Evolution and Geological Significance of Larger Benthic Foraminifera

1. Biology and history of larger benthic foraminiferaHistory and biological classification of foraminiferaEcology of the living larger foraminiferaPalaeontological and evolutionary history of the larger foraminiferaTaxanomic features used in larger foraminiferal classificationBiostratigraphic distribution over time of larger foaminiferaGeneral factors effecting the evolution of marine species in the mid to late Phanerozic2. The Palaeozoic larger benthic foraminifera: The Carboniferous and PermianMorphology and taxonomy of Palaeozoic larger benthic foraminiferaBiostratigraphy and phylogenetic evolutionPalaeoecology of the fusulinidsPalaeogeographic distribution of the fusulinids3. The Mesozoic larger benthic foraminifera: the TriassicMorphology and taxonomy of Triassic larger benthic foraminiferaBiostratigraphy and phylogenetic evolutionPalaeoecology of Triassic foraminiferaPalaeogeographic distribution of Triassic foraminifera4. The Mesozoic larger benthic foraminifera: the JurassicMorphology and taxonomy of Jurassic larger benthic foraminiferaBiostratigraphy and phylogenetic evolutionPalaeoecology of Jurassic foraminiferaPalaeogeographic distribution of Jurassic foraminifera5. The Mesozoic larger benthic foraminifera: the CretaceousMorphology and taxonomy of Cretaceous larger benthic foraminiferaBiostratigraphy and phylogenetic evolutionPalaeoecology of Cretaceous foraminiferaPalaeogeographic distribution of Cretaceous foraminifera6. The Palaeogene larger benthic foraminiferaMorphology and taxonomy of Palaeogene larger benthic foraminiferaBiostratigraphy and phylogenetic evolutionPalaeoecology of Palaeogene foraminiferaPalaeogeographic distribution of Palaeogene foraminifera7. The Neogene larger benthic foraminiferaMorphology and taxonomy Neogene larger benthic foraminiferaBiostratigraphy and phylogenetic evolutionPalaeoecology of Neogene foraminiferaPalaeogeographic distribution of Neogene foraminifera8. SynthesisImportance of application of larger foraminifera in biostratigraphyImportance of larger foraminifera as marine environmental indicatorsThe significance of the larger foraminifera assemblages in the understanding of the global distribution of carbonate sediments and their value in contributing raw data to palaeoenvironmental and palaeoclimatic modelsAppendixNomenclature terminology and glossary


Chapter 3
The Mesozoic Larger Benthic Foraminifera: The Triassic

Introduction
As seen in the previous chapter, the end of the Palaeozoic saw one of the most significant events in the history of life on Earth, with two mass extinctions occurring within a period of 10 Ma of each other (Kaiho et al., 2001;Chen and Benton, 2012).As a result of these events, about 90% of calcareous foraminiferal genera became extinct.The most affected were the large Fusulinida, which were wiped out.The only survivors of the Palaeozoic were a single member of each of the Endothyroidea and Earlandioidea superfamilies, which at that time were morphologically minute.In contrast, the extinction event had less impact on, for example, the simple Textulariida, which lost only 30% of its genera (Loeblich and Tappan, 1988).Forms from the Allogromiida, Miliolida and Lagenida also survived the end Permian extinction, albeit with significantly reduced diversity and as morphologically small forms.The Involutinida with aragonitic tests made their first appearance in the Triassic (Olenekian), persisting to the Early Cretaceous (Cenomanian).
In comparison with Permian larger benthic foraminifera, the Triassic larger foraminifera have not been systematically studied on a global scale.A revision of the taxonomy of the Early and Middle Triassic taxa was presented by Rettori (1995), Rigaud et al. (2015), and a stratigraphic summary of larger benthic foraminifera of the Tethyan realm was presented by Pybernes (in De Gracianski et al., 1998).The relationship between the microgranular Palaeozoic and agglutinated textulariides was explored by Rigaud et al. (2015).
In this chapter, the taxonomy of the main genera of the Triassic larger foraminifera is presented, and a number of revisions suggested.Although most of the Triassic foraminifera are relatively morphologically small they have complex internal structures that are distinguishable in thin section, and so for the purposes of this study they are considered as "larger foraminifera".Most of the superfamilies and families found in the Mesozoic are long ranging, but this chapter is only concerned with the genera characteristic of the Triassic.

Morphology and Taxonomy of Triassic Larger Benthic Foraminifera
The Triassic larger forms are found developed in six orders: The development and evolution of the superfamilies of these orders is schematically shown in Fig. 3.1.Below, are presented the morphological characteristics and taxonomic relationships of the major Triassic forms, while in the next section their biostratigraphic significance and their phylogenetic relations are discussed.

ORDER TEXTULARIIDA Delage and Hérouard, 1896
The tests of these agglutinated foraminifera are made of foreign particles bound by organic cement.They range from Early Cambrian to Holocene.

Superfamily AMMODISCOIDEA Reuss, 1862
The test is sub-spherical or tubular, with an aperture at the end of a tube.Cambrian to Holocene

Family Ammodiscidae Reuss, 1862
Members of this family have a proloculus that is followed by an uncoiled non-septate tubular second chamber.Early Cambrian to Holocene.
The initial coiling is the same as Pilammina, then the second chamber changes 90 o to the plane of coiling, followed by two or three oscillating coils.Middle to Late Triassic (Anisian to Carnian).

Superfamily ATAXOPHRAGMIOIDEA Schwager, 1877
Members of this superfamily have a multilocular, trochospiral test becoming biserial or uniserial in later stages.Middle Triassic to Holocene.

Family Ataxophragmiidae Schwager, 1877
Members of this family have three or more chambers per whorl in the early stages.The aperture is high and terminal.Late Triassic to Palaeocene.

Superfamily LOFTUSIOIDEA Bradey, 1884
The test is planispiral, may uncoil in later stage.The wall is agglutinated with differentiated outer layer and inner alveolar layer.Late Triassic (Carnian) to Holocene.

Family Mesoendothyridae Voloshinova in Bykova et al., 1958
The test is strepto-or planispirally coiled, has involute initial chambers, and later is uncoiled.Adult chambers are cylindrical or flattened, falciform to cyclical.They are simple, with radial partitions or with pillars.Walls may have alveoles or a hypodermic network.Late Triassic (?Carnian to early Norian).

Family Lituolidae de Blainville, 1827
The early stages of the tests are enrolled, but later they may become rectilinear.Walls are formed from agglutinated foreign particles.There are few chambers (less than 10) per whorl.Carboniferous to Holocene.

Subfamily Ammomarginulininae Podobina, 1978
The early stage of the test is coiled, but it becomes uncoiled in later stages.Apertures are single.Carboniferous (Early Mississippian) to Holocene.

Subfamily Lituolinae de Blainville, 1827
Members differs from Ammomarginulininae in having multiple apertures.Late Triassic to Holocene.

Superfamily COSCINOPHRAGMATOIDEA Thalmann, 1951
Members of this superfamily are attached and may be coiled in their early stages, but later are uncoiled or branched.Triassic to Holocene.

Family Coscinophragmatidae Thalmann, 1951
The wall is canaliculated, and perforated with alveoles.Late Triassic to Holocene.

Family Piallinidae Rettori, Zaninetti in Rettori et al., 1993
The test is multilocular and elongated, with a proloculus followed by a trochospiral development, or with a small streptospiral in the early stage followed by a high trochospire in the later stage.Late Triassic (Carnian).

ORDER LAGENIDA Delage and Hérouard, 1896
This order is characterised by having monolamellar walls, composed of low-Mg calcite in which the optical c-axes of the crystal units are perpendicular to the outer surface of the test.Primitive taxa are without secondary lamination, but more advanced forms are found with secondary lamination and a thin microgranular inner layer (see special terminology defined in Chapter 2).They range from Late Silurian to Holocene.
The test is trochospirally coiled, with pillars filling the umbilical region.Triassic (Carnian).

Superfamily GEINITZINOIDEA Bozorgnia, 1973
The tests of this superfamily are uniserial, and similar to the Palaeozoic form Nodosinelloidea, but the microgranular layer is the inner dark layer, while the radially fibrous layer is the outer layer.Late Devonian to Middle Triassic.

Superfamily EARLANDIOIDEA Cummings, 1955
This superfamily is characterised by having a free, non-septate test with a globular first chamber followed by a straight tubular one.It ranges from the Late Silurian to Early Triassic.

Family Earlandiidae Cummings, 1955
The Earlandiidae have a single free chamber and range from the Late Silurian to Early Triassic.

ORDER MILIOLIDA Delage and Hérouard, 1896
The miliolides have tests that are porcelaneous and imperforate, made of high Mgcalcite with fine, randomly oriented crystals.They range from the Carboniferous to the Holocene.

Superfamily CORNUSPIROIDEA Schultze, 1854
The test is free or attached, and composed of a globular proloculus followed by a tubular enrolled chamber.chamber.The coiling is planispiral throughout and involute, with a lamellar umbonal region on each side of the test.Early to Middle Triassic (Induan to Anisian, ?earlyLadinian) (Fig. 3.5).• Paratriasina He, 1980 (Type species: Paratriasina jiangyouensis He, 1980).The test is planispiral, involute with a possibly irregular central area.Internal pillars may be present.The wall is porcelaneous.Early whorls show short zigzag bends as in Meandrospira Loeblich and Tappan, followed by later planispiral developments.Triassic (lattermost Anisian to early Ladinian) (Fig. 3.5).

Family Cornuspiridae Schultze, 1854
The tests are free or attached, composed of a proloculus followed by an undivided planispiral to streptospiral, involute or evolute second tubular chamber.Early Carboniferous (Visean) to Holocene.

Family Hemigordiopsidae Nikitina, 1969
These forms are found with a test that has at least an early streptospiral stage, that later may be planispiral.Early Carboniferous (Visean) to Holocene.

Family Hoynellidae Rettori, 1994
A free test, with a globular proloculus followed by an early miliolid stage and an undivided tubular chamber arranged on several vertical planes.Triassic to ?Early Jurassic.

Superfamily SORITOIDEA Ehrenberg, 1839
These forms have chambers that are planispiral, uncoiling, flabelliform or cyclical, and may be subdivided by partitions or pillars.Late Permian to Holocene.

Family Milioliporidae Brönnimann and Zaninetti, 1971
The tests are free or attached with a proloculus and tubular chambers arranged in various planes of coiling, which may be irregular, oscillating, or sigmoidal.Late Permian to Late Triassic (Rhaetian).

ORDER INVOLUTINIDA HOHENEGGER AND PILLER, 1977
This order includes all forms with an enrolled second chamber.They have walls that are aragonitic, but commonly they are recrystallised to give a homogeneous microgranular structure.They have an umbilical region with pillar-like structures on one or both sides of the test.They range from Triassic to Cretaceous.

Superfamily INVOLUTINOIDEA Bütschi, 1880
These forms consist of a first chamber, followed by a planispiral to trochospiral enrolled tubular second chamber.Originally thought to date from Early Permian (Loeblich and Tappan, 1988;BouDagher-Fadel, 2008), but here defined from Triassic to Late Cretaceous (Cenomanian).

Family Triadodiscidae Zaninetti, 1984
The umbilical area is covered with additional lamellae added with each new whorl.Early Triassic to Late Triassic (Olenekian to Carnian).

Family Aulotortidae Zaninetti, 1984
These forms have a lenticular to conical test with calcareous imperforate walls, and consist of a globular proloculus followed by a tubular, enrolled and undivided second chamber, lying against the previous whorl to form planispiral, oscillating or trochospiral coiling.Each half whorl is followed by the lamellar deposition of one or two layers.The aperture is at the open end of the tubular chamber.Triassic (Anisian) to Middle Jurassic.
The second chamber is trochospirally enrolled and tubular.Each half whorl forms a lumina that covers the umbilicus, resulting in the build-up of a thick and solid umbilical filling.

Family Triasinidae Loeblich and Tappan, 1986
The tests have a proloculus, followed by a broad tubular chamber.The interior is filled with cylindrical pillars.Triassic (Ladinian to Rhaetian).

Family Involutinidae Bütschli, 1880
The globular proloculus is followed by a trochospiral coiled tubular second chamber.

General Biostratigraphy
The Permian-Triassic transition represents a critical period in foraminiferal evolutionary history.Without question, the end Permian extinction resulted in the greatest reduction of biodiversity in Earth history, claiming roughly 85 percent of all genera then in existence (Erwin et al., 2002;Chen and Benton, 2012).The dominant Palaeozoic order, Fusulinida, was eliminated, while diversity within the Lagenida, Miliolida and Textulariida declined by 30, 50, and 80 percent respectively.As discussed in Chap.2, the true Involutinida appeared as new forms in the Triassic.
The end Permian mass extinction, and the following survival and recovery intervals, resulted in a dramatic turnover in the taxonomic composition of calcareous benthic assemblages (Groves and Altiner, 2004).During the Early Triassic, shallow marine foraminifera were simple and rare, with the first recorded forms appearing in the eastern Palaeo-Tethyan realm (Sweet et al. 1992;Márquez, 2005), resulting elsewhere in a taphonomically induced gap in the understanding of the transition of the Permian survivors (Groves, 2000).They were initially dominated by small arenaceous forms (Tong and Shi, 2000).These are the "disaster forms" which are, as defined by Fischer and Arthur (1977), 'opportunistic species in the sense of MacArthur (1955) and Levinton (1970), and characteristic of the survival phase following a mass extinction (Hallam and Wignall, 1997).The subsequent disappearance of such forms, along with the proliferation of the survivors and the reappearance of 'Lazarus taxa', marks the beginning of the recovery phase in the Ladinian (Groves and Altiner, 2004).The recovered forms seem to be dominated by the miliolides and later by the involutides in the Eastern Tethys area.
The larger benthic foraminifera in the Early and Middle Triassic evolved slowly, and it was not till the Ladinian stage that highly diversified communities, such as the Ammodiscoidea and the Endothyroidea thrived.Among the most evolved foraminifera along with these communities are the Involutinida, such as Lamelliconus which became diverse and common in the Norian to the Rhaetian.Towards the end of the Triassic a gradual decline of the larger benthic foraminifera groups occurred, which climaxed with an end Triassic mass extinction event (Tanner et al., 2004), where most remaining larger benthic foraminifera disappeared.The biostratigraphic range of the main Triassic forms are summarized in Fig. 3.7.

The Palaeozoic-Triassic Lagenides
One of the most important groups which survived the Permian extinction was the lagenides.Early Triassic lagenides are direct descendants of Permian forms and  , 1998) and in previous analyses of foraminiferal diversity across the P-T boundary, a number of lagenides genera were also regarded as either belonging to the Fusulinida or Rotaliida.In our modification of the phylogenetic of the Carboniferous forms, we would suggest that they may have indeed derived from the Earlandiida.However, more recent work (Groves et al., 2003(Groves et al., , 2004) ) 2004) and Grove (2005) divided the lagenides, at the highest level, into nonseptate and septate taxa.Within the nonseptate group there are forms whose tubular second chamber is unpartitioned (e.g.Syzrania, see Chapter 2), and forms whose second chamber is partitioned, to varying degrees, by constrictions or thickenings of the wall (e.g.Tezaquina, (Fig. 3.2); see also Chapter 2).Within the septate group there are uniserial (e.g.Nodosinelloides, see Fig. 3.2) and coiled forms (Calvezina, see Chapter 2).The uniserial forms are further differentiated on the basis of chamber symmetry when seen in transverse section: i.e., radial circular (Nodosinelloides); radial bilateral flattened (Geinitzina); triangular (Pseudotristix); and polygonal (Rectostipulina).The phylogenetic evolution of the lagenides, as shown in Fig. 3.2, follows a morphological trend varying from uniserial tubular, non-septate forms to uniserial septate forms with rounded transverse section which become flattened and flaring in advanced forms.
The Moscovian-Kasimovian interval of the Carboniferous saw the initial evolutionary radiation of the early complex lagenides with the oldest known genus Syzrania, which as indicated above might have evolved from the Earlandioidea (Earlandia) in the Middle Pennsylvanian (see Figs 3.1 and 3.2), through the addition of a hyaline-radial layer external to the ancestral microgranular wall (Groves et al., 2004).This is shown in the earliest species of Syzrania where the wall was still dominantly microgranular with only an incipiently developed hyaline-radial layer (Fig. 3.2).The Syzranidae evolved in the Late Pennsylvanian and Permian into sub-septate and fully septate uniserial forms.In the late Ghzelian, the ancestor to all laterally compressed early lagenides, Geinitzina, made its first appearance, but it was not until the late Sakmarian that the Pachyphloia -Howchinella group finally developed.
The Late Permian (Lopingian) lagenides were diverse and abundant throughout the Tethyan region and northern higher paleolatitudes, filling the niches that became vacant after the larger fusulinides became extinct.Among these lagenides were the compressed forms Geinitzina, Pachyphloia, Nodosinelloides, Protonodosaria and Robuloides.
However, Early Triassic (Induan and Olenekian) rocks contain very few lagenides.These Early Triassic lagenides are morphologically simple forms, so-called "disaster forms".It was not until the late Anisian that true recovery really began, with the reappearance of more evolved Permian-like features, such as the laterally compressed test and the subdivided chambers, with radiate or modified apertures and secondary lamellarity of the wall (e.g.Grillina, see Fig. 3.3).The reappearance of these Permian features in the later Triassic and younger taxa is attributed to evolutionary morphological convergence (Groves et al., 2004).Indeed, this convergence almost certainly accounts for the many examples of so called "Elvis taxa" (Erwin and Droser, 1993) among Palaeozoic and Mesozoic-Cenozoic forms.

The Triassic Earlandiida and Endothyrida
As discussed in Chapter 2, the initial decline of the fusulinides coincided with the end Guadalupian in the Late Permian.This crisis event eliminated all large and morphologically complex forms of fusulinides, and by the end of the Permian all fusulinides were extinct.Indeed, only two genera (Earlandia, Endoteba), from the earlandiides and the endothyrides respectively, survived the end Permian mass extinction (Fig. 3.4), but they never experienced significant taxonomic recovery (Groves and Altiner, 2004).The Endotebidae have their origin in the Permian where they evolved from the true Endothyridae.The type species Endoteba controversa Vachard and Razgallah, 1988 is known from Late Permian rocks in Tunisia, Yugoslavia, Italy, Afghanistan and Japan.However, according to Vachard et al. (1993) the Triassic occurrence of this genus is known mainly from the Anisian to Ladinian.They are very rare in the Carnian and Rhaetian throughout the Tethyan realm, with the only documented Early Triassic (Olenekian) occurrence being that of E. ex gr.bithynica Vachard et al., 1993.Endoteba is regarded as a Lazarus taxon, as no known Induan occurrences have been documented to date.A slight increase in the number of genera characterized the Middle Triassic, there being five genera but with no more than ten species in all.In Tethys, Endoteba evolved into three genera or species-groups, Endotebanella (uppermost Olenekian through Carnian), Endotriada (Middle Triassic), and Endotriadella (Middle Triassic).The endothyrides became entirely extinct in the Late Triassic, while the earlandiides died out within the Early Triassic (see Fig. 3.4).Earlandia have been suggested as having survived into the Early Cretaceous, but this has not been confirmed (Arnaud-Vanneau, 1980;Vachard et al., 2010).

The Triassic Miliolides
Foraminifera in the order Miliolida first made their appearance at the beginning of the Carboniferous (Ross and Ross, 1991).Analysis by Flakowski et al. (2005) of SSU (small sub-unit) rRNA genes showed that the miliolides cluster with the calcareous Spirillinidae and agglutinated Ammodiscidae in an independent, fast evolving lineage (Pawlowski et al., 2003).This suggests that miliolides evolved directly from some allogromiide-like ancestor, which is consistent with earlier morphological observations (Arnold, 1978).This was subsequently questioned by Gaillot and Vachard (2007) and Vachard et al. (2010).The latter argued that the early attached miliolides derived probably from the attached Tournayellida and not from the Ammodiscidae, which are homeomorph of the Tournayellida.The question is still open, but in Although the miliolides proliferated during Middle and Late Permian, the end Permian extinction nearly eliminated the order, as almost all species disappeared.However, a few minute disaster forms survived the extinction, and forms such as Cornuspira and Rectocornuspira (see Chapter 2) are found in the Induan, apparently because of their tolerance of environmental stress (Grove and Altiner, 2004).Indeed, the middle Induan is zoned on the occurrence of R. kahlori by many authors, such as de Graciansky et al. (1998).
Like other forms, the miliolides were rare in the Early Triassic.The appearance of Meandrospira in the Olenekian represented a probable continuation of the Permian form assigned to Streblospira (which is according to Loeblich and Tappan is a synonym to Meandrospira), and is considered by Groves and Altiner (2004) as a Lazarus taxon.The late Olenekian of Tethys is zoned by M. pusilla (de Graciansky et al., 1998), and it was not before the middle Anisian that Meandrospira expanded, and subsequently evolved into forms such as Meandrospiranella and Turriglomina in the late Anisian.The appearance of the latter coincided with the disappearance of the Meandrospira species group from Tethys at the end of the Anisian.
A parallel evolution to that of Meandrospira (= Streblospira) also took place (according to Zaninetti et al., 1991, andRettori, 1995) in the Neohemigordius -Arenovidalina lineage.Neohemigordius in the Early Permian loses its prominent umbilical thickening and acquires a streptospiral early coil as is in Hemigordius and its species group of the Permian.The Hemigordius group disappears in the Late Permian.However, similar forms to Hemigordius, but with planispiral tests and thickening in the umbilical region, as in Neohemigordius, and referred to as Arenovidalina, reappear in the Olenekian.Arenovidalina could be regarded as a Lazarus taxon that gave rise, just before disappearing in the early Ladinian, but giving rise to the Mesozoic group ophthalmidiids, by losing the lamellar umbonal region on each side of the test and developing a streptospiral early coil with much irregular later coiling.The tubular undivided planispiral second chamber of Arenovidalina becomes subdivided into distinct chambers in Ophthalmidium.Another short lineage also to develop from Arenovidalina in the late Anisian is that of Paratriasina, with a streptospiral early coil that later becomes planispiral.This phylogenetic evolution is shown schematically in Fig. 3.5.

The Triassic Involutinides
The Early Triassic witnessed the first appearance of the aragonitic involutinides (older texts such as Loeblich and Tappan (1988) identify them as originating in the Permian, but this is based on the erroneous classification of the porcelaneous genera Neohemigordius (Fig. 3.5) and Pseudovidalina as involutinides rather than miliolides, see Chapter 2).The order Involutinida includes all forms with an enrolled second chamber and pillar-like structures in the umbilical region on one or both sides of the test (see Fig. 3.6).The oldest Triassic representative of the group is Triadodiscus, which first appeared abruptly in the Olenekian with no known occurrences in the Induan.The ancestor of Triadodiscus is still unknown.
One of the common hypothesis is that involutinides had an Archaediscoidean origin (Groves and Altiner, 2004).However, Archaediscoidean forms were confined to the Palaeozoic and were never recorded in the Triassic.Gargouri and Vachard (1988) proposed the ammodiscoides Glomospirella as being a possible ancestor, but other authors favoured a hemigordiopsid Multidiscus ancestor (Altiner et al., 2005).However, Multidiscus is not definitely known from the earliest Triassic.Furthermore, rDNA analyses suggest a significant genetic and evolutionary separation between miliolids and other testate foraminifera (Pawloski, 2000), which would mitigate against this proposal.
In the Anisian, the planispirally coiled Triadodiscus evolved into streptospirally coiled Aulotortus (see Fig.  2013) who demonstrated that trochospirally coiled involutinides are a separate group.On the other hand, Involutina is planispiral-evolute, non-septate, perforate, and possess at least two laminae per whorl, that are, as in Aulotortus, interfingered in the median part of the umbilical region (Rigaud et al., 2015).It was also postulated that Involutina evolved from Triadodiscus (Piller, 1978;Gaździcki, 1983;di Bari and Laghi, 1994)

Palaeoecology of the Triassic Larger Foraminifera
The Triassic saw the single vast super-continent of Pangea straddling the equator, with the Tethys Ocean intruding into Pangea from the east, leading to the division between Laurasia in the North and Gondwana in the South.Land animals were free to migrate from Pole to Pole (Fig. 3.9).The interior of Pangea was hot and for the most part dry and very arid.Warm temperate climates extended to the poles.Sea levels were low and the seas had little or no dissolved oxygen and were possibly alkaline (Woods, 2005).
Rapid global warming at the very end of the Permian expanded the deserts and created a "super-hothouse" world, that may have contributed to or exacerbated the great Permian-Triassic extinction.The carbon dioxide content of the atmosphere was very high and the level of atmospheric oxygen was unusually low (Berner et al., 2003), see Fig. 3.10 The end Permian extinction led to a profound decline in reef production and caused the near-total elimination of metazoan reef systems (Hallam and Wignall, 1997), giving rise to a so-called "reef gap" (Fagerstrom, 1987;Flügel, 1994) during the Induan and early Olenekian.Recovery was very slow for foraminifera, and ecological recovery was delayed until the middle Olenekian.The start of the Triassic was characterised by extremely impoverished taxa, dominated by opportunists and generalists (Rodland and Bottjer, 2001).Many genera which seemed to have disappeared at the Palaeozoic-Mesozoic boundary remained hidden, possibly in geographically restricted environments, before returning as "Lazarus" taxa in the Olenekian or Middle to Late Triassic.Loeblich and Tappan (1988) suggested that the morphologies of the surviving faunas are characteristic of infaunal detrital feeders, which would have been therefore less susceptible to primary productivity crashes, in contrast to the larger benthic foraminifera which lived symbiotically in reefal environments.On the other hand, Chen and Benton (2012) postulated that recovery of complex life in the Triassic could have been delayed either by a complex multispecies interaction combined with physical perturbations.
It was not before the Anisian that larger benthic foraminifera became more widespread and cosmopolitan.During this time, a tropical sea formed between the supercontinents of Gondwana (in the south) and Laurasia (in the north).This sea, called the Tethys (Fig 3.9), became home to large diverse assemblages of foraminifera.However, the larger Triassic benthic foraminifera never recovered the relatively gigantic sizes seen in the Permian, but rather remained small and indistinctive.This was caused most probably by the drop in atmospheric and marine oxygen levels at the Permian-Triassic boundary (Berner et al., 2003), see Fig. 3.10.Increasing atmospheric oxygen levels have, for example, been implicated in the rise of late pre-Cambrian and Cambrian marine faunas (Cloud, 1976;Runnegar, 1982;McMenamin and McMenamin, 1990) and are consistent with the presence of Permian-Carboniferous giant insects.Similarly, anoxia has been regularly correlated with the dramatic Permian-Triassic extinction events in the ocean and the small size of the larger foraminifera during the Triassic (Erwin, 1993;Knoll et al., 1996;Wignall and Twitchett, 1996).In the oceans today, many benthic invertebrates compensate for hypoxic conditions via a broad spectrum of behavioural Trias. 251.9 Pem. 298.9 Carb. 358.9 Dev.

485.4
Cambrian High level of oxygen enables large sizes to be achieved.
Low level of oxygen inhibits the development of large forms.
Atmosphere oxygen levels % Fig. 3.10.Oxygen variation over time, highlighting the low level of oxygen during Triassic time (modified after Berner et al., 2003).
and morphological adaptations (Rogers, 2000).Similarly, infaunal penetration by the foraminifera may be a response to deplete sediment oxygenation in the Triassic (Berner et al., 2003).
During the Anisian, carbonate platform development reoccurred with the important contribution of reefal debris, which as noted above are almost totally absent in Early Triassic carbonate platforms.This was accompanied by the appearance of scleractinian corals and the increasing importance of dasycladoidean green algae (e.g.Griphoporella sp., Plate 3.1, fig.9), the increasing frequency of crinoids and molluscs, and the scarcity of ooids (Kiessling et al., 2003).During the Ladinian there was a clear stabilization of marine ecosystems, accompanied by the development of wide carbonate platforms bearing highly diversified communities (Márquez and Trifonova, 2000;Márquez, 2005).
The climate in the Carnian was unusually arid and hot and the seaway itself appears to have experienced a "salinity crisis" (general evaporation) and a breakdown of the reef system.In the Carnian, foraminiferal assemblages were dominated by endothyrides and miliolides .The Late Carnian-Norian interval saw major reef extinctions in the Tethys province, with the loss of older coral species, but diversity was maintained with reciprocal replacement by new taxa (Stanley, 2001).These in turn became extinct, possibly a result of a sudden global cooling.This is mirrored by the disappearance of many foraminiferal genera in western Tethys, which were subsequently replaced by new forms of Involutinida in the Norian.The early Norian Tethyan reef systems were replaced by much larger reef developments during the Late Triassic (mid Norian to Rhaetian) coinciding with a major rise in global sea-level.At this time the new foraminiferal taxa of Involutinida became dominant and corals diversified, constituting a new reef building consortium.There was a period of world-wide expansion of carbonate platforms and maximum reef diversity (Stanley, 2003).Associations of Late Triassic benthic foraminifera dominated by Ammodiscoidea, Involutinoidea, and Duostominoidea are mainly found in shallow marine facies, often restricted and ecologically highly unstable (Márquez, 2005).They are generally typical of low energy, bay or lagoon-type, protected settings, with a salinity sometimes higher than normal, on shallow carbonate ramps.The different reef facies include forms common to the Tethys such as Triadodiscus mesotriasica (Koehn-Zaninetti), Palaeolituonella meridionalis (Luperto), Endoteba wirzi (Koehn-Zaninetti), Duostomina alta Kristan-Tollmann and D. astrofimbriata Fuchs, to mention a few.In these reef environments, the foraminiferal fauna are more numerous and diverse than in the restricted carbonate ramps of the Triassic basins (Márquez, 2005).Many of the Late Triassic species have morphological characteristics, such as the irregularly distributed papillose lamellae and tube infolding of Involutina, which have been interpreted as being rudimentary features associated with photosymbiosis (Rigaud et al., 2015), typically developed in shallow, high-energy tropical carbonate platforms (Martini et al., 2009).

Palaeogeographic Distribution of the Triassic Larger Foraminifera
The Early Triassic was characterised by small and low-diversity taxa, and is viewed as a time of delayed biotic recovery that persisted until the Middle Triassic (Hallam, 1991;Galfetti et al., 2008;Chen and Benton, 2012).Explanations for this vary from invoking the sheer scale of the Permian extinction to the prolonged stresses of the environment post end-Permian extinction (Hallam, 1991;Payne et al., 2004;Chen and Benton, 2012), or the effects of further extinction crises in the Early Triassic (Orchard, 2007;Stanley, 2009;Song et al., 2011).
The Early Triassic larger benthic recovery shows roughly the same trajectory everywhere.The foraminifera were mainly small, and they followed the model of the "Lilliput effect" described by Urbanek (1993), where he refers to the pattern of size change through extinction events, specifically the temporary appearance of dwarfish organisms (Twitchett, 2006).There was a significant decrease in maximum and mean size among species and genera across the Permian/ Triassic boundary.This was followed by gradual size increase through the late Induan and into Olenekian.The recovery of reef-building larger benthic foraminifera began 4 Ma later, in the Anisian, but they never recovered the pre-extinction sizes of the Permian (Payne et al., 2011;Song et al., 2011;Rego et al., 2012).The anoxia and global warming that prevailed through the Permian-Triassic period may have contributed to this "Lilliput effect" on larger benthic foraminifera in the aftermath of the end-Permian crisis.
The distribution of the Triassic genera is plotted in charts (see Figs 3.11 to 3.13) in order to understand their palaeogeographic distribution.The genera are divided into three provinces: Europe and Russia, China and East Asia, and North America.There is a general and progressive increase in diversity from the Induan to the Anisian, with the end Olenekian being marked by the increase in the number of orders that exhibit larger morphologies.A possible minor extinction event occurred at the end of the Anisian affecting the Ammodiscoidea in Europe.The ancestor of the Involutinida appeared in all the three provinces, and the order increased in diversity in China and East Asia during the Ladinian, but it was not before the Norian that they became widespread in Europe.The Endothyroidea were common during the Anisian and Ladinian in China, East Asia and Europe, but they decreased gradually toward the end of the Norian.However, they did not disappear completely from these provinces until the end of the Rhaetian.From Fig. 3.11, it can be seen that throughout the Triassic, the diversity in North America was constantly low, but there was a distinct increase in the number of genera throughout Europe, and to a lesser extent in China and East Asia, in the Anisian and Norian.From Fig. 3.12, we see that there was a sharp decline in speciation in the Ladinian, and that no new forms appeared at all in the Rhaetian.However, during the Anisian and the Norian the larger benthic foraminifera speciation was at its most productive.North American foraminifera speciation mirrored generic diversity but remained poor throughout the Triassic.There was a gradual increase in the number of extinctions from the Ladinian to the Carnian in all three provinces, that was followed by a large extinction event at the end of the Rhaetian (Fig. 3.13).
The trends described above in all three provinces, can be understood to some extent from an analysis of the palaeogeography of the Triassic.After the great extinction of the end Permian, foraminifera were struggling to survive during the Induan interval.The recovery process was very slow in the Induan, but new forms were appearing, 80 % of the Induan foraminifera were new Triassic forms with the first records of foraminifera appearing in the eastern Tethys area (China) and Eastern Europe.They are dominated by opportunist, euryfacial forms, giving rise to associations that are sometimes numerous but of low species diversity, since they are mostly comprised of arenaceous genera (Tong and Shi, 2000) from the Ammodiscoidea (see Fig. North America having the least diversity.This is probably due to its relative isolation during the Early Triassic (see Fig. 3.9).
The Anisian saw the highest number of new genera in the Triassic (see Fig. 3.12).However, at the end of the Anisian a small extinction occurred, mostly among European Ammodiscoidea (affecting 35% of the genera), and within the Ladinian, 60% of the Cornuspiroidea from all three provinces disappeared.This may have been associated with environmental stress caused by the large volcanic event (ca.235 Ma) along the northwest margin of North America, and which formed the Wrangellia Terrane.After this event, the foraminifera in North America and Europe did not recover completely until the end of the Carnian.The Far East seems not to have been affected by this event.The Wrangellia volcanic sequences were oceanic events, and so may not have had the same globally devastating environmental and climatic effects inferred to be associated with sub-aerial volcanic eruptions (e.g. the Siberian Traps).
At the end of the Ladinian, there was a general decline in speciation after the blooming of the Early Triassic recovery, except after the end Carnian event which saw the expansion in the Norian of the superfamily Involutinida in European Tethys.The ancestral form of this family appeared in the Anisian, but only attained importance in the Norian and Rhaetian.In addition, the first forms of Lamelliconus emerged in the Ladinian, a genus that was to develop substantially during the Norian.The miliolide genus Turriglomina, which developed during the Anisian, gave rise to many species of stratigraphic significance, such as T. conica (He), T. mesotriasica (Koehn-Zaninetti) and T. scandonei (Zaninetti, Ciarapica, Martini, Salvini-Bonard and Rettori).The species Palaeolituonella meridionalis (Luperto), widely cited for the Middle Triassic from several Tethyan localities, is especially common in the Ladinian (Trifonova, 1992;Márquez, 2005).
Early Carnian Triassic foraminifera had become cosmopolitan, as a small seaway connected the Tethys Ocean with North America (see Fig. 3.14).Foraminifera thrived until the end of the Carnian.The high number of extinctions at the end of the Carnian coincide with the occurrence of set of multiple of impacts (Spray et al., 1998).Five terrestrial impact structures have been found to possess comparable ages (214+/ -2 Ma), close to Carnian-Norian boundary (see Fig. 3.15).These craters are Rochechouart (France), Manicouagan and Saint Martin (Canada), Obolon (Ukraine) and Red Wing (USA).These five large, chronologically-close impact events might have triggered adverse ecological changes that in turn might have led to the high extinction rates observed.
However, foraminifera were soon again to recover (see Fig. 3.12), with new forms filling the empty niches.The Norian saw the expansion of the Involutinida in European Tethys.The Late Triassic also witnessed the appearance in the West Pangean reefs of reportedly Permian Lazarus taxa (Stanley, 2001).Presumably these forms had remained rare and geographically isolated during most of Triassic time.Panthalassan volcanic islands might have served as refuges during time of crisis when the Tethys was affected (Stanley, 2003), and probably middle Norian conditions were similar to those of the Permian.During the Rhaetian, foraminiferal diversity in all provinces dwindled gradually to near full extinctions in the three provinces (Tanner et al., 2004;Scherreiks et al., 2010).These extinctions mirror the abrupt extinction seen for all other groups in the marine realm at the end of the Triassic.This Triassic-Jurassic extinction is generally recognized as being one of the five largest in the Phaenorozoic (Hallam, 1990).Only 16% of the Triassic foraminifera survived the end Triassic extinction.There has been much speculation as to the cause of this extinction event, and debate as to whether there was a catastrophic event at the end of the Triassic, or if it was preceded by a gradual decline.Certainly, a gradual decline of the foraminifera (see Fig. 3.12) was apparent.According to Tanner et al. (2004) the Late Triassic extinction appears protracted rather than catastrophic.Marine regression reduced the available shallow marine habitats for the Triassic foraminifera, and consequent competition may have been the forcing mechanism for extinction (Newell, 1967).Tucker and Benton (1982) specifically cited climate-induced changes occurring during the Late Triassic as a possible cause for mass extinction.Evidence of anoxia has also been documented in Triassic-Jurassic sections and has been suggested to be a significant factor in this event (Hallam and Wignall, 1997;2000).closely associated with the end-Triassic extinction (Bonis et al., 2009;Whiteside et al., 2010;Schoene et al. 2010;Ruhl et al., 2011;Macleod, 2013;Blackburn et al., 2013;Percival et al., 2017), andspecifically Deenen et al., (2010) claim that the extinction of the larger benthic foraminiferal correlate well with the detail timing of the CAMP eruptions.
Thus, it would seem that a globally significant volcanic event at the end of the Triassic saw another catastrophic decline in larger foraminiferal assemblages and their associated corals.This, as will be seen in Chapter 4, was followed by the now familiar trend of a "reef gap" in the Early Jurassic.
Fig. 3.1.The evolution of the Triassic larger benthic foraminifer orders and superfamilies.
Fig. 3.2.The phylogenetic development of the lagenides through the Palaeozoic and Triassic (sections of some lagenides are modified from Sellier de Civrieux and Dessauvagie, 1965).
Fig. 3.3.A schematic figure showing the convergence of lagenides features in the Late Permian and the Late Triassic forms.
Fig. 3.6.Evolutionary lineages of the main genera of the Involutinida.(drawings of foraminifera are not to scale).
suggests that the order Lagenida is monophyletic.Authors, such as Palmieri (1983), Groves and Wahlman (1997), Pinard and Mamet (1998), Groves (2000) and Groves et al. (2004), suggested there were very close similarities in wall structures between Palaeozoic and Mesozoic-Cenozoic lagenides, with no change in wall structure at the Permian-Triassic boundary.If so, the Triassic Robuloidoidea would have had its origins in the Parathuramminida (see Fig 3.1).This is still an unresolved issue.Studies by Grove et al. ( Fig 2.1 and 3.1 they are shown as having an allogromiide-like ancestor.
3.6).The late Ladinian of Tethys is recognised (de Graciansky et al., 1998) by the appearance of A. praegaschei (Koehn-Zaninetti).However, it was not before the Norian that significant diversification occurred, with changes in the shape of the coiled tests and the shape and occurrences of pillars.Several evolutionary trends in the involutinides occurred from Middle to Late Triassic, which are biostratigraphically useful.The Norian and Rhaetian are zoned using Triasina oberhauseri and T. hantkeni (Plate 3.4, fig.12) respectively.The development of Involutina (see Figs 3.6; 3.8) has been debated by many authors.Kristan-Tollman (1963) proposed a direct development from the trochospiral Lamelliconus.However, this theory was refuted by Rigaud et al. ( Fig. 3.8.Sections of Involutina sp., A) Schematic axial section: B) Photomicrograph of an Axial section.
Fig. 3.11.The number of larger benthic foraminifera genera found throughout the Triassic in the three main palaeogeographic provinces.
Fig. 3.13.The number of larger benthic foraminifera genera extinctions occurring throughout the Triassic.

Fig. 3
Fig. 3.16.A map showing the location of the end Triassic Central Atlantic Magmatic Province (CAMP).

•
Wernlina Rigaud et al., 2014 (Type species: Wernlina reidae Rigaud et al., 2014).The test is symmetrical and planispirally coiled.The wall is dark, thick and microgranular, formed by an inner alveolar layer sealed by an outer imperforate layer.The septa are thick and non-alveolar.The aperture is single and basal.Rigaud et al (2014) included in Wernlina, the species Everticyclammina praevirgulina described and illustrated from the Sinemurian-early Pliensbachian of Spain byBouDagher- Fadel and Bosence (2007, pl. 3, fig.6).However, the latter differs from typical Wernlina in having an initial streptospiral coiling, fewer and proportionally thicker chamber walls and septa (see Chapter 4).Late Triassic (?late Carnian to early Norian).
Superfamily LITUOLOIDEA de Blainville, 1825Members of this superfamily have a conical, multilocular, rectilinear and uniserial test.The early stage has plani-(strepto-) or trochospiral coiling.The periphery of the chambers has radial partitions; but centrally they are with or without scattered, separated pillars.The septa are arched into hummocks (almost solid masses) between the apertures, with bases of the arches that can fuse to the hummocks of the previous septum, with the apertures then opening at the suture.The alignment of the apertures and thickening of the hummock walls produces the appearance of a series of "gutters".No true pillars are formed.The walls are solid, non-alveolar, non-canaliculate.The aperture is simple, with no internal tooth plates, areal or multiple, cribrate.Late Triassic (Carnian) to Holocene.
Representatives of this superfamily have a trochospiral test throughout, or only in the early stage.They may be triserial, biserial or uniserial.Some forms have a streptospiral initial part.The aperture is single or multiple.Late Carboniferous to Holocene.

ORDER EARLANDIIDA SABIROV IN VDOVENKO ET AL., 1993 EMEND. VACHARD ET AL., 2010 This
order has simple, free or attached tests, consisting of a proloculus and a rectilinear second chamber.The aperture is terminal and simple.Late Silurian to Early Cretaceous.

Family Endotriadidae Vachard, Martini, Rettori and Zaninetti, 1994 Tests
are trochospiral, almost planispiral, and may be uniserial in later stages with a microgranular wall.Apertures are basal, simple.Middle to Late Triassic.

Family Arenovidalinidae Zaninetti, Rettori in Zaninetti, Rettori, He and Martini, 1991
The coiling is planispiral or trochospiral, evolute or involute, and may become irregular.Apertures are simple, at end of the tube.Early Carboniferous to Holocene.
Biostratigraphic ranges of the main Triassic genera.originatedwith the family Syzraniidae in Moscovian time.The wall in the earliest species of Syzrania (a form of Robuloidoidea) is dominantly microgranular, with only an incipiently developed hyaline-radial layer.This led authors such asAltiner and Savini  (1997)to retain the Syzraniidae within the Fusulinida.Similarly, in certain reference books (e.g.Loeblich and Tappan