecophenotypic response; that the larger proloculus embryonts would preferentially survive at the deeper, darker depths. Drooger (1993) went one step further and suggested that variation in a morphocline of an entire lineage was the result of a shift in environmental habitat of the whole lineage, and that "the results [of ontogenetic measurements] are not really elucidating evolution; actually environmental changes seem to play an important if not dominating role".

Drooger noted that this shift was comparable to the data of Ozawa (1975) on simple biometrics (the size of the protoconch) in Permian fusulinids, which was cited by Gould and Eldridge (1977) in their proposal of punctuated equilibrium as one of the few possible fossil records of gradual evolution. Drooger argued that the observations of Fermont undermined such gradual morphometric changes as merely indicating gradual changes in environment, over geological time. Drooger published very little on the stratigraphic distribution of his material, and it is by applying a stratigraphic test that this negative view of gradual evolution can be challenged. Observation shows that biometric characters related to nepionic acceleration are highly reliable in determining stratigraphic position at separate locations on either side of the Borneo land mass (Fig. 3; Ho, 1973; van der Vlerk and Postuma, 1967). During the thirty million years of evolution of Cycloclypeus recorded by Tan (1932; see Fig. 4), there was a prolonged, one-way, evolutionary trend, that is hard to explain as a gradual migration of the genus through an environmental morphocline. It is highly unlikely that the populations in all these areas migrated in the same way, and at the same rate.

5.2 Geographic Migration

Adams (1984) discussed the possibility that the Lepidocyclinid group, the first appearance of which defines the base of Letter Stage Td, could have migrated gradually across Tethys at a rate slow enough to be detected in the stratigraphic record. This was mainly because his records had more instances of overlap of Lepidocyclinids with Nummulites (extinct at top Td) in the west, along with independent planktonic foraminiferal age control. His Indo-Pacific data summary chart had no records of samples with both Lepidocyclinids and Nummulites along with Zones O1-O2 plankton, although he acknowledged samples with Nummulites and Lepidocyclinids were known in the Indo-Pacific region. Allan et al. (2000, also Lunt and Allan, 2004 using a more modern sea-water calibration curve of McArthur and Howarth, 2004) have strontium dates for the Lepidocyclinid group in the Papuan region as old as about 32 Ma, and also found with Zone O2 planktonic foraminifera (see below).

Modern summaries from the Mediterranean use the base Td migration to define the base of the SBZ 22, dated as being mid-Rupelian (Serra-Kiel et al., 2016). Some supporting data in papers such as Özcan et al. (2009) show the base of this zone within Zone O2. Therefore the modern data indicates very rapid dispersion of larger foraminifera across the entire Mediterranean and Indo-Pacific areas.

BouDagher-Fadel and Price (2013) proposed that there was diachronous migration of the miogypsinid lineage over a few million years from west to east across the Mediterranean and Indo-Pacific realms, although their paper neither cited or contained any age data other than summary charts. The evolution of Miogypsinoides from N. mecatepacensis defines the base of Te4 (Muhar, 1957; where N. mecatepacensis was called Miogypsinoides "praeubaghsi"). The evolution of Miogypsina from Miogypsinoides defines the base of Te5 (=Upper Te), and the final extinction of the lineage (including Lepidosemicyclina) was the mass extinction event at the top of Tf2 (Lower Tf). On the figures of BouDagher-Fadel and Price (2013), these boundaries are not honoured by the ranges of the defining taxa. Their Letter Stage calibration to standard chronostratigraphic stages was derived from the very short review of BouDagher-Fadel and Banner (1999). However, Allan et al. (2000), Lunt and Allan (2004) and van Gorsel et al. (2014), based on SE Asian service company reports, re-adjusted the Letter Stage to planktonic zonal correlations and added independent age dating from strontium isotopes. This made the time scale and Letter Stage calibration of BouDagher-Fadel and Banner (1999) obsolete, and the paper of BouDagher-Fadel and Price does not cite any data to support gradual migration of this lineage across Tethys. Data in this present paper shows the base Te5 evolution of Miogypsina to have been at the same time from the Mediterranean to East Java.

BouDagher-Fadel and Price (2017) also proposed that orthophragminid forms (the Discocyclina group) migrated gradually to the Indo-Pacific area, arriving in the Lutetian (Zone E7-8), some ten million years after their first appearance in late Thanetian (Zone P4b) in the Mediterranean. However, there is a lack of sedimentary record over most of SE Asia before the mid Lutetian (and even these earliest sediments are non-marine facies until latest Lutetian; van Bemmelen, 1949). Rare Paleocene limestones on Java contain Discocyclina (Jatibungkus Limestone; Lunt, 2013, with Paleocene Miscellanea miscella and Distichoplax biserialis, and Ranikothalia and the distinctive Paleocene to?Early Eocene algae Distichoplax biserialis- cf. Sarkar, 2018; with some discussion of rare instances possibly into the "Mid" Eocene of Papua in Lunt and Allan, 2004). Numerous limestones mentioned in Liechti (1960) from calci-turbidites in the Crocker and Trusmadi formations of North Borneo contain Discocyclina with these same four Paleocene markers. In East Indonesia, the Daram Formation, dated on planktonic foraminifera as Middle to Later Paleocene Zone P3-4 with Morozovella angulata and M. velascoensis and others (Gold et al., 2017), also contained Discocyclina. This confirms the ranges assigned to these units and fossils in Visser and Hermes (1962), and Wilson (2002) who also reported Discocyclina in this formation. Again, this is evidence for rapid migration of larger foraminifera across the entire Mediterranean and Indo-Pacific Ocean.

6. THE STRATIGRAPHIC RECORD

The following is an account of the main lineages of larger foraminifera in SE Asia, discussed in the framework of the Letter Stages that they define. The ranges of the genera are summarized in Fig. 6.

Figure  6.  Stratigraphic summary of the main lineages of larger foraminifera in SE Asia. Highly peramorphic lineages are highlighted in red.

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6.1 Ta Faunas

The Letter Stage Ta ("Tertiary a") is a disproportionately large unit consisting of the Paleocene through Middle Eocene, i.e., some twenty million years. It is included in a single stage because sediments of this age are very rare in SE Asia. Shallow marine, transgressive sediments began to be deposited around the eastern flank of Sundaland at about 45 Ma, initially as non-marine and becoming marine with carbonates in the latest Lutetian or Bartonian. The stratigraphic record of SE Asia therefore covers the acme in diversity of Nummulites mentioned above. The record in east Indonesia and Papua will eventually give a more complete account of the Paleocene and earlier Eocene but outcrops there are remote. In addition well-sections suffer from no circulation of drill-cuttings samples in the thick and porous New Guinea Limestone (Visser and Hermes, 1962). Rare records of older Eocene carbonates on the flank of Sundaland such as the supposed Ypresian to early Lutetian of the Toraja Group (in the Ranteballa area, White et al., 2017) are from a remote site visited by one of the present authors in 2012 (120.110630°E, 3.358650°S, c. 800 m from White's samples at 120.10997°E, 3.350830°S) and after new analyses as well as a review of White's microphotographs, we can confirm these small outcrops are later Ta (Ta3 on Fig. 6), with common Nummulites javanus and Nummulites bagelensis.

6.2 The Ta to Tb Boundary

This boundary is defined on the mass extinction of numerous nummulitid taxa, as well as Planocammerinoides/Assilina and Alveolina and the rare genera Linderina and Orbitolites. It is not based on the evolutionary appearance of Pellatispira (contra Adams, 1970) as there are many records of this genus with the Ta3 assemblages, prior to the major extinction (Leupold and van der Vlerk, 1931; van der Vlerk and Umbgrove, 1927).

Lunt and Allan (2004) noted multiple wells and outcrops around Java and SW Sulawesi with Zone E13 planktonic foraminifera in samples with Ta3 larger foraminifera, and Zone E14 planktonics with Tb larger foraminifera. Unfortunately the record is complicated by a regional unconformity reflecting sudden subsidence, which usually terminated the larger foraminifera bearing facies. This unconformity is dated shortly before the end of zone E13 in wells such as Tanakeke-1 and Kelara-1, which have granulate and large embront bearing species N. djokdjakartae immediately below the event and a very short section above it with E13 foraminifera such as Morozovella.

Onshore West Sulawesi, about 100 km from these wells, there was less severe subsidence, where the effect of the associated transgression was to initiate a new carbonate facies. Here Crotty and Englehart (1993) found Ta3 fossils including the large N. javanus as minor components in the siliciclastic and coal- bearing Malawa Formation sediments below the siliciclastic- starved Tonasa limestone. Crotty and Englehart mis-assigned these samples to Letter Stage Tb as there were also a few Pellatispira forms. One of the present authors revisited the Tonasa I quarry location (located 4.845683°S, 119.884883°E) and confirmed rare N. javanus and small granulate Nummulites in thin calcareous sands close of the top of the Malawa Formation. The lower part of the overlying Tonasa Limestone contained Tb foraminifera.

In North Sarawak, the Melinau Gorge and Batu Gading sections record a transgression of Eocene limestone over meta-sedimentary basement that began shortly before the extinction of Ta larger foraminifera. In parts of the Batu Gading area and only in the very basal part of the Melinau Gorge Section up to 15 m of limestone contain Ta markers N. javanus and N. bagelensis, overlain by about 450 m of Letter Stage Tb (Adams, 1965; Adams and Haak, 1962). In the Engkabang-1 well (70 km west of the Melinau Gorge) about 250 m of deep marine limestone overlies an unconformity, of which the lowest 50 m contains G. semiinvoluta (restricted to Zone E14, early Late Eocene).

These Sulawesi and Sarawak locations suggest that the regional tectonic event was very slightly before the end Ta and E14 extinctions.

6.3 Letter Stage Tb

After the mass-extinction of many forms at the end of Ta, the Tb letter stage records a rapid diversification of the Operculina and Pellatispira lineages. Large flat Operculina present in Ta became slightly involute and developed secondary septa as Heterostegina (Vlerkina). These then developed lateral chamberlets of Tansinhokella (see Banner and Hodgkinson, 1991). At higher, subtropical, latitudes, the heterostegine-like Grzybowskia is recorded (Lunt, 2003).

The evolution of the pellatispines saw a rapid development of the adult or gerontic stage and the separation of the Biplanispira lineage. The work of Hottinger et al. (2001) details the complex morphology and canal systems of these forms, but this new taxonomy has not been applied to most East Tethyan records, which are still largely based on gross morphology. Within E14 times (from material dated with Globigerinatheka semiinvoluta from Sangiran, Gamping Barat and Nanggulan in Central Java; Lunt, 2013) forms had arisen with the spiral stage reduced to a single whorl and the bulk of the test being composed of small chamberlets or cubiculae derived from an evolutionary exaggeration of the late adult stage of the ancestral form. This form is called Vacuolispira. However, a single field sample from Halmahera Island in East Indonesia was illustrated in Lunt and Allan (2004) and contains Pellatispira inflata which would become the type species for Vacuolispira, but this sample contains Letter Stage Ta taxa Planocamerinoides and Alveolina. The radiation of pellatispirines occurred very rapidly in the early part of Tb, with Biplanispira being found in latest E14 through to E16 (Lunt, 2013) and the very large Vacuolispira specimens with a greatly reduced juvenile whorl and emphasized gerontic stage by mid Tb times (Gamping Barat, Central Java)

On the Australian Plate, which was much further south in Eocene times, the Pellatispirines are unknown and Tb is often characterized by the species Lacazinella wichmani, which appears to be restricted to the Australian Plate (Lunt, 2003). Forms that were present in Ta but became more common in Tb include Amphistegina and Asterocyclina.

Two subsidence related unconformities, at about 36 and 34 Ma affects stratigraphic records for the latest Tb across SE Asia, especially the eastern side of Sundaland (Lunt and Woodroof, 2021). In many eastern locations, there was a two million year gap in the stratigraphic record of shallow carbonate facies. The only known un-broken carbonate section over the Eocene-Oligocene boundary is in the Melinau Gorge Section of North Sarawak (with the associated isotopic shift observed by Cotton et al., 2014), and it is only in the latest Tb samples that the mildly peramorphic form Wilfordia sarawakensis is found (Adams, 1965), indicating it must have had a very short stratigraphic range.

6.4 The Tb to Tc Boundary and Letter Stage Tc

This boundary is a major extinction in foraminifera well-covered in literature from around SE Asia and apparently coinciding with the end E16 planktonic zone and NP20 nannofossil zone. This extinctions in mixed planktonic and larger foraminifera assemblages in East Africa (Cotton and Pearson, 2011). ODP/IODP data differentiates slightly different times for the extinction of Turborotalia species (33.8 Ma), Hantkenina (33.7 Ma, and the reference datum for the top Eocene) and Discoaster saipanesis and D. barbadiensis (34.44 and 34.76 Ma, respectively). This degree of stratigraphic resolution has not been achieved for the larger foraminifera extinction event. There is no reliable evidence for more than a single larger foraminifera extinction datum, and also no high resolution dating capable of suggesting which of the planktonic extinction events it correlates to.

It is only from about the base of Letter Stage Tc that the strontium isotope sea-water reference curve begins to have a positive gradient that allows age determination. Carbonate faunas from Tc are characterized by Nummulites fichteli-intermedius with their distinctive reticulate septal traces and strong dimorphism. This reticulate septal pattern can usually be considered diagnostic of post-Eocene Nummulites. A small and partly reticulate Tb ancestor, Palaeonummulites fabianii, is known in the Middle East and Mediterranean (Racey, 1994), but so far there are no records of this form in SE Asia, which could be due in part to the absence of latest Tb carbonates in most SE Asian sites.

Forms appearing early in Tc include large species of Planostegina (P. bantamensis and praecursor). Within Letter Stage Tc, the descendant Cycloclypeus appeared by the acquisition of annular chambers after an extended Planostegina juvenile stage. Recording the evolution of Cycloclypeus from Planostegina is imprecise because the tests contained up to 30 heterostegine chambers before the first annular (cycloclypid) chamber appeared, and therefore fragmented tests, or random thin sections of hard limestone cannot reliably display the last gerontic growth stage that would indicate Cycloclypeus. The Cimanggu and Ciapus sections of West Java studied by Tan (1932) and Lunt (2013) are important because specimens can be processed out of calcareous claystones, and here the evolutionary datum for Cycloclypeus can be determined as being within Tc, Zone O1.

The genus Borelis also appeared very soon after the end Tb extinction. Some range charts suggest this genus occurs in Tb, but this is based on a single specimen in a single sample of Cole (1957b). Moreover, large numbers of Tb samples, including the densely sampled Melinau Section, lack any Borelis before base Tc.

6.5 The Tc to Td Boundary

This is a migration event discussed above and dated at about 32 Ma. The field sections of Ciapus and Cimanggu of West Java, where debris beds of diverse bioclastic material are found in a siliciclastic/volcaniclastic section, shows the simultaneous first appearance of Eulepidina, Lepidocyclina and Neorotalia mecatepacensis. The highest sample without these genera gave an strontium age of ⁸⁷Sr/⁸⁶Sr = 0.707 897 (±0.001 1% equip. precision) = 32.1 ± 31.64 to 32.53 Ma. This first appearance in the region is between the extinction datums of Globigerina amplipertura and Pseudohastigerina species at between 30.3 and 32.0 Ma (Wade et al., 2011), and just below the extinction of Discoaster tanii nodifer (c. 31.5 Ma; a poor quality datum in the lower part of NP23; Perch-Nielsen, 1985).

6.6 The Td to Te Boundary

This boundary is defined on the extinction of the single genus Nummulites sensu stricto, which is not a clear event since the genus declined in abundance within Td. Lunt and Renema (2014) reviewed numerous sections from Java with planktonic and strontium isotopic dating. In the Tuban Plateau near the Kujung-1 well (Lunt, 2013), the highest consistent Nummulites is found slightly below the extinction datum of Chiloguembelina cubensis (28.4 Ma). Strontium dating of the youngest Nummulites bearing samples was 29.17 Ma (28.71 to 29.62 Ma; ⁸⁷Sr/⁸⁶Sr = 0.708 000 ± 0.001 8 NBS 0.710 235) and from the Central Java Pelang Beds 28.19 Ma (27.76 to 28.57 Ma; ⁸⁷Sr/⁸⁶Sr = 0.708 040 ± 0.001 6 NBS 0.710 235) and the oldest sample with a rich larger foraminifera assemblage but lacking Nummulites was dated at 29.1 Ma (28.79 to 29.39 Ma; ⁸⁷Sr/⁸⁶Sr = 0.707 908 ± 0.001 2 NBS 0.710 140; all data from Lunt and Renema, 2014).

This date of 28.5 to 29 Ma applies to a major reduction in Nummulites, but it may not be its final extinction. Lunt and Renema (2014) found rare, individual specimens of Nummulites (that were too large to be considered ancestral Palaeonummnulites, which survived the extinction of Nummulites s.s.) slightly above the extinction of C. cubensis. Hashimoto et al. (1977) studying the Bugton Limestone of East Mindoro in the Philippines illustrated a single Nummulites associated with Tansinhokella (Te2-3) in a loose boulder of limestone. Although their photograph of the specimen is clear and shows no difference in preservation between the two taxa that might suggest stratigraphic reworking.

6.7 Radiation within Lower Te

In the later part of Letter Stage Td Heterostegina (Vlerkina) had evolved from a Planostegina ancestor by becoming increasingly involute in the adult chambers, and this became a common component of larger foraminifera faunas in later Td and Lower Te. The base of Te2 was defined by the evolution of this form into Tansinhokella by acquisition of lateral chamberlets, which is well seen in the disaggregated specimens from the Tuban Plateau (Lunt and Renema, 2014; Muhar, 1957). The Te2 to Te3 boundary was originally proposed at the last occurrence of Lepidocyclina isolepidinoides by Leupold and van der Vlerk (1931) but this was abandoned as this taxon has also been found higher in the section (Fig. 2). As noted above, there is not a precise stratigraphic level at which this biometric values changes, as there can be about 5% variance in average factor A in populations at any time (Fig. 3). Since then the Te2-3 substage has been left undivided.

The radiation of larger foraminifera continued with Neorotalia mecatepacensis acquiring a small fan of chamberlets that had bi-directional stolons and coiling directions to create a new gerontic form named Miogypsinoides. The evolution of Miogypsinoides defines the base of Te4. Other names such as Paleomiogypsina and Miogypsinella are considered synonyms for the early Miogypsinoides primitiva. Within Te4, true Spiroclypeus with cubiculae appeared as a gerontic stage to the ancestral Tansinhokella, then rapidly the lateral chambers of the Tansinhokella form were completely replaced by the cubiculae of Spiroclypeus, in which no remnant whorls of growth can be discerned. This anagenic development of the Heterostegina to Spiroclypeus and the miogypsinid lineages during Lower Te has given rise to a large number of generic names based on peramorphic development of gerontic features rather than the radiation of new lineages.

In the Mediterranean region, a parallel style of evolution of the same lineages is seen. The evolution of Miogypsinoides in the west is also within O6-7 (Abdulsamad et al., 2009), or in older reports, at the base of SBZ 23 where it is correlated to middle Chattian times (Serra-Kiel et al., 2016; Cahuzac and Poignant, 1997), although the precision of these observation is not fully explained. No Mediterranean studies have yet considered the iterative evolution of Tansinhokella/Spiroclypeus, and so the intra-Oligocene evolution of these genera would be worth investigating and comparing with the SE Asian record.

Within the Lower Te of SE Asia (probably within Te1), the original Cycloclypeus lineages with large proloculus (about 180 μm, called C. koolhoveni) changed to forms with a small proloculus (80–90 μm), called C. eidae (Tan, 1932). As explained above, there was apparently no change to the steady reduction in the planostegine juvenile stage which was about 28 to 22 chambers in Td and 21 to 17 chambers in Lower Te. The small proloculus of C. eidae would gradually increase in size as the juvenile stage further decreased in numbers of chambers through the Miocene (Renema, 2015).

6.8 Lower to Upper Te Boundary

This boundary is defined by the acquisition of lateral chamberlets in Miogypsinoides to define the new genus of Miogypsina. This has long been recognized as an important datum in SE Asia. Note that in old reports, the generic assignment was "Miogypsina (without lateral chambers)" and "Miogypsina (with lateral chambers)". In these cases, it might falsely appear in summary charts that Miogypsina ranges older that Te5. The genus Miogypsinoides was defined by Yabe and Hanzawa in 1928 (type Miogypsina dehaartii van der Vlerk 1924).

As noted above and summarized in van Gorsel et al. (2014), this datum is found in SE Asia in the same samples around the Globigerinoides datum and base Paragloborotalia kugleri, or top of nannofossil Zone NP25, all of which are proxies for the Oligo-Miocene boundary.

Serra-Kiel et al. (1998) and Cahuzac and Poignant (1997) placed the base of their SB Zone 24 in Europe at the evolution datum of Miogypsina. The rare instances of M. septentrionalis in the top of SBZ 24 are probably equivalent to the transitional form with just a very few lateral chamberlets called M. primitiva in East Tethys. The base of SBZ 24 is correlated to the O7 to M1, near Chattian to Aquitanian boundary, which is supported by the observation noted above of the lowest occurrence of Miogypsina with the top of NP25 in the Terra Limestone in Cyprus.

6.9 Top Te Boundary

This boundary is marked by the extinction of Tansinhokella and Spiroclypeus (both lumped into Spiroclypeus by some) and the genus Eulepidina. Around Sundaland, the tectonically induced subsidence and transgression during Upper Te led to widespread reefal growth (Lunt and Woodroof, 2021), and the Spiroclypeus/Eulepidina assemblages appear to decrease in number compared to the abundance of other larger foraminifera (e.g., Saw et al., 2019). With its large, flat form, Eulepidina was typically a reef-edge, deep photic specialist. Spiroclypeus was more widespread as it had more diverse ecophenotypic forms, but it was usually only a minor part of larger foraminifera assemblages. In both SE Asia and the Mediterranean, these genera are uncommon in Upper Te samples. There may be sampling bias as across Asia there are few outcrops of this age and wells primarily drill reef crests that would be devoid of Eulepidina. The likelihood of the taxa being recorded is also proportional to the size of the samples available. This is why the Rebab-1 core samples from offshore Sarawak (Lunt, 2021a) are important in dating the Te-Tf boundary (using multiple Sr isotope dates). In this well, almost ten meters of cut core-face was examined and many tens of large format thin sections were used to ascertain that by an age of 19.0 Ma (⁸⁷Sr/⁸⁶Sr = 0.708 496 (±0.001 4%), NBS987 ⁸⁷Sr/⁸⁶Sr = 0.710 235) these genera were absent from a basal Tf fauna, older than the appearance of Lepidosemicyclina (see below). Lunt (2021a) notes several sites where Te faunas with Spiroclypeus and/or Eulepidina had been dated to as young as 20.5 Ma by Sr data, matching adjacent planktonic biostratigraphy for Zones M2/NN2.

As noted above, in the Mediterranean, workers rarely report Eulepidina and Spiroclypeus above the evolution of Miogypsina (e.g., Cahuzac and Poignant, 1997), although the three genera were noted to be concurrent in the Terra Limestone of Cyprus (Lunt, 1984) and in SW Turkey into SBZ 25 (Özcan et al., 2009), although not present in every sample. The end of Letter Stage Te was about the time of separation of the Mediterranean and from the Indo-Pacific realm and subsequent differentiation of faunas in each realm (Adams, 1983). It was also the time of rapid uplift in Central Borneo, introducing clastic sediments after a four million year clastic-starved period, ending carbonates over south, northeast and northwest Borneo (Batu Raja, Kujung, Taballar, Gomantong and Subis limestones; Lunt and Woodroof, 2021). The closure of the Arabian seaway is probably coincidental, occurring as part of a prolonged tectonic compression, and is unlikely to be related to the local plate movements that uplifted Central Borneo. The closure of the Arabian seaway allowed Borelis to continue in the Mediterranean, but in SE Asia it is thought to have anagenically evolved into Flosculinella through acquisition of small attics to the chambers.

The type location of Flosculinella riecheli is in Te5 beds in SE Borneo (Mohler, 1950), but it is extremely rare in the extensive Te5 Kujung and Batu Raja limestones drilled and cored by large numbers of wells across the adjacent Java Sea. Even the descendant F. globulosa (type location in the Jonggranan Limestone of Lower Tf age Lunt, 2013; similar to F. reicheli but slightly larger and with an elongate axial dimension) is uncommon until later Early Miocene. Flosculinella did not manage to migrate to the Mediterranean before closure of the Arabian seaway. This contrasts with notes below on bispiral Miogypsina, a common part of larger foraminifera assemblages throughout the Early Miocene, that appeared in both Mediterranean and Asia areas in earliest Lower Tf times.

6.10 Radiation in Lower Tf

The Letter Stage Lower Tf saw gradual radiation of many new forms. The increased number of proposed generic names during this period is a better reflection of morphological diversity than the synonym-rich Lower Te, which included multiple generic and species names applied to anagenically evolving lineages. However, there is some intra-lineage taxonomic redundancy in Lower Tf names, such as Miogypsinodella, which is a microspheric generation of Miogypsina with a unusual structure of widely spaced cubiculae.

There was an intra-lineage acquisition of a novel character in Miogypsina that did not merit a new generic name. This involved the nepionic reduction of the juvenile whorl so far as to allow a second smaller spiral to appear on the opposite side of the embryont as part of a shift to increased radial symmetry. These are known as bispiral forms (Fig. 2) and appeared in species called M. cushmani or globulina (cf. Lunt and Allan, 2004; Amato and Drooger, 1969 their Fig. 10 where biometric factor gamma reaches +45°). This appears to have occurred very early in Lower Tf, possibly in Zone M2 in SE Asia and at the same time in the Mediterraenan (Cahuzac and Poignant, 1997) where it was used to define the base of SBZ 25. This was the last biostratigraphic event that can be correlated between the two areas, prior to the closure of the Arabian seaway.

True radiation in the miogypsinid lineage occurred at about the same time or shortly afterwards and is seen in SE Asia, but not the Mediterranean. This included the appearance of the bispiral Lepidosemicyclina lineage, which are found in lowest Tf samples across SE Asia, in Zone M3 samples and younger from Sundaland to Saipan and Eniwetok cores in the West Pacific (Cole, 1957a, b), as well as West India (Singh and Raju, 2018) and also northern Australia (Chaproniere, 1984, 1975). There are several available species names for this genus, of which Lepidosemicyclina thecidaeformis is the main form ranging almost all of Tf1 and Tf2, while the form L. polymorpha (possibly synonymous with L. excentrica) has a greatly enlarged embryont and distinctly hexagonal chamberlets. Chaproniere (1981) records both these species with M5 and M6 faunas in NW Australia. Van Vessem (1978) found them in samples as old as M4-5 in South Borneo, and he and other workers reported them from carbonate interbeds in the Ngrayong Formation from M6 to M8-9 in NE Java. Renema et al. (2015) found L. polymorpha in samples from East Kalimantan as young as the upper part of Lower Tf (upper Tf2), c. 11.6 to 13 Ma based on strontium dating in adjacent field sections.

The genus Lepidosemicyclina has only unreliable records from the Mediterranean area and studies such as Özcan and Less (2009) and Özcan et al. (2009) specifically note that this genus is not recorded in many samples of the appropriate mid Early Miocene age. However the form Miolepidocyclina is found (a miogypsinid not known in SE Asia; with the nepiont placed centrally, not close to the test periphery). This differentiation in the Miogypsinids is further evidence for the closure of the Arabian seaway near the end of Letter Stage Te.

In the lepidocyclinid lineage, there were at least two candidates for cladogenic radiation plus an intra-lineage peramorphic development. This latter feature was the appearance of highly dimorphic types with giant B or microspheric generations that sporadically occur from latest Early Miocene Miocene to the top of Lower Tf. These are several centimetres in diameter and are usually given the name Lepidocyclina glabra. Slightly older than this in about early Lower Tf there are macrospheric forms with robust columns or ridges, especially away from the central embryont, which in axial thin section produce a profile and nickname of "peanut" lepidocyclines. There may be four of five such columns of ridges and these are usually placed in Lepidocyclina ferreroi, although the name L. crucifera is also used for forms with a cross of thickened ornament on the exterior surface of the test. Other coeval forms had thickened and extended equatorial chambers in rays projecting as pseudospines, sometimes with delicate spines protruding (rarely preserved). These were referred to as Lepidocyclina martini. Where data is available, these forms have the same embronic stage (factor A) as other specimens of Lepidocyclina. This diversity of morphological types in mid and late Lower Tf sediments is absent in older Te or Td lepidocyclinid populations.

Variation in embryonic structure is strongly seen from near the base of Lower Tf, in a form with an increasingly irregular embryonic apparatus. The older specimens are known as L. (N). transiens, and it appears that these were ancestral to the more extreme form L. (Multilepidina), having multiple embryonic chambers, which survived until the end of Lower Tf (Fig. 2).

After the closure of the Arabian seaway the genus Cycloclypeus disappeared from the Mediterranean area (Renema, 2015). In the SE Asian cycloclypids the distinct form with annular banding is either called C. annulatus or separated into Katacycloclypeus annulatus. The review of Adams and Frame (1979) and Renema (2015) suggests while some specimens have up to 5 nepionic chambers there is also reduction to just two nepionic chamber and even a radial form lacking any distinct juvenile (illustrated by Adams and Frame) and hence a separate generic name is arguably valid. Note that Adams and Frame (1979) claim a "N13/14 probably N14" age (=M10–M11) for their records of K. annulatus in the Futuna Limestone of Fiji. The planktonic fauna listed indicates an age between the evolution datum of Globorotalia menardii and extinction of Globorotalia siakensis/mayeri and also Globigerinoides subquadratus, which indicates a Middle Miocene age no younger than M10. The absence of Orbulina and Sphaeoroidinellopsis types suggests an incomplete faunal record and so the absence of Fohsella species cannot be used as evidence of a post M9 age.

The complex milolid forms continued evolving by anagenesis in SE Asia. As noted above, from about the base of Lower Tf boundary, the genus Borelis evolved into Flosculinella, initially small globose forms (F. reicheli, F. globulosa) but gradually becoming spindle-shaped and elongate (F. bontangensis). This then developed gradually into Alveolinella fennemai or praequoyi near the top of Lower Tf by the appearance of additional rows of attic chamberlets near the axial ends. These additional attics were progressively developed in more equatorial areas to define the species Alveolinella quoyi, which is extant. It is therefore probably only a coincidence that F. bontangensis appears to have become extinct close to the top Lower Tf mass extinction.

This Lower Tf radiation of larger foraminifera was during the peak transgression onto Sundaland, which occurred until about M5 times, after which uplift in Central Borneo (post the "N8 inversion"; Moss and Chambers, 1999) led to the regressive progradition of the major Mahakam Delta and similar clastics towards Southeast and South Sundaland (Ngrayong and Main Sands). However, the Luconia Province offshore Sarawak and the equivalent Terumbu Platform east of Natuna underwent accelerated subsidence at this time and became important areas of carbonate deposition (Lunt, 2021b). Local variation in relative sea-level curves and associated shifts in carbonate deposition like this may be one reason why there is no correlation between global sea-level and the evolution of larger foraminifera.

Adams (1984) followed earlier workers in trying to subdivide Tf into parts. He proposed Tf1 and Tf2 with a boundary separating them at the highest occurrence of Miogypsinoides, Austrotrillina and Lepidosemicyclina. However Austrotrillina has been found younger than this into early Middle Miocene of Papua (Allan et al., 2000) also in Sarawak (Lunt, 2021a, b). Data is given above on Lepidosemicyclina as young as mid Middle Miocene. The extinction of Miogypsinoides may have been at about this time, but in the later Lower Tf, the genus is so rarely found, so we can not be sure of the precise age of this extinction.

6.11 Lower to Upper Tf Boundary

This boundary has been the source of confusion, even though in outcrops around Sundaland, the extinction of many lineages of larger foraminifera at the end of Lower Tf has long been noted as a major paleontological event. The original definition of the Letter Stages (e.g., Leupold and van der Vlerk, 1931) used this mass extinction of larger foraminifera to define the top of Letter Stage Tf, and this was tied to the traditional Epoch scheme based on the percentage of extant molluscs (Morley Davies et al., 1971; Lyell, 1833), which, prior to any planktonic biostratigraphy, had been used to date Cenozoic sediments in SE Asia. However, the detailed review of Adams (1970) adjusted the defining feature for top Tf to be the extinction datum of rare Lepidocyclina. As a result, top Letter Stage Tf was extended to near top Miocene, and the extinction of the other lineages was used to subdivide Adams' Letter Stage Tf2 to Tf3. The influence of the Adams paper has been so widespread that this misinterpretation is now overlooked, and acceptance of the revised definition is established.

The age of this event is best seen in the continuous cores from the E11 and F13 fields in Luconia offshore Sarawak (Lunt, 2021b). In this area, a regional unconformity changes the style of carbonate deposition but the carbonate sedimentary record is unbroken and well-sampled. It is cored multiple times in the E11 field wells, and in E11-2 the extinction event is just below a thin 5 m marly limestone with Cycloclypeus (not annulatus) and traces of planktonic foraminifera marking the transgression that drowned the adjacent F13 reef. The first clean limestone in E11 above this transgressive event (10 m above the larger foraminifera extinction event) had a strontium isotope age of 11.67 Ma (11–12.4 Ma, ⁸⁷Sr/⁸⁶Sr = 0.708 830, NBS987 = 0.710 235). In the adjacent very low relief F13 field, the limestone has Lower Tf foraminifera to the top of the reef, above which the first sample of clays contained Fohsella fohsi in one sample only (Lapre and Thornton, 1970; extinct at 11.71 Ma).

In East Java, the same regional transgressive event terminated the Platen Limestone. Marls to near the top of this limestone contain Fohsella fohsi and a strontium isotopic age from near the top of this limestone was 11.45 Ma (10.59 to 12.63 Ma, ⁸⁷Sr/⁸⁶Sr = 0.708 738 ± 0.000 016; NBS987 = 0.710 140; Lunt, 2013). Marls rich in planktonic foraminifera above the Platen Limestone contain M10 Globigerinoides subquadratus and Globorotalia mayeri, but only traces of transported Operculina, Amphistegina and fragmented cycloclypids (not K. annulautus types). Considering the potential error and imprecision demonstrated in Sr dating (Zeiza et al., 2012; Vahrenkamp, 1996), the location of the Tf extinction before the 11.71 Ma extinction of the Fohsella lineage is considered a primary datum, and this is within the error range of the Sr data, but the true age of the end of Lower Tf could be slightly older.

The end Lower Tf extinction event differs from the c. 39 and 34 Ma Eocene mass extinctions as in the former event, while larger foraminifera were greatly affected, planktonic foraminifera or other organisms were not. The Fohsella lineage, a minor part of the diverse planktonic foraminiferal faunas became extinct slightly after the end Lower Tf extinction and seems to be unconnected.

6.12 Radiation of New Larger Foraminifera since Tf

Multiple cores and many hundreds of thin sections from the Upper Tf carbonates in Luconia offshore Sarawak and the Kais Limestone of the Salawati Basin in West Papua have been examined by one of the authors and the faunas are extremely poor in highly peramorphic larger foraminifera. Amphistegina, Palaeonummulites and operculinid forms can be common, and Cycloclypeus is present in deeper photic facies, but Lepidocyclina is only very occasionally found. The small outcrop of Lawak Beds of Java studied by Tan (1932) was re-visited by Lunt (2013), and is described in Lunt and Allan (2004, Image 24). This is a rare facies with frequent specimens of the trybliolepidine form Lepidocyclina rutten, dated on nannofossils to be from the lower part of Zone NN11.

This paucity of larger foraminifera is also reflected in the fact that the Letter Stages (based on larger foraminifera to replace percentages of extant molluscs) were very poorly defined above the top of Lower Tf. The summaries of Leupold and van der Vlerk (1931) and Rutten (in van Bemmelen, 1949) continued to use the percentage of extant molluscs for Tf, Tg and Th (Tg having 35%–45% and Th 50%–60% extant molluscs; Latest Miocene through Pliocene; see review in Lunt, 2013). The Tg to Th boundary was not defined on any larger foraminiferal change, but on the onset of 50% extant molluscs. However in some facies, mildly peramorphic larger foraminifera appear at about this time, and it could be argued that there was a Latest Miocene through Pliocene foraminiferal radiation.

The distinct form Calcarina spengleri, a morphologically robust benthic rotaliid, is common in calcareous lithofacies from the Latest Miocene to recent. Five other types also appeared at about the same time, or shortly afterwards. Across Java, a series of thin limestones appeared in Latest Miocene to basal Pliocene times above a regional unconformity (Lunt, 2013). These contain locally abundant Quasirotalia and a few Alanlordia (Lunt and Allan, 2004, their Image 26). The latter genus was also found in limestone in the islands off Sumatra (type location; Banner and Samuel, 1995). During the Pleistocene, the genus Baculogypsina appeared as a form similar to Calcarina but with a greatly reduced juvenile trochosipre and becoming larger and with 5 to 7 stronger spines. The genus Baculogypsinoides appeared shortly after and also has a small, trochospiral juvenile Baculogyspina stage, but the adult has four or five spines arranged in a tetrahedron with a mass of cubiculae around the reduced juvenile. Both these forms are only about 2 mm in diameter.

The genus Schlumbergerella is considered a Pleistocene to recent form and shares the same sub-spherical form of a mass of cubiculae as Baculogypsinoides. There is a small embryont and no obvious juvenile stage, and instead of extruding spines it has a surface covered in robust pillars. It is typically 2–3 mm in diameter. Baculogypsinoides, Baculogypsina and Schlumbergerella can be abundant as modern beach sands in reefal areas. In some areas dominated by Schlumbergerella (Bali, Lombok islands) or in others by Baculogypsina (Saipan, Guam; Cole, 1963, 1957; see Fig. 1b), where they can be mixed with Sorites, Amphistegina and other foraminifera. The nearby reefal areas however are dominated by an aragonitic fauna.

The genus Heterocyclina (Hottinger, 1977) recorded from the recent sediments in Gulf of Eilat has not been recorded yet in SE Asia (Hohenegger, 2000). This genus is a homeomorph of Cycloclypeus probably descended from Heterostegina operculinoides and with a very much longer juvenile heterosteginid phase and much smaller embryont than Cycloclypeus carpenteri, as well as a different arrangement of inter-cameral stolons.

7. DISCUSSION

7.1 Taxonomic Confusion and the Species Question

The lineages of larger foraminifera in SE Asia are complicated by an abundance of species and genus names. The overlapping and partially ecophenotypic species names have been held in low regard by working biostratigraphers as most species have no stratigraphic application, and generic names seem to reflect a more reliable evolutionary series. For example, the lineage of Heterostegina (Vlerkina) to Tansinhokella and then Spiroclypeus is a simple peramorphic transition covering about five million years, but which could be re-defined as a single genus with three species. However since Banner and Hodgkinson (1991) it has been a habit to elevate the reliable defining features to generic level, to emphasize the confidence in the evolutionary history and their biostratigraphic application. In contrast, the five species of Spiroclypeus (including Tansinhokella) suggested by Krijnen (1931) and based on simple morphology have almost no biostratigraphic value.

However, even generic names have some ambiguity in the way they have been applied, usually historical changes between genera and subgenera (e.g., Lepidocyclina (Eulepidina) or Eulepidina; "Miogypsina without lateral chamberlets" or Miogypsinoides etc.). In spite of this confusing history, the lineages of larger foraminifera are mostly distinct as they are dominated by gradual peramorphic evolutionary series. Biometric analysis of embryonic or nepionic to juvenile stages can be reliably used to correlate strata, and these have been proposed as the basis of some species names. However, this does not fit well with the rules of the ICZN which assumes that distinct forms arise through cladogenesis, and there is no need or validity to define species by arbitrary boundaries that arise through anagenesis.

Some workers assume that there are many more species in nature than in the fossil record, and this seems to have encouraged splitting rather than lumping. However, if the biometric series of age-controlled Oligo-Miocene forms are compared across the Mediterranean and Indo-Pacific realms (Cycloclypeus, Lepidocyclina and Miogypsinids), combined with the dating of the appearance of key novel characters such as the lateral chambers that define Miogypsina, the appearance of bispiral coiling in Miogypsina, or the appearance of small proloculus C. eidae forms, then these all seem to occur across the entire ocean at the same time. This suggests a single genetic identity for each lineage, gradually evolving as one population. Rapid migration of forms across the Mediterranean to SE Asia seems to have been demonstrated by the influx of Central American Eulepidina, Lepidocyclina and Neorotalia mecatepacensis types apparently simultaneously at about 32 Ma (based on Sr dating and a position within Zone O2). In contrast, the biometric development of Miogypsinoides and its descendent Miogypsina, from India to Papua, was very different after branching apart at the base of the Miocene. A similar style of biometric divergence would be expected for genetic populations isolated by geography, since there would be no reason to expect the same rate of change.

7.2 Radiation and Extinctions

Most larger foraminifera lineages evolved gradually by anagenesis with only periodic radiation of novel branches (e.g., Lepidosemicyclina, Lepidocyclina (Multilepidina) and Cycloclypeus annulatus). The most notable events in this stratigraphic history are the mass extinctions. Three major and one lesser extinction stand out; the top of Letter Stage Ta, the top of Tb and the top of Lower Tf (the latter originally used to defined the top of Tf, but inadvertently changed by Adams, 1970). The top of Te saw the extinction of just two genera that had already faded in abundance in most carbonate facies. The top of Td is not a major extinction, it was the final demise of the super- genus Nummulites (but not the ancestral Palaeonummulites). It was the end of a form that had already undergone decline after earlier extinctions, and the migration of competing larger foraminifera from Central America at the start of Td.

The less peramorphic carbonate facies foraminifera appear to have been less affected by these mass extinction events. The Palaeonummulites and Operculina/Planoperculina types, and the ubiquitous Amphistegina were apparently unaffected, as was the long ranging, small Sphaerogypsina form. The selection pressure towards highly specialized adults seems to have made major rock-forming organisms like Nummulites and Lepidocyclina susceptible to periodic extinction. The question is what controlled these extinction events. There is a remarkable correlation to tectonic events around SE Asia. There are, depending on location, about half a dozen major unconformities around Sundaland (Lunt and Woodroof, 2021), and these correlate from sub-regional to regional level. All four larger foraminifera mass extinctions appear to coincide with four of the largest of these events.

Both the top Letter Stage Ta and Tb extinctions appear to be parts of global events. In planktonic foraminifera Wade (2004) noted the turnover in multiple genera of these global, shallow living oceanic forms at end zones E13 and E16. Even in American molluscs, two extinctions seem to correlate with the end Middle and end Late Eocene (Hassl and Hansen, 1996; Hansen, 1987). This has been attributed to stages in the prolonged growth in Antarctic ice sheet (e.g., Prothero, 1994) but even modern data (Westerhold et al., 2020; Wade, 2004) can find only minor isotopic excursions correlating with end Ta, E13, and the discussion of global causes is speculative. The nature of the end Middle Eocene tectonic event in SE Asia is described in Lunt and Woodroof (2021) and it may very slightly precede the end of Ta.

Clearly the terminal Eocene, end Tb, Grand Coupure event is part of a large scale global transition, correlated to formation of Antarctic ice sheets (Westerhold et al., 2020). The apparent occurrence of a tectonic event and subsidence of that age around Sundaland are therefore probably a coincidence. Even the phased opening of the South China Sea and Makassar Straits, which the SE Asian tectonism represents, is probably too small to have caused eustatic sea-level falls or shifts in global climate. It should also be noted that the largest of the sudden seaway-opening events of the South China Sea and Makassar Straits, at the Oligo-Miocene boundary (Lunt and Woodroof, 2021), had no effect on larger foraminifera in SE Asia.

Lunt (2021a) speculated that the larger foraminifera mass extinction at c. 12 Ma, at end Lower Tf, might have been associated with sub-regional climate change as the Indonesian throughflow between Pacific and Indian oceans became constricted. This was a weak argument mainly countering a previous mis- correlation of such throughflow constriction with a known climatic shift, based on palynology at the Oligo-Miocene boundary (seasonal to ever-wet conditions; Wilson, 2008; Morley, 2000). As Adams (1970) and Lunt pointed out, there is a paucity of continuous carbonate sections across this c. 12 Ma event, especially from outcrops outside SE Asia in which to look for geographic clues as to the cause of the larger foraminifera mass extinction. Such material may be present in cores from Bikini and Eniwetok Atolls (Cole, 1957, 1954), but Cole's studies were not stratigraphic reviews. However his range summary from Eniwetok (Cole, 1957, Table 1) shows a deeper Miocene section with multiple highly peramorphic larger foraminifera, and an upper thousand feet of core having only Cycloclypeus, Alveolinella and the less peramorphic taxa. There are also outcrops of larger foraminifera-bearing limestones from the latest Lower Tf and Upper Tf on Guam (the Alifan Limestone; Adams, 1970), New Britain and Fiji (Bromfield and Renema, 2011; Adams and Frame, 1979).

As part of the long term shift from calcitic to aragonitic oceans (Stanley and Hardie, 1998), the calcitic larger foraminifera were already in decline as a primary rock forming organisms. The peramorphic larger foraminifera had radiated in forms from roughly 19 to 12 Ma, but occupied a reduced niche associated with biohermal build-ups.

8. CONCLUSIONS

The first part of this review considers whether modern publications have a framing bias regarding long-established species concepts for larger foraminifera. If correct, the proposed new approach based on slow, gradual peramorphic development, with ranking of taxonomic parameters guided by their stratigraphic continuity, will greatly impact our views of evolution, and biostratigraphy of a historically important group of marine organisms. Multiple examples in this review, including the evolution of later Eocene Nummulites, the migration of forms across the combined Mediterranean to Indo-Pacific Ocean, and examples of iterative evolution, show the importance of utilising biostratigraphy and other forms of age dating to construct a record of morphotypes in the dimension of time. This dimension of data is either missing or very weakly applied in many previous evolutionary studies.

Using a well-dated series of sections across SE Asia the main lineages of larger foraminifera are examined from the later Eocene to recent times, in an almost continuous stratigraphic record. During an overall decline in importance as reef bioclasts, the larger foraminifera continued to develop through anagenesis, with a slow rate of cladogenesis, punctuated by a few mass extinctions. Rates of anagenic change due to orthoselection appear to have been the same across the Mediterranean to Indo-Pacific Ocean, and at least three distinct morphological events (evolution of Cycloclypeus eidae, of Miogypsina, and of biplanispiral Miogypsina forms) appear to have been simultaneous across the Mediterranean to Indo-Pacific Ocean. This suggests each larger foraminiferal lineage had low genetic diversity until the closure of the seaway between the Mediterranean and Indo-Pacific realms in mid Early Miocene times.

There is remarkable correlation between regional unconformities and extinction events. The first two regional unconformities are major and rapid transitions in the simultaneous development of both the South China Sea and the Makassar Straits; large break-up type tectonic events at c. 39 and 34 Ma. However the first two larger foraminifera extinctions, near the end of the Middle Eocene and the end of the Eocene, seem to be part of global climatic changes affecting multiple organisms around the world. The third, intra Early Miocene (c. 20 Ma) extinction is of just two genera that were already in decline and appears to be approximately coincidental with two unrelated compressive tectonic events. These are the separation of the Mediterranean and Indo-Pacific into separate realms by closure of the Arabian seaway, and the uplift in Central Borneo that terminated widespread carbonate deposition in SE Asia. The last extinction at c. 12 Ma (mid Middle Miocene), when the Indo-Pacific was a center of global carbonate productivity (Renema et al., 2008), might have had a regional tectonic cause as no abrupt climatic event is known at this time and global planktonic foraminifera survived while many SE Asian larger foraminifera lineages were terminated.

The larger foraminifera have applications in climatic, stratigraphic, geological and evolutionary studies and an excellent fossil record in SE Asia. After being a focus of study in the first half of the 20th century, they have been neglected, and are overdue for a new period of investigation.

LIST OF DEFINED LARGER FORAMINIFERAL TAXA

Alanlordia Banner and Samuel 1995. Type species Alanlordia banyakensis Banner and Samuel 1995

Alveolinella H. Douville 1907. Type species: Alveolina quoyi dʼOrbigny 1826 (as quoii, nom. imperf.)

Alveolinella fennemai Checchia-Rispoli 1909

Alveolinella praequoyi Wonders and Adams 1991

Baculogypsina Sacco 1893. Type species: Orbitolina concava Lamark var. sphaerulata Parker and Jones 1860

Baculogypsinoides Yabe & Hanzawa 1930. Type species: Baculogypsinoides spinosus Yabe & Hanzawa 1930

Borelis de Montfort 1808 = Nautilus melo Fichtel and Moll 1798. Type species: Borelis melonoides de Montfort 1808 = Nautilus melo Fichtel and Moll 1798

Cycloclypeus Carpenter 1856. Type species Cycloclypeus carpenteri Brady 1881

Cycloclypeus eidae Tan 1932

Cycloclypeus koolhoveni Tan 1932 (syn. C. oppenorthi Tan 1932)

Cycloclypeus (Katacycloclypeus) Tan 1932. Type species: Cycloclypeus annulatus Martin 1880

Discocyclina Güembel 1870. Type species: Orbitolites prattii Michelin 1846

Eulepidina H. Douville 1911. Type species: Orbitoides dilatata Michelotti 1861

Flosculinella Schubert 1910. Type species: Alveolinella bontangensis L. Rutten 1912

Flosculinella globulosa Rutten 1917

Flosculinella reicheli Mohler 1949

Heterostegina (Vlerkina) Eames, Clarke, Banner, Smout, and Blow 1968. Type species: Heterostegina borneensis van der Vlerk 1929

Lepidocyclina glabra Rutten 1922, B form

L. (Nephrolepidina) crucifera Mohler 1846

L. (Nephrolepidina) ferreroi Provale 1909

L. (Nephrolepidina) martini Schlumberger 1900

L. (Trybliolepidina) rutteni van der Vlerk 1924

L. (Trybliolepidina) transiens Umbgrove 1929

Lepidosemicyclina Rutten 1911. Type species Orbitoides (Lepidosemicyclina) thecidaeformis Rutten 1911

Lepidosemicyclina polymorpha Rutten 1911

Lepidosemicyclina excentrica (Tan 1937)

Miogypsina Sacco 1893. Type species: Nummulites globulina Michelotti 1841

Miogypsina primitiva Tan 1936, placed in Miogypsinodella by BouDagher-Fadel et al. (2000)

Miogypsina dehaartii van der Vlerk 1924

Miogypsinella Hanzawa 1940. Type species: Miogypsinella borodinensis Hanzawa 1940

Miogypsinodella BouDagher-Fadel et al. 2000, subjective junior synonym of Miogypsinella Hanzawa and of Miogypsina primitiva Tan

Miogypsinoides Yabe & Hanzawa 1928. Type species: Miogypsina dehaartii van der Vlerk 1924, Miogypsinoides Chapman 1932 nom. transl.

Miogypsinoides ubaghsi Tan 1936, placed in Miogypsinella by Hanzawa 1940

Miogypsinoides complanata Schlumberger 1900, placed in Miogypsinella by Hanzawa 1940

Neorotalia mecatepecensis (Nuttall 1932)

Nummulites Lamark 1801. Type species Camerina laevigata Bruguiere 1792

Nummulites bagelensis Verbeek 1891, A form, probably corresponding to N. javanus

Nummulites djokdjokartae Martin 1881, A form

Nummulites fichteli Michellotti 1841, A form

Nummulites intermedius d'Archaic 1846, B form

Nummulites javanus Verbeek 1891, B form

Palaeonummulites fabianii (Prever 1905)

Paleomiogypsina Matsumaru 1996, subjective junior synonym for Miogypsinoides ubaghsi Tan 1936

Pellatispira Boussac 1906. Type species: Pellatispira douvillei Boussac 1906 = Nummulites madaraszi Hantken 1876

Pellatispira inflata Umbgrove 1928, the type secies for Vacuolispira Tan 1936

Planostegina Banner & Hodgkinson 1991. Type species Heterostegina costata d'Orbigny 1839

Planostegina bantamensis and P. praecursor Tan 1932

Quasirotalia Hanzawa 1967. Type species: Quasirotalia guamensis Hanzawa 1967

Schlumbergerella Hanzawa 1952. Type species: Baculogypsina floresiana Schlumberger 1896

Sphaerogypsina Galloway 1933. Type species: Ceriopora globula Reuss 1848

Spiroclypeus H. Douville 1905. Type species Spiroclypeus orbitoideus H. Douville 1905

Spiroclypeus granulosus Boussac 1906

Tansinhokella Banner & Hodgkinson 1991. Type species Spiroclypeus yabei van der Vlerk 1925

Vacuolispira Tan 1936. Type species: Pellatispira inflata Umbgrove 1928