Chapter 1. Introduction—Cenozoic Order Discoasterales Hay 1944 emend. Aubry 2019

“Prins (1971) considered these to be descendants of the Early Cretaceous representatives of the genus Eprolithus Stover, 1966.”

(Hay, 1977, p. 1146.)

The fine fraction (<50 μm) Cenozoic sediments deposited between ~62 Ma and ~2.2 Ma is generally dominated by two groups of skeletal pieces occurring in about equal amounts, except at high latitudes. One group is comprised of placoliths — i.e., coccoliths with morphologies that are common in living coccolithophores such as Coccolithus pelagicus Wallich and Gephyrocapsa oceanica Kamptner. The other group consists of morphologically diverse corpuscles with an essentially radial structure and made of wedge-shaped elements in which each wedge is a single, strongly modified rhomb of calcite. Because these are without counterparts among the living coccolithophores, they were long placed with other enigmatic nannofossils in the arbitrary category of nannoliths (see Aubry, 2013). Only recently has it been determined that these corpuscles with radial symmetry are also coccoliths (Aubry et al., 2011). The Order Discoasterales was introduced by Hay (1977) for all these Cenozoic taxa, but in fact it incorporated unrelated genera, such as Braarudosphaera Deflandre since placed in the Order Braarudosphaerales Aubry 2013, and Ceratolithus Kamptner properly placed in Order incertae sedis. To remedy this situation, the order is emended here so that its Cenozoic lineages are restricted to those that developed from Biantholithus, a genus that appeared immediately after the Cretaceous/Paleogene (K/P) boundary, although possibly one of the included Paleocene genera may have arisen directly out of the same Late Cretaceous ancestry. The order itself is deeply rooted in the Mesozoic, with an origin that has been traced back to Early Cretaceous Eprolithus (Prins, 1971).

The first illustrations of coccoliths that would later be included in the Order Discoasterales were stellate asteroliths which Ehrenberg (1854) identified as “Crystalldrusen” and “Scheibensternchen” (Chapter 12, Note 1, figs. 1, 2). These tiny corpuscules, which he found in marine samples from around the world, were interpreted as having been directly precipitated from seawater. This was also the interpretation he gave (1836 (1838) to the elliptical “Kreide Morpholithe” that had previously been illustrated from chalk deposits. While the organic origin of the latter, which Huxley (in Dayman, 1858) named coccoliths, was rapidly established following the recovery of Atlantic deep sea deposits (Sorby, 1861; Wallich, 1861), the nature of the stellate specimens — which are absent from both the Cretaceous Chalk and Recent oceanic deposits — remained enigmatic.

Murray and Renard (1891, pl. 13, fig. 4) illustrated particles from the famous Challenger Site 338 that were similar to Ehrenberg’s Crystalldrusen (Chapter 12, Note 1, fig. 3). By contrast, Jukes-Brown and Harrison (1892) recognized their importance as components of the Eocene-Oligocene Oceanic Formation of Barbados, describing the rich foraminiferal fauna embedded in a “fine powdery matrix in which coccoliths and certain curious crystalloid bodies are often abundant” (op. cit., p. 171; emphasis mine). They quoted the expertise of Mr. W. Hills (“Fellow of the Geological Society”), who, citing the occurrence of similar forms in muds from western Java and in an Atlantic ooze, gave a thoughtful description of their morphology, birefringence and preservation, and concluded that they must be of organic origin (op. cit., p. 201; Chapter 12, Note 1, fig. 4).

Between this pioneering study and the first study exclusively focused on asteroliths (see below), they were occasionally discussed and/or illustrated in various ways (e.g., Murray and Renard, 1891, pl. 11, fig. 4, unnamed, only figured; Haupf, 1906, p. 565, “Kalkkörper” assigned to holoturians following Zittel’s suggestion [1876; Chapter 12, Note 1, fig. 5] and Schütt's determination [1895] of a Peridinian (dinoflagellates) of the genus Gymnaster), although their taxonomic affinity remained unsettled (e.g., Lemmermann, 1908; Gemeinhardt, 1930). Pliocene limestones from the Island of Rotti recovered during the Deutsch Timor Expedition (Indonesia) were made available for petrographic analysis to Tan Sin Hok who (1926), upon careful preparation of smear slides, reported a great abundance of “Disco-asters” in the limestones from Bebalin (Chapter 12, Note 1, fig. 6) but deferred their description for a later paper, in which he (1927) characterized members of the new group “discoaster” as consisting of single crystals of aragonite, which were optically isotropic when lying flat under the microscope — in other words, that the crystallographic c-axis was perpendicular to the plane of the discoaster structure. Considering the varying number of arms and their form, the concavo-convex shape of the specimens and the homogeneity of the single crystal, he not only concluded that discoasters are of organic origin, as Jukes-Brown and Harrison had concluded before him, but he then constructed a taxonomic framework of a new family with three genera and five species (Chapter 12, Note 1, fig. 7). Tan Sin Hok’s contribution resulted in abundant difficulties that will be discussed in appropriate chapters in this work. Nevertheless, the “Crystalldrusen”, “Scheibensternchen”, “Kalkkörper” and “crystalloid bodies” had now been united in as a single paleontologic group, Family Discoasteridae incertae sedis, and as counterparts of coccoliths. The term “discoaster” is still used in a vernacular manner, but “asterolith” (Sujkowski, 1931; Deflandre, 1952) is a preferred substitute.

Other, isolated reports of asteroliths in Cenozoic deposits followed (Sujkowski, 1931; Paréjas, 1934; Bersier, 1939; Colom, 1940; Colom and Gamundi, 1951, Deflandre, 1934; Chapter 12, Note 1, figs. 8–13). Ultimately, Bramlette’s rigorous work (Bramlette and Riedel, 1954; Bramlette and Sullivan, 1961; Martini and Bramlette, 1963, Bramlette and Martini, 1964; Bramlette and Wilcoxon, 1967) revealed the stratigraphic significance of the asteroliths. Concurrently with the broadening of discoaster studies, other coccoliths with a radial symmetry were discovered and assigned to additional genera (Sphenolithus: Deflandre, 1952; Fasciculithus and Heliolithus: Bramlette and Sullivan, 1961; Catinaster: Martini and Bramlette, 1963; Nannotetrina: Achutan and Stradner, 1969). These studies gave the impetus for abundant documentation (e.g., Hay et al., 1966e.g., Hay et al., 1967; Hay and Mohler, 1967; Perch–Nielsen, 1971a, 1971b, 1971c, 1971d, 1977, Perch–Nielsen et al., 1978; Wise and Wind, 1977) and detailed taxonomic and crystallographic investigations (e.g., Stradner and Papp, 1961; Roth et al., 1971; Black, 1972; Romein, 1979; Theodoridis, 1984), at the same time as they provided the means for developing broadly applicable biozonal schemes (e.g., Hay et al., 1967; Roth, 1970; Martini, 1971a; Bukry, 1973a, 1975), and for considering evolutionary lineages and trends (e.g., Bukry, 1971a; Prins, 1971; Romein, 1979; Perch–Nielsen, 1981a). The introduction of the Order Discoasterales by Hay in 1977 is a testimony to the active research that has surrounded the asteroliths and related forms in the 23 years following Bramlette and Riedel’s seminal publication.

The demand for biostratigraphic resolution imposed by the oil industry as well as by academic research in the Earth Sciences has resulted in sustained efforts since the 1970s to refine our knowledge of the Discoasterales, as synthesized here. The evidence accumulated in the following chapters in support of my interpretation that the highly specialized coccoliths of the Discoasterales are indicative of mixotrophic physiology in this extinct group of coccolithophores (Aubry, 2018), as are the highly specialized coccoliths in living species of the Order Syracosphaerales (Aubry, 2009), may be of interest for research in the private sector and the academia at a time when understanding the fate of organic carbon is of critical importance.

The Order Discoasterales, as emended here, is comprised of 16 Cenozoic genera belonging to two main subordinal clades, Eudiscoasterineae and Sphenolithineae, that diverged from Biantholithus during the late Early Paleocene (text-fig. 1). The origin of two genera (Gomphiolithus, Hayella) is debatable and two taxa (Genus 1 and Genus 2) are poorly documented. Impacted by the climatic, oceanographic and/or extraterrestrial events that have punctuated the history of Earth biosphere, the history of the order during the Cenozoic is documented by nearly 400 species that are known (with two exceptions) only from the residual coccoliths of their collapsed cells. These are “paleontological species”, i.e., taxa based on specimen morphology alone. Our understanding of “true” biologic diversity in this extinct group would have been considerably higher if pseudocryptic speciation was as pervasive as in many living coccolithophores (e.g., Calcidiscus: Geisen et al., 2002, Braarudosphaera: Hagino et al., 2009). Unfortunately, it may be more difficult to determine original species richness in the Order Discoasterales than in any other order, even with the most discriminatory morphometric analysis, because of massive recrystallization that grossly overprints all but a tiny percentage of specimens. Descriptions such as that of Sphenolithus and Fasciculithus as being “forms with innovative calcitic structures, characterized by massive crystals” (Agnini et al., 2007, p. 235, emphasis mine) exemplify the common view of the Discoasterales coccolith. Yet, nothing could be further from reality, as illustrated in this work. In most preservational settings, the coccoliths with delicate morphologies have been modified by postmortem crystal growth along the main axes and faces of the elements, resulting in massive, symmetrical shapes with smooth surfaces and angular sides that are commonly mistaken for original (primary) shapes. As components of coccospheres surrounding living cells, the coccoliths that were secreted by species in the Order Discoasterales probably had remarkably graceful shapes as well as delicate and tidy construction. Glimpses of this original fine delicacy can be seen in exceptionally well-preserved material in ocean-floor sediments that were never deeply buried, and thus not subjected to chemical conditions favoring extensive calcite recrystallization (e.g., Early Miocene sphenoliths from Deep Sea Drilling Site 282 from depth of 45 m below sea floor, Edwards and Perch–Nielsen, 1975) as well as in neritic epicontinental sediments (e.g., New Jersey Margin, Bybell and Self-Trail, 1995; Tanzania, Bown, 2010). These coccoliths matched in every way the delicate morphologies exhibited by some living coccolithophores (e.g., Gaarderella, Papposphaera). As in extant species (Aubry, 2009), the coccolith morphology was highly functional, likely reflecting the mixotrophic physiology of their bearers. This is briefly discussed herein and elaborated on in Aubry (2018).

Serendipitously, the only known coccospheres in the Order Discoasterales are from the stem genus Biantholithus. Assuming that it may serve as a model, it seems reasonable to infer that the diploid (heterococcolith) phase of the life cycle in the Order Discoasterales was non-motile, and with few coccoliths per cell in most if not all taxa. As shown by the living coccolithophores, motility/non-motility is not a taxonomic character at the rank of order. The shape and the large size of many of the coccoliths of the Order Discoasterales are not hydrodynamic and would not fit well with cell motility, however. The high concavity of the proximal face also suggests that coccospheres were composed of few coccoliths, at least in the Paleogene taxa.

A remarkably broad morphologic diversity conceals a profound structural unity in the Order Discoasterales, and this is true for both its Cenozoic and Mesozoic representatives (the latter not discussed here). The coccoliths may be flat and disc-, star- or rosette-shaped; or they may be tall and diabolo-shaped or columnar; some are basket-shaped, others are conical. Symmetry in distal and proximal view is always radial (or rotary), from triradiate to multiradiate. Size varies considerably from tiny (<4 μm) to very large (>30 μm).

All coccoliths are heterococcoliths, i.e., coccoliths formed of modified rhombohedrons (known as elements) arranged in cycles that compose characteristic structural units (see Aubry, 1998a; see also discussion in Aubry, 2013 see also discussion in Aubry, 2018).

With one major exception, each element is typically a tetragonal wedge with two adjacent sides [(a), (b)] of equal length and two sides [(c), (d)] of unequal length (text-fig. 2). The difference in length between the latter sides is pronounced in the older genera, but it may be rather subtle in the younger taxa. Sutures between neighboring elements in a cycle occur along sides (a) and (b). The opposite sides are freestanding. Their unequal lengths result in an asymmetrical but consistent serrate pattern at the periphery of each cycle (text-fig. 3) which is characteristic of two groups, treated here as suborders. In proximal view, from suture to suture and in clockwise direction, the longer side (d) precedes the shorter one (c) in one group. Conversely, in distal view, the short side precedes the long side. This describes the LS_prox/SL_dist pattern that helps orient the coccoliths in the Suborder Eudiscoasterineae. In contrast the coccoliths of the Suborder Sphenolithineae exhibit an SL_prox/LS_dist pattern, which is opposite to that of the Suborder Eudiscoasterineae.

The Order Discoasterales is extinct and no record of coccospheres is known to date except in one genus, Biantholithus. Three lines of evidence concur to show, however, that the LS_prox/SL_dist pattern is ubiquitous in the Suborder Eudiscoasterineae, and that the LS_prox sequence is characteristic of the proximal face:

• a- the concavo-convex profile of some coccoliths (e.g., of Fasciculithus) betrays a proximal position on the cell;

• b- highly derived coccoliths can be oriented by comparison with ancestral coccoliths having a well defined proximal face (as is the case, for instance, for Heliodiscoaster that can be traced back sequentially to Heliotrochus, to Fasciculithus and to Biantholithus;

• c- the coccosphere of Biantholithus itself, constitutes a definitive evidence. All Cenozoic lineages of the order are anchored in this genus. The only possible exception concerns the Early Paleocene genus Gomphiolithus (see below).

An exception to the LS_prox/SL_dist rule concerns the Family Sphenolithaceae in which the coccoliths are more distantly derived from the ancestral Biantholithus than in any other family of the order. In this family, the elements are considerably evolved from the Biantholithus ancestral condition, in which the LS_prox pattern is not as strict as in families of the Suborder Eudiscoasterineae (see below).

Characteristically, the elements form circular cycles. This confers a radial symmetry to the coccoliths that varies from tri- to multi-radial (with as many as 50 elements/cycle). Cycles differ in diameter and height. More substantially they differ by the geometric relationship between their elements, and prominent cycles constitute structural units that occur in superposition. Three structural units characterize the Order Discoasterales. These are the column (Prins, 1971), which is in proximal position, the calyptra (Aubry et al., 2011), located distally, and the collaret (Aubry et al., 2011), which (when present) is located between the column and the calyptra. The column and collaret are always monocyclic units; the calyptra is monocyclic in the older genera but polycyclic in several younger ones, with cycles arranged in superposition. The calyptra is the least conservative of the three structural units. The column and calyptra are present together in most coccoliths of the order, but the calyptra may occur alone (e.g., in asteroliths) and the column may be predominant (e.g., in fasciculiths). The central body is an additional structural unit seen only in certain genera. Together with their relative development, the number of structural units determines the generic classification in the order.

Column – This proximal structural unit is characterized by the absent or very weak imbrication of its elements. The elements are radially arranged with radial sutures in the older genera (text-fig. 4a) and their descendants, or tangentially arranged with sutures curved in clockwise direction in a few of the younger genera. The column may be discoidal, columnar or in the shape of a truncated cone, and its proximal face is always concave (text-figs. 4b–e). It is a conservative structure that differs little between genera, and then mostly in terms of size (diameter and height).

Calyptra – This distal structural unit is easily differentiated from the column. It may be monocyclic or polycyclic. It is characterized by the dextral imbrication of its elements on the distal face, with sutures curved anticlockwise (text-fig. 5a). When polycyclic, the elements of the outer cycle are non-imbricate with anticlockwise sutures (text-fig. 5b). The calyptra exhibits a much greater morphologic diversity than the column, being circular or stellate in distal view and discoidal, basket-, or umbrella-shaped in side view (text-figs. 5c–j). Whether within a genus or between genera, diversification of the Order Discoasterales mainly resulted from morphologic changes to the calyptra, which documents much of the evolutionary history of the order.

Collaret – This monocyclic intermediate structural unit is characterized by sinistral imbrication of its elements in the oldest genera, but dextral imbrication in the youngest. It is present only in the fluted fasciculiths and the helioliths.

The Central Body – This is a diamond-shaped structure at the distal end of the central canal in crateriform and fluted fasciculiths. It is poorly documented, but would seem to be highly perforated. The central plug in helioliths and asteroliths may be homologous with it.

The structural model described above is specific of the Order Discoasterales. The LS_prox/SL_dist pattern is not unique to the suborder Eudiscoasterineae, but is also seen in other orders, including the Braarudosphaerales, Pontosphaerales and Zygodiscales. On the other hand, the coccoliths of the latter two orders are typically comprised by a margin surrounding a central area, whereas no Cenozoic coccolith of the Order Discoasterales exhibits this basic anatomy (see below).

The coccoliths of the Order Braarudosphaerales also consist of tetragonal wedge-shaped elements. However, these coccoliths are composed of superposed laminae organized in segments (Young et al., 1997; Aubry, 2013; Aubry and Bord, 2013a) not of cycles of elements forming distinct structural units as in the Order Discoasterales. They are homococcoliths, not heterococcoliths.

As in the Handbook of Cenozoic Calcareous Nannoplankton (appropriate chapters in Aubry, 1984appropriate chapters in Aubry, 1988appropriate chapters in Aubry, 1989) the taxonomy of the Order Discoasterales is discussed here in terms of morphostructural groups, for which I have taken appropriate names from the literature.

The diversity of shapes exhibited by the coccoliths of the Order Discoasterales has created a need for more vernacular terms in description. Some terms have been formally introduced (e.g., “sphenolith”: Deflandre, 1952; “stelolith”: Gartner, 1981), but in general researchers have made use of the relevant taxonomic names. For instance, the coccoliths of Fasciculithus are called fasciculiths and those of Heliolithus are called helioliths. In the face of this simplistic redundancy, Young et al. (1997) recommended that the imitative vernacular names be abandoned. This, however, has an unsatisfactory result. Based on structural grounds, Prins (1971) showed that the genus Discoaster could be divided into several genera, all characterized by discoaster coccoliths. In the same way, fasciculiths were recently redistributed among three genera (Aubry et al., 2011). Vernacular descriptive terms thus refer not simply to overall shape, but to a specific morphostructure. Seen in this way, and with classification becoming ever more diverse, it is more important than ever to differentiate the descriptive (morphostructural) from the taxonomic (generic) groupings (Aubry, 1998a). The first category is factual and objective whereas the second is interpretative. The application of this methodological approach allows more morphostructural groups to be introduced in this work, that consist of coccoliths comprised of the same structural units and exhibiting similar overall shape. Most structural units are monocyclic but some consist of several cycles that are identical except for their diameter. Groups exhibiting the same structural components, regardless of morphology, are included in the same taxonomic order, because structural unity permits delineation of phylogenetic history among the groups. Genera within each lineage are then distinguished by differences in shape, combination of structural units, and their ratios. Families are groupings of genera with similar morphologies, and suborders consist of families whose genera belong to a common lineage. Finally, the basic structural model that is evidently common to all these taxa supports monophyletic development of the Order Discoasterales, as defined here. This testable proposition can be verified (or rejected) by future crystallographic analysis and by additional structural documentation of carefully selected specimens.

There is an additional important reason to use morphostructural terms. Referring to coccoliths solely by Latinized taxonomic terms considerably restricts the concept of the coccolithophore species. A living species is characterized by its coccoliths and its coccosphere (also by the presence/absence of flagella and other characters that are not preserved in the fossil record). The use of morphostructural terms is an invitation to expand our knowledge of species, a recognition that each possessed a coccosphere, was motile or non-motile, may have had a holococcolith-bearing stage, and lived at a specific water depth, among other information. With the exception of Biantholithus sparsus and B. astralis, species in the Order Discoasterales are presently known solely from their coccoliths, but it can be hoped that their coccospheres will be discovered in Lagerstatten, like those of several other extinct species in other orders [e.g., Mai et al., 1997; Bown, 2010, 2014]). Also, as the relationship between coccosphere types and environmental conditions are better known, in part through experimentation (e.g., Villarosa Garcia and Porter, 2013) it may also be possible to infer the construction of the coccospheres of extinct species and thus aspects of their biology.

The structural terms adopted here to describe coccoliths of the Order Discoasterales are employed not only for the sake of practicality but also because they identify homologies in support of phylogenetic links between genera. From Prins (1971) we have column, to designate the proximal structural unit characteristic of the order, and from Romein (1979) the name central body to designate a triangular to rhomboidal shaped body occurring in several of the Early Paleocene genera of the order. The name calyptra was introduced by Aubry et al. (2011) for the distal structural unit that is also characteristic of the order, a feature that was previously identified as the “dome-shaped structure” of Prins and (in part) the “cone” of Romein. The term collaret, also introduced by Aubry et al. (2011) refers to the monocyclic unit that occurs between column and calyptra in some morphostructural groups. This median cycle underwent a reversal in the direction of imbrication of its elements, from sinistral in fluted fasciculiths to dextral in helioliths.

The Order Discoasterales includes eight well established morphostructural groups. They are introduced below (see also Glossary), in alphabetic order (for convenience), with a brief review of taxonomic content. Three other isolated groups of coccoliths are also assigned to the order, but remain unassigned to a morphostructural group. These are the genera Hayella Gartner 1969a and Ilselithina Stradner and Adamiker 1966, previously not included in this order, and certain other coccoliths (Heliolithus floris, Heliolithus crassus) that are placed in open nomenclature at this time.

Overview – Asteroliths (syn. discoasters) are a major component of coccolithophores assemblages at low and mid-latitudes. They range from Upper Paleocene to Upper Pliocene, with an evolutionary history punctuated by distinctive radiation and extinction events, as well as turnovers and pronounced trends, that make them the most biostratigraphically useful Cenozoic coccoliths.

Morphology – Asteroliths are generally divided into two morphologic groups of rosette- and star-shaped discoasters, albeit with a considerable overlap in shape and structure between them. Asteroliths exhibit a broad morphologic diversity, whether in terms of size, general shape in plane and side views, number and shape of elements (or rays), diameter of the central disc, presence and shape of central knobs and/or stems.

Structure – Most asteroliths consists of a single structural unit, the calyptra, with polycyclic structure that is identified by comparison with the calyptra of Heliotrochus. In some of the earliest asteroliths, the column is present, but flattened and nested at the center of the proximal face of the calyptra; this remnant cycle and the polycyclic calyptra are evidence that the asterolith structure is an evolutionary modification of the heliolith in Heliotrochus.

In most asteroliths the sutures between the rays are radial on the proximal face although slightly curved dextrally in a few others. In contrast the shape of the sutures on the distal face is indicative of two main groups. In one group, the sutures are straight, as on the proximal side. In the other group, the sutures curve anticlockwise, and are sometimes crooked. These two groups are further distinguished by the orientation of the knob or stem when present. In the group with radial sutures on both faces, the tips of the lobes of the distal knob point towards the axis of the rays whereas the tips of the lobes of the proximal knob are aligned with the sutures between rays. In the other group, the lobes of both the proximal and distal knobs are aligned with the sutures. In both groups the serration pattern at the periphery of the astroliths is of the LS_prox/SL_dist type. These differences are at the basis of the generic taxonomy adopted here, in which asteroliths of the first group are assigned to the genus Eudiscoaster and those of the second group to the ancestral Heliodiscoaster.

Generic taxonomy – Asteroliths have generally been collectively assigned to the genus Discoaster Tan Sin Hok 1927 ex 1931, and this is still common practice. The name Discoaster is however tainted with original ambiguity, because three other names (Eudiscoaster Tan Sin Hok 1927, Heliodiscoaster Tan 1927 and Hemi-Discoaster Tan Sin Hok 1927) were simultaneously introduced in apparent synonymy with it. Other genera and subgenera introduced to describe asteroliths, notably by Prins (1971), are impractical, while the use of the names Eudiscoaster and Heliodiscoaster have been encouraged (notably by Theodoridis, 1984) and this is followed here. These two genera represent natural groupings as indicated by the differences in the details of their structure (see above).

Heliodicoaster – Asteroliths consisting of a rosette- to star-shaped calyptra with sutures radial or dextrally curved on the proximal face, and sinistrally curved on the distal face. When a knob or stem occurs on one or both faces, the tips of its lobes are aligned with the sutures between the rays on both faces.

Eudiscoaster – Asteroliths consisting of a star-shaped calyptra with sutures radial on both faces. When a knob or stem occurs on one or both faces, the tips of its lobes are aligned with the sutures between the rays on the proximal side, and with the axis of the radiating rays on the distal side.

Overview – Biantholiths are a small group of Paleocene coccoliths with exceptional evolutionary significance. As the first coccoliths to have evolved immediately after the end-Cretaceous mass extinction event, they are at the origin of the Cenozoic diversification of the Order Discoasterales.

Morphology – In proximal or distal view, biantholiths are simple, concavo-convex discs, which, in side view, may be thin or with a diabolo-shaped profile.

Structure – Biantholiths consist of two superposed, discoidal, monocyclic structural units of similar diameter, that differ in the imbrication of their elements and the orientation of the sutures between them.

The column consists of six to twelve non-imbricate elements separated by radial sutures.

The calyptra consists of six to twelve dextrally imbricate elements separated by strongly anticlockwise sutures.

Generic taxonomy –

Biantholithus – Biantholiths are discoidal and thin. The column and the calyptra are little differentiated morphologically.

Diantholitha – Biantholiths essentially in the shape of a diabolo. The column and calyptra are morphologically well differentiated, the latter being taller than the former.

Overview – Catinaliths occur exclusively in upper Middle and lower Upper Miocene sequences, making them excellent zonal markers at low and mid-latitudes. Regarded by some as asteroliths from which they are clearly derived, they differ by an unusual construction, in which extension and broadening of the finger-like projections at the tip of the bifurcated rays of a six-rayed discoaster merge with the radially and vertically extended lobes of the distal knob to form six septas.

Morphology – Catinalihs are in the shape of a deep or shallow basket spanned by a asterolith-like, hexaradial star. The latter confers a typical hexaradial symmetry that is enhanced, in some species, by long, free rib-like arms.

Structure – Catinaliths are formed by a considerably modified calyptra that is folded onto itself into a calyx spanned by septa. The calyptra is monocyclic, consisting of six elements, each element forming both one sixth of the calyx and a septum. The septa may extend as thin ribs beyond the rim of the calyx.

Generic taxonomy –

Catinaster – All catinaliths, as described above, are assigned to the genus Catinaster. However, this genus has previously included the form Catinaster mexicanus for which the genus Myrsaster is introduced here. Catinaliths and myrsaliths are of different ancestry within Eudiscoaster.

Overview – Fasciculiths are a main component of Late Paleocene calcareous nannoplankton assemblages at low latitudes, and they constitute one of the best known groups of extinct coccolithophores. Many species have been abundantly illustrated, in particular by Perch–Nielsen (1971d, 1977). Their structure was first discussed by Prins (1971) and Romein (1979) and revised in Aubry et al. (2011). On the basis of the number of constituting structural units, fasciculiths form three groups, each corresponding to a genus.

Morphology – Fasciculiths are coccoliths in the general shape of a cylinder. Most average 5 to 8 μm, which is smaller than most other coccoliths in the order, but a few measure up to 17 μm in height. Their shape is roughly that of a low cylinder surmounted, in most instances, by a conical or needle-shaped edifice. The proximal end of the fasciculith is depressed while the distal end is convex or sharply pointed, except in the two oldest forms, where it is deeply concave. They exhibit bilateral symmetry in lateral view, and axial symmetry in proximal view. Their surface may be smooth or ornamented with small or large depressions. Under the light microscope, in cross-polarized light, the extinction lines are straight and parallel with the directions of polarization (Romein, 1979, p. 150).

Structure – All fasciculiths consist of a (proximal) column and a (distal) calyptra.

The column is the prominent unit in fasciculiths. It is essentially cylindrical, concave at the proximal end, slightly convex, flat or concave at the distal one, and consists of a single cycle of radiating, tall, tri- or tetrahedral elements that are wedged around a central canal. The transverse section may be rosette-or star-shaped (in Fasciculithus) because of the vertical ridges separated by deep and narrow furrows or broad notches that run on the sides of the fasciculith. The primary characters of the elements is known in Fasciculithus, poorly documented in Lithoptychius and undocumented in Gomphiolithus.

The calyptra (‘cone’ in Romein, 1979) is a single cycle of triangular plate-like elements that are dextrally imbricated with oblique sutures oriented anticlockwise. Generally prominent in Fasciculithus and Lithoptychius, it is reduced to a very thin cycle in Gomphiolithus.

The collaret, located between the column and the calyptra, consists of a single cycle of lath-shaped elements with sinistral imbrication. Together the collaret and calyptra form the cone, a term used here only for descriptive purpose.

The central body, at the distal end of the column, is not well exhibited. It is located at the distal end of the central canal in some fasciculiths.

Generic taxonomy – Fasciculiths clearly constitute a characteristic morphostructural group, and for this reason have been assumed to represent a single lineage (Prins, 1971, Romein, 1979; Perch–Nielsen, 1981a), an assumption followed to this day, and assigned to the single genus Fasciculithus Hay & Mohler 1967. However, beyond the morphostructural similarities, there are significant differences, which support consistent subdivision of fasciculiths into three subgroups, the older two with disjunct stratigraphies. A possibility is that rather than being directly related to one another, the three subgroups evolved separately from the same common ancestor. In this perspective, Gomphiolithus, Lithoptychius and Fasciculithus would result from iterative evolution. While this requires further consideration, the three subgroups are treated as three genera, which are distinguished on the basis of morphostructural differences (Aubry et al., 2011):

Fasciculithus – Fasciculiths with column and calyptra both exhibiting an alveolar texture in most species, leading to their nickname of “honey-comb fasciculiths”. There is no central body or collaret.

Gomphiolithus – Fasciculiths with a prominent column, a well differentiated central body at the distal end of the generally broad central canal. The calyptra is possibly a very reduced lining in the deeply concave distal end; no collaret. Nicknamed “crateriform fasciculiths” for their deeply concave distal end.

Lithoptychius – Fasciculiths with a collaret between column and calyptra and with a central body at the distal end of the central canal. The column was likely ornamented with vertical ridges delineating deep depressions, justifying their nickname of “fluted fasciculiths”.

Overview – Helioliths are characteristic components of Late Paleocene calcareous nannoplankton assemblages. They may be best described as wheel-shaped coccoliths as seen in plane view, which, in this position and in cross-polarized light, are strongly birefringent, whether partly or completely, and produce an extinction cross with orthogonal arms except near the periphery where they curve. Their shape in side view varies considerably as a result of differential development of their three component structural units, column, calyptra and collaret. Three genera are recognized accordingly. In Bomolithus the collaret and calyptra are joined in a super-unit (cone) that flares in opposition to the column. In Heliotrochus, the collaret and column form a super-unit (pillar) overlain by a broad, thin calyptra. In Heliolithus, it is the column and calyptra that flare in opposite directions.

Morphology – Helioliths are large coccoliths (6–17 μm in diameter). Always circular in plane view, they may be diabolo-, mushroom-, or disc-shaped in side view. The proximal face is deeply concave in most species, and the distal face may be flat to slightly convex, or more or less strongly concave. Their symmetry is essentially radial in plane view, bilateral in side view.

Structure – Helioliths may be comprised of two or three structural units:

The column is cyclindrical, of variable height and with a concave proximal face. It consists of a single cycle of tall, wedge-shaped, tangentially arranged elements or of thin, wedge-shaped elements arranged in a flaring cone. The sutures typically curve in clockwise direction. The elements are ornamented with ridges delineating deep valleys and furrows.

The calyptra is polycyclic. The inner cycle(s) are composed of lath-like elements that are dextrally imbricated with oblique sutures oriented anticlockwise. One or more such cycles are surrounded by a cycle of non imbricate elements with sutures oriented anticlockwise. There may be a plug-like central cycle.

The collaret consists of a single, low cycle of lath-shaped elements with dextral imbrication. It is absent in some species of Heliotrochus, and vestigial in Heliolithus.

Generic taxonomy – Helioliths have been divided into three groups represented by the genera Bomolithus Roth 1973, Discoasteroides Bramlette & Sullivan 1961, and Heliolithus Bramlette & Sullivan 1961. Romein (1979) has shown the inappropriateness of the combination Discoasteroides megastypus. Unlike helioliths, the generotype Discoasteroides kuepperi does not possess a ‘column’. A few authors (e.g., Romein, 1979; Aubry, 1989) have considered the differences between Bomolithus and Heliolithus species too small to support a generic distinction.

Two competing interpretations of the structure of the helioliths have been given in support of different generic determination. Romein (1979) described helioliths as comprised of three structural units, and saw no need for a genus name other than Heliolithus (text-fig. 6). He based his conclusions on extinction patterns in cross-polarized light with a gypsum plate, and determined that in all helioliths the extinction lines are laevogyre, being straight over most of their length and curving peripherally. The extinction cross is offset in clockwise direction with the polarization directions. The angle is ~20°. Whereas some helioliths are completely birefringent, only the column is birefringent in others. This was ground for Perch–Nielsen (1984) to transfer the taxon conicus from Heliolithus to Bomolithus (in which only the column is birefringent). Steurbaut (1998), in contrast, distinguished two groups of helioliths, one with three structural units and the other with only two, based on differences in birefringence among the units, and identified the two groups as species of separate genera (text-fig. 7). In this interpretation, Bomolithus Roth 1973 consisted of helioliths in which one or two of the three units lack birefringence, and Heliolithus was restricted to completely birefringent helioliths regardless of the number of component units.

Neither scheme is satisfactory, in that both ignore the fact that it was not birefringence but the geometric relationships between the structural units of their helioliths that define the two genera. Heliolithus was erected for “Forms consisting of two partial cones joined at truncate apices and having concave basal ends” (Bramlette and Sullivan, 1961, p. 164). Bomolithus was introduced for helioliths in which “the uppermost cycle is higher than the others and the elements slope towards a central depression. The two lower cycles are sinistrally imbricate and slope towards the periphery” (Roth, 1973, p. 734). While Roth actually oriented the Bomolithus heliolith upside down, this is secondary to his identification of the structure. An important difference between Heliolithus and Bomolithus, thus, concerns the median cycle that flares distally in Bomolithus, forming a concavity in which the distal unit is nested, whereas in other helioliths, the median cycle is more subdued and the distal structural unit is free standing.

There is much heterogeneity among helioliths with no consistent patterns in the association of structural characters (Table 1). Additionally, their documentation in the SEM is very uneven, some species (e.g., H. kleinpellii) being well documented, whereas others (e.g., H. riedelii) remain poorly illustrated and understood. Further, the distal faces are much less well documented than the proximal ones, perhaps because of the position of the helioliths in the SEM preparations. Side views are plentiful although they are not as valuable as distal views for species description and phylogenetic reconstructions. Despite these limitations, the geometric relationships and characteristics of the structural units, as above, is the basis for the present assignment of helioliths to three genera in the present work.

Bomolithus – Helioliths in which the collaret and calyptra are similarly oriented to form a cone, in opposition to the column.

Heliotrochus – Helioliths in which the collaret and column are of similar diameter and similarly oriented to form a pillar. The calyptra is much broader than the pillar, and essentially planar.

Heliolithus – Helioliths diabolo-shaped with column and calyptra flaring in opposite direction. The column is lower and more flaring than the calyptra, and the distal and proximal faces are deeply concave.

Overview – Myrsaliths are described from the Upper Miocene and they may also occur in the Middle Miocene and Pliocene. They are clearly related to the Eudiscoaster extensus group.

Morphology – Myrsaliths are small and globular, in the shape of a deep basket spanned by a an asterolith-like, hexaradial star. Their rim is typically scalloped, and the central star is restricted to the calyx.

Structure – Myrsaliths consist of a considerably modified two-tiered calyptra that forms the distal calyx with its typical lobate elements as well as the proximal hexaradial septa, each septum meeting the calyx between consecutive elements.

Generic taxonomy –

Myrsaster – All known myrsaliths exhibit the same morphology and structure; thus, despite their disjunct stratigraphic range, all are assigned to the genus Myrsaster. It is important to recognize that although morphologically similar, myrsaliths and catinaliths have markedly distinct structure and should be treated as separate morphostructural entities.

Overview – Sphenoliths are a main component of Middle Paleo-cene through early Late Pliocene deposits on epicontinental shelves and in the deep sea. Although generally small (<10 μm in height, and 3 to 4 μm in diameter, on average), they are readily noticed during analysis in cross-polarized light because of their distinctive extinction patterns. The combination of characteristic morphologies, high diversity, rapid rates of evolutionary turnovers and broad geographic distribution confers to the group a dominant role in biostratigraphic correlations.

Morphology – Sphenoliths have a radial symmetry, being circular in proximal and distal view, and in transversal section. They are most commonly seen in side view, however, where they exhibit a bilateral symmetry, typically with a hemispherical or triangular profile. Under a light microscope, they are highly refringent with a characteristic spiny texture in bright field, and strongly birefringent in cross-polarized light. In SEM images they clearly exhibit two parts, one a concavo-convex proximal column, surmounted by a generally extended distal calyptra, which may be rounded, pointed or bi- or multi-furcate. More often than not, both parts are sturdy, with the calyptra made up of robust spine-shaped elements. Based on general morphology and extinction patterns, sphenoliths are here differentiated into five morphological groups: hemispherical, conical, flaring, lanceolate and elongate.

Structure – Sphenoliths are comprised of two structural units, each primarily consisting of highly differentiated elements, or triades. Triades are trihedral elements that combine to form the honeycomb texture that characterizes sphenoliths. The very thin and delicate triades are easily affected by secondary overgrowth after release from the coccosphere, and become thick spines that fill the original alveolae.

The column is in the shape of a truncated cone with more or less steeply inclined sides. It consists, characteristically, of keeled triades regularly arranged in a single cycle, the keels being parallel to the side of the column.

The calyptra is polycyclic, and may consist of triradiate triades only (hemispheral sphenoliths), winged triades only (lanceolate sphenoliths) or of a combination of triradiate and winged triades, arranged in distinct cycles to form, respectively, the lower and the upper calyptra (conical, flaring and elongate sphenoliths).

Generic taxonomy – All sphenoliths are assigned to the genus Sphenolithus Deflandre 1952. Sphenolithus tribulosus may, however, be sufficiently distinct from other sphenoliths to warrant a separate generic assignment, once adequate documentation of the pristine condition is available. In addition, while the coccoliths of Ilselithina are sufficiently different to justify their exclusion from the sphenolith category, their structure is not well enough known to support the introduction of a new name for this morphostructural group. Ilselithina coccoliths are viewed here as strongly derived sphenoliths.

Sphenolithus – Coccoliths are sphenoliths, comprised of column and calyptra both formed from a highly specialized type of element called triade: the column with keeled triades, and the calyptra with triradiate and/or winged triades.

Ilselithina – Coccoliths similar to sphenoliths in which the column consists of keeled triades and their derivatives, and the calyptra consisting of strongly modified triradiate triades.

Overview – Tetrinaliths are known only from the lower Middle Eocene, in which they provide a powerful although regionally inconsistent biozonal tool.

Morphology – Tetrinaliths are large, basket-shaped coccoliths with a four-fold symmetry created by a four-rayed cover that spans their open end.

Structure – Tetrinaliths consist of four elements folded on themselves to form both a calyx and the four septa that span it.

Generic taxonomy –

Nannotetrina – All tetrinaliths are assigned to the genus Nannotetrina.

Since the initial presentation by Prins (1971), no review of the evolutionary history of the Order Discoasterales as a whole has been attempted, and the published phylogenetic studies have been limited to a few genera and only for specific stratigraphic intervals (Romein, 1979; Perch–Nielsen, 1981a; Theodoridis, 1984; Aubry et al., 2012; Monechi et al., 2013). In the following review, various aspects of the overall evolutionary history of this group are discussed, including some that have been given little previous consideration, such as the forcing mechanism(s) that has/have driven diversification.

The heterococcoliths of the Order Discoasterales are radically different from most other heterococcoliths, such as placoliths (e.g., Coccolithus pelagicus) and cribriliths (e.g., Pontosphaera japonica). A typical heterococcolith is comprised of two basic anatomical parts—margin and central area. The margin consists of one (or more) annular structural unit, while the open central space is itself filled, partly or completely, by at least one structural unit distinct from the marginal unit with which it interlocks (text-figs. 8a, b). In this manner, the central structural unit is contained within the marginal unit with which it is laterally juxtaposed. The heterococcoliths of the Order Discoasterales are atypical in this regard, in that they exhibit a “tubular architecture” (Prins, 1971, p. 1026) in which there is no distinction between margin and central area, because the structural units are in superposition rather than in lateral juxtaposition. In other words, in these coccoliths, the structural unit(s) of the central area overlies the marginal structural unit(s) rather than being surrounded by it (text-figs. 8c, d).

Two possibilities may explain this difference from other heterococcoliths. One is that the two types of heterococcoliths evolved separately, which would indicate a major divergence during the Late Triassic evolution of the earliest coccoliths. The other possibility is that Discoasterales coccoliths evolved through the closure of the central opening of a typical circular heterococcolith, leading to the distal migration of the central structural unit over the marginal structural unit. The latter interpretation is preferred for two reasons. Firstly, coccoliths of the Order Discoasterales (hetero)coccolith are not known prior to the Early Cretaceous (Aubry and Bord, 2013b, and unpublished), which seriously conflicts with a basal divergence among heterococcoliths. Secondly, the central hole of the distal unit in the Discoasterales coccolith is centered over the radial axis of the coccolith and aligned with the narrow conduit that is a remnant of the ancestral central opening (see below), which indicates that the Discoasterales coccolith evolved from a typical heterococcolith.

Different evolutionary paths could have led to the development of the Discoasterales coccolith (text-fig. 9) from a typical heterococcolith. In one path, the closure of the central opening would result in distal migration of the central structural unit over the marginal structural unit (text-figs. 9a1–a3). Alternatively, progressive reduction of the distal marginal structural unit itself would cause the central structural unit to move to an increasingly distal position (text-figs. 9b1–b4).

With regard to this latter path, there is compelling evidence that this was in fact the route in the evolution of coccoliths of the Order Discoasterales from coccoliths of the short–lived Cretaceous Family Eprolithaceae Black 1973, as first suggested by Prins (1971). As seen from above, the margin of the circular coccoliths of Eprolithaceae enclose a tubular or diabolo-shaped central area that is spanned by a central structural unit (text-fig. 10). Appropriately named “diaphragm” this very characteristic unit — which is unique to the Family Eprolithaceae among Mesozoic coccoliths — consists of “nine triangular sectors or nine imbricating, rhombohedral plates”(Black, 1973, p. 99; text-fig. 10), that are dextrally imbricated with sutures that strongly curve anticlockwise. This structure resembles in all characters but the number of elements the calyptra, a unique feature that in turn distinguishes the Order Discoasterales among Cenozoic coccoliths. With little question that diaphragm and calyptra are homologous, we may safely conclude that the Order Discoasterales evolved from a species within the Family Eprolithaceae.

Black (1973) illustrated coccoliths of Eprolithaceae from the Gault Clays (Albian) of southern England and France. In Eprolithus apertior (text-figs. 10a–f) the margin encloses a tubular to diabolo-shaped central area that is spanned at mid height by the “diaphragm”. In Radiolithus caliciformis (text-figs. 10g–k) from the same levels, the central area is also tubular but the diaphragm is located distally. This difference may be significant for the origin of the Discoasterales coccolith. In Eprolithus species the margin consists of two superposed structural units, with the central diaphragm aligned with the sutures between them, suggesting that the relocation of the diaphragm to a distal position, as seen in R. caliciformis, is due to progressive reduction in height, that would eventually lead to the disappearance of the distal marginal unit in the ancestral lineages of Discoasterales. The remaining step in evolution of the Discoasterales coccolith would have been a relatively simple centripetal expansion of the marginal elements so as to fill in the central area, resulting in the marginal structural unit supporting the central diaphragm as seen in the typical superposition of column–calyptra (text-fig. 9, model b).

In conclusion, the coccoliths of the Order Discoasterales are highly derived. The column and the calyptra are, respectively, marginal and central structural units that are in superposition by derivation. This agrees well with the fact that the column (proximal) is a more conservative structural unit than the calyptra (see above). With only few exceptions, marginal structural units are more conservative than central structural units (as shown in Coccolithophores). The terms margin and central area should thus be avoided when discussing the coccoliths of the Order Discoasterales.

The reorganization of the spatial relationship between marginal and central structural units at the foundation of the Order Discasterales was a unique innovation that carried unprecedented evolutionary possibilities. It led to a morphologic and structural diversity greater than in any other order with the possible exception of the Order Syracosphaerales, resulting in genera that achieved success and others that achieved dominance (Aubry, 1998a) according to the concepts of success and dominance cited by Wilson (1992, p. 129). For example, success, “best defined as the longevity of a species and all its descendants”, characterizes Heliodiscoaster and Eudiscoaster. Dominance, which is “both an ecological and evolutionary concept […] measured by the relative abundance of the species group in comparison with other, related groups, and by the relative impact it has on the life around it” can be attributed to Lithoptychius and Fasciculithus. The superposition of structural units also led to extremely specialized coccoliths, some with highly modified elements such as the triades of sphenoliths, and others melded into a single structural unit — both features being unique to the Order Discoasterales.

By comparing optical properties among the coccoliths of the Order Discoasterales, Prins (1971) was able to determine homologous morphostructural characters. Without the abundant iconography in electron microcopy now available, he was still able to determine that a biantholith is comprised of two cycles, and placed Biantholithus at the origin of Fasciculithus from which three main lineages were proposed to have arisen, leading to the highly diversified Heliodiscoaster and Eudiscoaster (and other genera) (text-figs. 11a, b). He (and subsequent authors) illustrated specimens that were interpreted (often without much hard evidence) as being the transitional forms that supported these lineages (text-fig. 12, and individual chapters in this work). In time, while further optical analysis of coccoliths provided definitive evidence of a Fasciculithus-Heliolithus-Discoaster lineage (Romein, 1979; text-fig. 13), it failed to confirm a linkage to Biantholithus, leaving this taxon isolated. The recent discovery of new taxa, in particular of Diantholitha, has helped to confirm the central role that Biantholithus has had in the diversification of the Order Discoasterales (Aubry et al., 2012; text-fig. 14a,b).

The early Paleogene lineages presented here (text-fig. 1) essentially agree with Romein’s interpretation, in particular with regard to the derivation of helioliths from fasciculiths, not through Fasciculithus tympaniformis and Heliolithus riedelii, respectively, but rather with Lithoptychus, Heliotrochus, and Bomolithus elegans (Heliolithus elegans in Romein, 1979) serving as a link in this transformation (compare text-figs. 1 and 13). An important difference between the two interpretations concerns the relationships within fasciculiths. Romein (1979) established a direct linear lineage in which Fasciculithus [now Lithoptychius] ulii evolved from Fasciculithus [now Gomphiolithus] magnus, and then gave rise to Fasciculithus tympaniformis. While this is also the interpretation of Monechi et al. (2013), Diantholitha is inserted in the Gomphiolithus–Lithoptychius lineage (text-fig. 15). In this case, a difficulty arises in that Diantholitha is a biantholith, not a fasciculith (see definition above). Its morphostructure is directly comparable to that of Biantholithus sparsus in which the column would be expanded proximally and the calyptra distally.

The divergence of fasciculiths from biantholiths involved several morphostructural changes. These were 1) the proximal expansion of the column in the fasiculiths Gomphiolithus and Lithoptychius; 2) a reduction of the calyptra in both genera, with that in Gomphiolithus being more extreme; 3) the appearance of a prominent central body, also in both genera; and 4) the appearance of the collaret in Lithoptychius. I argue that the rise of these two fasciculith genera represent successive divergences from Biantholithus, and not a sequential evolution from Biantholithus to Gomphiolithus to Lithoptychius. In contrast, the trends in Lithoptychius fasciculiths clearly demonstrate that, while these were ancestral to the typical fasciculiths of Fasciculithus, they were also at the origin of the helioliths of the Bomolithus–Heliotrochus lineage, from which, ultimately, the asteroliths of Heliodiscoaster and their descendants evolved. There is thus a clear lineage rooted in Biantholithus that involved successively fasciculiths, helioliths and asteroliths, and from which tetrinaliths, catinaliths and myrsaliths branched out. This lineage forms the Suborder Eudiscoasterineae (see below for formal definition).

Present evidence makes it clear that sphenoliths also evolved from biantholiths. This involved a characteristic change in the shape of the elements, from scaly in biantholiths to trihedral in sphenoliths. Furthermore, a trend towards acquiring trihedral elements can be seen in biantholiths (notably in the calyptra of the Diantholitha-biantholiths) that presages the sphenolith’s entire composition of triades. In parallel with this, the monocyclic calyptra of biantholiths gave rise to the polycyclic calyptra of sphenoliths, with monocyclic calyptras in some sphenoliths a secondary development. Finally, the presence of triades in the coccoliths of Ilselithina indicates with high probability that this genus derived from Sphenolithus. Although the existing iconography is inadequate to explain how the transition occurred, a Sphenolithus-Ilselithina lineage rooted in Biantholithus forms the Suborder Sphenolithineae (see below for formal definition).

The primary difference between the coccoliths of the Suborder Fasciculithineae and Suborder Sphenolithineae lies in the peripheral pattern of serration. In distal view, the coccoliths in the first noted suborder are characterized by the SL pattern, while those of the second display the LS pattern. This divergence would seem to reflect the inheritance of these respective patterns from different populations of the ancestral Biantholithus in which the SL pattern, while more common than the LS pattern, is not universal. It is as if a differentiation at the very basic level of the orientation of a crystal was determinant for the subsequent evolution and diversification of the coccoliths that carried one character or another.

With sixteen comprehensively described genera in eight morphostructural groups, the Order Discoasterales is the second most diversified order of the Cenozoic coccolithophores. In addition, with close to 400 morphologic species it also ranks second with regard to species richness, with this number expected to increase significantly if cases of cryptic speciation are demonstrated in all genera. Within the order, diversification was uneven, with suborder Eudiscoasterineae contributing over 80% of the diversity whether measured in terms of species richness, number of morphostructural groups or longevity of genera (Table 2). Three Discoasterales genera were particularly successful (see also text-fig. 1). These are (in order of appearance) Sphenolithus, Heliodiscoaster and Eudiscoaster, with life spans of ~59, 30 and 40 Myr, and >60, >80 and 150 described species, respectively. Other genera, however, had a short life span, and low species richness.

In general, diversification in the coccolithophores resulted from the introduction of morphologic and/or structural innovations that would allow the exploration of new morphospaces to extents that varied in large part depending on the effectiveness of the innovations themselves. As cited above, the collaret and the triades that replaced the ancestral scaly elements are examples of innovations that were determinant in the establishment of Discoasterales lineages. A means of assessing the extent of diversification in a clade, and in particular the amount of divergence from the basal to the crown taxa, is to compare formulas that ‘mathematically’ describe the taxa in the clade. The methodology is as follows: first, we take the maximum number of structural units in the coccoliths of the Order Discoasterales at four (column, collaret or medial cycle, calyptra, central body) and the minimum is one (either column or calyptra). As we have seen the column and calyptra are the fundamental structural units inherited from the ancestral morphostructure, and these units are in superposition because of a translation of the central area cycles over the marginal cycles during evolution from the stem coccolith. It appears most likely that the column originated from the margin and the calyptra from the central area. Given this understanding, it is possible to establish a formula that describes a genus in terms of the number and relative location of the structural units (and their cycles) characteristic of its coccoliths (text-fig. 16). Once the formulas are placed in a phylogenetic framework, their comparison offers a rapid means of assessing the amplitude of the differences between genera and higher taxonomic ranks.

The comparison between formulas (text-fig. 17) reveals very different evolutionary paths in the Suborders Eudiscoasterineae and Sphenolithineae. The latter arose from two basal innovations: a) triade, and b) polycyclic calyptra. The lack of further major innovations explains the relatively limited diversity in this group. By contrast, four main innovations occurred sequentially in the Suborder Fasciculithineae: a) collaret, b) polycyclic calyptra, c) loss of the column and tranformation of the scaly elements of the calyptra into rays and d) rotation of distal knob. This sequence resulted in marked morphological changes in the clade, with the crown taxa deviating considerably from the basal taxa. The ultimate deviation from the ancestral morphostructure was achieved with the catinaliths in which the ray tips in the calyptra folded on themselves while considerably broadening and lengthening.

The distribution of the innovations marks three main episodes of diversification among the Discoasterales. Groups differentiated rapidly during the earlier episode, leading to short-lived Paleocene radiations and extinctions (see below). This was followed by the broad diversification of Heliodiscoaster through the Eocene, from which Eudiscoaster stemmed during the Middle Eocene, and from this leading on to a Miocene episode of more rapid diversification. The diversification of Sphenolithus began in the earliest Eocene and continued through the Miocene. Its decline parallels that of Eudiscoaster during the Pliocene. Details of this diversification history are presented in appropriate chapters of this work. The Paleocene radiation, however, is discussed in more detail here because it involved several taxa simultaneously, and also because these developments are relevant in global chronostratigraphy.

Two genera stand out in the early stage of diversification in the Order Discoasterales. Lithoptychius and Fasciculithus underwent major radiations, the first named at the beginning of the Middle Paleocene (at ~62 Ma), and the second in the Late Paleocene (at ~59 Ma). These radiations were first described by Romein (1979) at a time when all fasciculiths were assigned to Fasciculithus (text-fig. 18) so that they became known as the “First Radiation” and “Second Radiation” of Fasciculithus. Although it would seem simple enough to rename them, respectively, the “Lithoptychius radiation” and “the Fasciculithus radiation”, this requires consideration of their descriptions by different authors (Table 3). For instance, Romein included species that are now assigned to other genera in the first radiation. More importantly, this radiation has since been divided into two diversification events (Steurbaut and Sztrákos, 2008), which led to the initially confusing renaming of the second radiation sensu Romein as the “third radiation of fasciculiths” (Bernaola et al., 2009). This simplified characterization is now widely accepted, even as the contents of the first and second radiations sensu Bernaola et al. have become less distinct, for example with the uncertain placement of Diantholitha.

There is a difference in scale between the original radiations sensu Romein, which were truly bursts of diversification, each with its own mode and tempo, and the diversification event named the “Second Radiation of Fasciculiths” by Bernaola et al., and which can be seen as little more than a new threshold in the first radiation sensu Romein. In fact that threshold is difficult to interpret because the sections that provide the information for the first radiation sensu Romein consist of a relatively thin stratigraphic interval that is almost (but not totally) devoid of Lithoptychius fasciculiths (Steurbaut and Sztrákos, 2008; Aubry et al., 2012; Monechi et al., 2013). This interval immediately precedes the second radiation sensu Bernaola et al., suggesting that the two episodes of diversification were likely to have been separated by a period of rarefaction (dubbed the “Lithoptychius paracme”, Monechi et al., 2013, p. 36). If the Lithoptychius paracme was truly the result of a temporary global change in oceanographic conditions (i.e., change to mesotrophic cooler waters as inferred by these authors), the “second diversification of fasciculiths” was a real evolutionary event that marked the end of disastrous environmental conditions for Lithoptychius. However, at both the Zumaya and Qreiya sections, the paracme interval is characterized by intense dissolution of coccoliths, so that fasciculiths are very poorly preserved (Aubry et al., 2012; Aubry et al., Criscione, 2017); the increase in relative abundance of the diagenetically resistant coccoliths Toweius spp. and Sphenolithus spp. in the paracme interval, as cited by Monechi et al. (2013) is easily understood in this context, and strongly suggests that the “second radiation of fasciculiths” may be a misinterpretation of differential preservation during the paracme. A radiation being classically understood as a sudden burst of diversification within a clade, I therefore refer here to the “Radiation of Lithoptychius” and the “Radiation of Fasciculithus” (Table 3) rather than to a succession of three evolutionary pulses.

The radiation of Lithoptychius is part of a broader expansion that can be referred to as the late Early Paleocene diversification of the Order Discoasterales, an event that led to the domination of this group in coccolithophore history through the Middle and Late Paleocene and during which the Cenozoic representatives of the order became established. This biotic experiment began with Gomphiolithus, a conservative form with few and scarce species, continued with the rise to Diantholitha slightly before the appearance of Lithoptychius, and which diversified very rapidly into three species before becoming extinct without known descendant only 400 kyr after its appearance. Sphenolithus appeared shortly thereafter, but would diversify little until the Eocene. In contrast, with the evolution of Lithoptyclius the diversification of the order during the Cenozoic began in earnest.

There is an interesting contrast in the fate of these four genera. As evolutionary experiments, Diantholitha and Gomphiolithus were failures or dead ends in the sense that their morphostructure had little potential for further useful modification. Diantholitha in particular did not diversify further for the same reason that the genus Biantholithus had few, relatively short-lived species: there was little possibility for variation within the boundaries of the biantholith morphostructure. The evolution of a biantholith ancestor into the Gomphiolithus fasciculith, essentially formed by a massive column, also offered little potential for diversification. However, the modification of a biantholith by inflation of the calyptra, elongation of the column, and insertion of a collaret between column and calyptra, as described above, resulted in the Lithoptychius fasciculith with its great potential for wide adaptations. The biantholith-sphenolith transformation, which involved a change in the shape of the elements and the multiplication of cycles in the calyptra, would also prove a successful innovation, although with more limited evolutionary potential (see above).

As the Order Discoasterales diversified, coccolith morphologies and structures developed that were unique among coccolithophores. At the same time, iterative evolution led to repetition both within Suborder Eudiscoasterineae and between it and Suborder Sphenolithineae (text-fig. 1). The independent acquisition of the same morphology is seen in the fasciculithshape of the coccoliths of Gomphiolithus and Lithoptychius, thought to have diverged separately from Biantholithus, and also in the basket form common to tetrinaliths (Nannotetrina), catinaliths (Catinaster) and myrsaliths (Myrsaster). Likewise, the structural innovations of polycyclic calyptras was developed independently in sphenoliths (Sphenolithus) and helioliths (Bomolithus), as well as the return to a simpler calyptra in the unrelated lineages of S. predistentus and Heliodiscoaster (monocyclic and bicyclic calyptras, respectively).

It is in the fine detail of the surficial texture of the coccoliths, however, that the instances of convergence are strongest (text-fig. 19).

The honeycomb texture of sphenoliths, which conferred an overall honeycomb surface to the entire coccosphere, is present in the earliest (late Danian) species. On the other hand, while the earliest fasciculiths (Danian-Selandian) did not have such a texture, the Late Paleocene-earliest Eocene (Biochron NP9) species of Fasciculithus developed intersecting surface ridges outlining deep rectangular alveoli in a pattern highly reminiscent of the one produced by the triades of sphenoliths, so that the Fasciculithus coccospheres also exhibited a honeycomb aspect.

A marked trend among fasciculiths gives clear evidence that the convergence in surface texture between sphenoliths and fasciculiths was adaptive, as might be expected. Although the texture of the oldest fasciculiths (Gomphiolithus) is unknown at this time because all SEM-illustrated specimens are strongly recrystallized, we can see that the column of the Lithoptychius fasciculiths was deeply fluted in a pattern reminiscent of that created by the keeled triades in the column of sphenoliths, even though the pattern in Lithoptychius fasciculiths was more extensive because of the greater height of their column. The later honeycomb pattern, possibly a simple modification of the fluted pattern, resulted in the remarkable textural convergence between sphenoliths and fasciculiths. This was enhanced by an associated morphologic convergence, in which some fasciculiths acquired hemispherical and conical shapes (e.g., F. involutus, F. schaubii) that mimicked the shape of Late Paleocene sphenoliths (e.g., S. primus, S. rio).

The Sphenolithus and Fasciculithus coccospheres that were formed by these unusual coccoliths were unlike any heterococcolith-bearing coccosphere in today’s living plankton. Instead, they would have come very close to the most porous holococcolith-bearing coccospheres among living species. This is not to say that the probable similarity justifies taking these living forms as precise models for the coccospheres of Fasciculithus and Sphenolithus considering the basic differences in morphology and structure but this nevertheless suggests the general appearance and delicate construction of these extinct groups. An even better understanding of the function of honeycomb surface may be found in certain fungi, which cannot be compared with submicroscopic protist in any other ways than their shape and texture. In this regard, sphenoliths and honeycomb fasciculiths were like the cups of true morels (genus Morchella), such that their coccospheres had the form of deeply pitted morel cups spreading out from a small central sphere. This image makes the point that such a coccosphere would have been too delicate to provide significant protection to the living cells, which is the usual role of coccospheres (e.g., Young, 1994). Instead the honeycomb texture sacrifices robusticity to gain intended surface area in which the alveoli act as passive traps for drifting particles of food, possibly in combination with sheltered populations of symbiotic bacteria. If we recall that sphenoliths and fasciculiths possessed a central canal that permitted exchange between the cell within the coccosphere and seawater outside it, the coccosphere would have had sieve-like properties that enhanced the flow of seawater concentrated in dissolved nutrients (including perhaps ammonia from diazotroph cyanobacteria) towards the cell via the axial canal of the coccoliths while retaining food particles.

The Paleocene radiation of the Discoasterales has been interpreted as a response to oceanic oligotrophication that was initiated in the late Danian (Aubry, 1998a, Fuqua et al., 2008). Such features as fluted and honeycomb texture (Lithoptychius, Fasciculithus, Sphenoltihus), large size (Heliotrochus), diabolo-shapes (Diantholitha, Heliolithus), crateriform distal face (Gomphiolithus, Bomolithus, Heliolithus), and triades (Sphenolithus) were among many adaptive morphologies that were adaptations to life in warm oligotrophic waters through mixotrophic physiology. An increase in mixotrophic capabilities in the Family Fasciculithaceae can be reconstructed in the sequence from the crateriform fasciculiths of Gomphiolitus to the fluted fasciculiths of Lithoptychius to the honeycomb fasciculiths of Fasciculithus (text-fig. 19; see also Aubry, 2018). The most successful, if transient, functional morphologies are seen in successive radiations, such as those of Lithoptychius and Fasciculithus, when one genus or another achieved temporary dominance. In the Late Paleocene the appearance of large, rosette-shaped asteroliths marked a radical change in morphology, while their ornamentation in the form of numerous tiny dimples on their extensive flat surfaces served the same purpose as the honeycombs of their ancestors (see Aubry, 2015 a,b).

In conclusion, the available evidence suggest that adaptation in the Order Discoasterales to a mixotrophic physiology would have helped them achieve their dominance and success in the warm oligotrophic waters of the Cenozoic oceans.

We are only now beginning to fully understand the evolutionary history of the remarkably distinctive groups that make up the Order Discoasterales, and which give the order its outstanding role in global correlation of deep-sea deposits — its coccoliths, in fact, make up more than two-thirds of the species upon which the various Cenozoic coccolith biozones are based. It was possible for Prins (1971) to establish a zonal scheme for Upper Paleocene through Pliocene using only asteroliths, and the radiation of Lithoptychus (see above) provides one of the most widely and clearly recognizable markers in global chronostratigraphy (Schmitz et al., 2011). Many other equally impressive examples of the role of asteroliths in biostratigraphic research are reserved to the appropriate sections of this work.