The Orbitolinidae are an agglutinated, and now extinct, family of the Larger Benthic Foraminifera (LBF). Orbitolinidae were present in the warm, shallow marine waters of the Early Cretaceous to the early Oligocene, however, they were most diverse during the mid-Cretaceous. During the Early to mid-Cretaceous (Valanginian to early Cenomanian), there was an identifiable increase in the complexity of their morphological structure, which enabled them to house within their tests symbiotic algae , and it is these forms which are the subject of this paper. Traditionally, orbitolinids are considered to define two major, distinct paleogeographic realms, namely those of the Americas and the Tethys (see BouDagher-Fadel ), but in this study we document forms from the Western Pacific that are distinct from their Tethyan forebears, and so define a third orbitolinid province.
The symbiotic orbitolinids were rock-forming organisms, and they are found in association with other marine forms, including planktonic foraminifera. This coexistence with planktonic forms, enables their stratigraphic ranges to be defined very precisely, as they can be tied to the high resolution planktonic zonal (PZ) dating scheme of BouDagher-Fadel (; see Fig. 1), which itself is tied to the absolute time scale of Gradstein et al. .
Early to mid-Cretaceous orbitolinids have been described from Tethyan limestones from, for example, the Mediterranean , Southwest England [5–10], Spain [11, 12], France , Italy , Israel, Lebanon and Syria , Yemen , Oman [17–19], Saudi Arabia [20, 21], the United Arab Emirates , Iran ([23–27]; Rahiminejad and Hassani, 2016), Afghanistan , and Tibet [29–31]. They are also reported from the Northwest Pacific , Japan and Sakhalin [33–44], and in Africa, where they are found in Ethiopia , Somalia (e.g. [46–48]) and Tanzania .
Furthermore, orbitolinids have been reported from the northwestern Atlantic, off the Flemish Cap, Newfoundland [50, 51], and have been described from the Caribbean and the Americas , Mexico [53–55], and Venezuela .
During their existence, the structurally complex orbitolinids showed relatively rapid phylogenetic evolution, developing many stratigraphically short-ranged species, which when combined with the PZ scheme (see Fig. 1) act as a very important and precise index fossil group for the shallowmarine environments of the mid-Cretaceous Tethys [1, 6, 31, 57]. As a result, they have been widely adopted as a biostratigraphic tool by industry in the exploration of Middle Eastern and other oil and gas fields.
In this paper, the evolution and paleogeographic development of these symbiotic, morphologically complex orbitolinids is inferred from the re-analysis of the published data referred to, and combined with new observations from over 1800 thin sections of material from 13 outcrops of Langshan limestone of the Southern Tibetan Plateau (see Fig. 2), the Sangzugang Formation in Southern Lhasa subterrane (see ), the Xiagezi-II section of the Langshan Formation in southern part of the Northern Lhasa subterrane (see [59, 62]), the Azhang and Guolong sections from the Langshan Formation in the Northern Lhasa subterrane (see ), the Jingshughan, Langshan, Xiongba, Xiongmei, Baoji, Daya, Gegi, Letie and Zulong sections , and the Jiarong and Laxue sections from the Linzhou Basin (see ). In addition, material has been studied from the western flank of the Meratus Mountains, an uplifted accretionary collision complex that records suturing of East Java–West Sulawesi to the Sundaland margin during the mid-Cretaceous (see Fig. 3). The uplifted complex now forms the eastern boundary of the Barito Basin, South Kalimantan, Indonesia (see ).
By correlating these observations and the literature data with our high-resolution PZ scheme (, Fig. 1), we are able to infer, for the first time, a comprehensive, global synthesis of the biostratigraphic, phylogenetic, and paleogeographic evolution of these orbitolinids. We infer that the earliest morphologically complex orbitolinids evolved in the Tethys from primitive Valanginian forms such as Valdanchella, Paleodictyoconus and Campanellula (Fig. 4). More complex forms developed rapidly into different Tethyan phylogenetic lineages (e.g. Figs 4 and 5). It appears that major, global sea level regressions starting in the early Aptian (PZ Aptian 1, 125.0 Ma) and in the late Aptian (PZ Aptian 4, 116.5 Ma; see Fig. 6), correlate with and probably facilitated bidirectional transoceanic migration of orbitolinids. One migration was from the Tethys to the previously recognised American province, but a second migration was from Tethys to the newly defined Western Pacific province (see Fig. 7). These migrations stopped after rising sea level during the early Albian (PZ Albian 1) appears to have isolated the provinces one from another.
The isolated orbitolinids of the Northwest sub-province of the Western Pacific (present day Japan) became extinct at end of the early Albian (top of PZ Albian 1), whereas those in the isolated American province became extinct at the end of PZ Albian 2 (106.7 Ma). All forms in the subprovince that is today South East Asia (on the margins and to the west of the Wallace Line) went extinct at the end of the Albian (top of PZ Albian 4). The ‘hotspot’ for orbitolinid evolution, however, remained in Tethys, where environmental conditions continued to contribute to their success until the end of the Cenomanian, when virtually all symbiotic, morphologically complex orbitolinids became extinct, as indeed did many of the other agglutinated LBFs that dated from the Early Cretaceous and Jurassic (see ). These extinctions coincided with an anoxic oceanic event , and correlate with a near-peak Mesozoic eustatic sea level high-stand (see Fig. 6, and ).
Morphological characteristics of orbitolinids
The orbitolinids are members of the order Textulariida, which have agglutinated tests that are made of foreign particles bound by organic/calcitic cement. They are characterised by having conical tests, subdivided into numerous chambers, and are usually a few millimetres in height and diameter (although as noted, some forms attained diameters of 5 cm or more). The numerous uniserial discoidal chambers are partially subdivided by radial or transverse partitions, or pillars. They have cribrate, areal apertures (see Fig. 8).
The Cretaceous morphologically complex orbitolinids are divided into the dictyoconines and orbitolinines, and range from the Valanginian to the Cenomanian. They are divided into the following five morphological groups (see ):
Orbitolinids with no complex central zones (e.g. Campanellula, PZ Valanginian 1). They lack thick radial partitions and pillars in the central zone.
Orbitolinids with a complex central zone and radial partitions thickening away from the periphery and breaking up into pillars in the central zone, first appeared in the late Valanginian with developed peripheral tiered rectangular chamberlets. They evolved into the dictyoconines (e.g. Paleodictyoconus, PZ Valanginian 2, Fig. 4; Paracoskinolina, PZ Barremian 1–Albian 4), or into the orbitolinines (e.g. Urgonina, PZ Barremian 1, Fig. 4) from forms with the outer parts of their chambers lacking partitions but with interseptal pillars connecting the adjacent septa.
Orbitolinids with radial partitions thickening away from the periphery to anastomose centrally around the aperture and form a reticulate zone in the transverse section, also first appeared in the late Valanginian (e.g. Valdanchella, PZ Valanginian 2). The peripheral zones of their chambers are subdivided into rectangular chamberlets by fine radial partitions (Fig. 4).
Orbitolinids with radial partitions that became zigzagged, thickening and fusing centrally, giving a stellate appearance in the transverse section, first appeared in the Aptian (e.g. Simplorbitolina, PZ Aptian 1-Albian 4). Their tests may have tiered peripheral chamberlets (e.g. Dictyoconella, PZ Cenomanian 3-Maastrichtian 3, Fig. 4).
Orbitolinids with radial partitions thickening, with triangular cross-sections away from the periphery and anastomosing in the central area, first appeared in the Barremian (e.g. Eopalorbitolina, PZ Barremian 1, Fig. 5) and evolved rapidly in the mid-Cretaceous. The test of these orbitolinids is defined by the shape of the embryonic apparatus, and by the size and shape of the chamber passages that can be seen in tangential sections. The earliest formed chambers of the megalospheric generation can form a complex embryonic apparatus, which can be divided into a protoconch, a deuteroconch, a sub-embryonic zone and peri-embryonic chamberlets (see Plate 1, b, e; Fig. 4). In the axial section, the embryo is located at the apex of the cone, followed by a series of discoidal chamber layers. The embryonic apparatus evolved from a simple apparatus, consisting of a large globular fused protoconch and deuteroconch, followed by peri-embryonic chambers as in Palorbitolina, to an embryonic apparatus divided into a protoconch and deuteroconch but a not completely divided sub-embryonic zone, as in Praeorbitolina. This latter evolved in turn into forms in which the deuteroconch and sub-embryonic zone are more or less of equal size, as in Mesorbitolina (Plate 1, d). In Conicorbitolina (Plate 3, f) the marginal zone became extensively divided by vertical and horizontal partitions, while in Orbitolina the deuteroconch is highly subdivided and of much greater thickness than the sub-embryonic zone (see Figs 4, 5; [6, 28, 31, 57, 66, 67]). In transverse section, the chambers are seen divided into a marginal zone, with sub-epidermal partitions, and a central zone with radial partitions (Plate 1, a; Figs 8.1–8.2, 9). The chamber passages are formed in the radial part of the central zone of each chamber layer (Figs 8.1–8.2, 9h), where each chamber passage is subdivided by vertical main partitions, which are prolongations of the vertical main partitions of the marginal zone (Figs 9a–f, h). The radial partitions (Fig. 9f) in advanced orbitolinids (e.g. Mesorbitolina, Orbitolina) thicken away from the periphery and anastomose in the central area, producing an irregular reticular network (Plate 1, c, f–h; Figs 9g, i–j; Fig. 10b). In cross-section, the chamber passages can be triangular (Figs 9c, 10a), rectangular (Fig. 10c) or oval, or can show a gradation between shapes (Fig. 9e) . In the radial zone of Orbitolina, the stolons are arranged in radial rows alternating from one chamber to the next one (see ). Their alternating position would have obliged the protoplasm to flow in an oblique direction . In the annular radial zone of the conical test (Plate 1, a, c, g), radial septula subdivide the chambers into radial compartments with various thickness and textures (Plate 1, h; Fig. 9f, h, k–r), narrowing towards the centre to fuse into a reticular network (Plate 1, a, f, h; Fig. 9g, i, j) which minimizes the volume of chamberlet cavities (Plate 1, a, f–h).
Biostratigraphy, phylogeny and paleogeographic distribution of the orbitolinids
The orbitolinids are very useful biostratigraphic markers in early to mid-Cretaceous Tethyan carbonate, siliciclastic or mixed deposits [28, 31, 68]. They have short ranges and are, with practice, easily identified in thin sections (e.g. see Plates 2 and 3). Orbitolinids show provincialism unlike some LBFs of the period (e.g. the miliolides). Traditionally, they have been considered to define two major, distinct paleogeographic realms, namely those of the Americas and the Tethys (see ).
Many forms from the morphological Group (i) described evolved gradually to more advanced forms of Groups (ii) to Groups (vi). Notable and characteristic paraphyletic lineages include:
Campanellula–Paracoskinolina–Coskinolinoides–Dictyoconus (PZ Valanginian 1–Cenomanian 3; all forms in this group became extinct in the Cenomanian, except Dictyoconus, which persisted to the Oligocene). The evolutionary trend of this Group (i)–Group (ii) lineage is characterised by an increase in test diameter and the development of increasingly complex radial partitions radial partitions thickening away from the periphery, that break up into pillars in the central zone, forming highly developed and complex layers of chamberlets.
Valdanchella–Paleodictyoconus–Montseciella–Rectodictyoconus–Simplorbitolina–Neorbitolinopsis (PZ Valanginian 1–Cenomanian 1). The evolutionary trend of this Group (ii)–Group (v) lineage is characterised by the increase in size, a gradual enlargement of the whole embryo the development of the megalospheric embryo in a centric or near centric position, and the development of increasingly complex radial partitions, becoming zigzagged with a stellate appearance in the transverse section (as in Simplorbitolina) or thickened and fused centrally forming highly developed and complex layers of chamberlets (as in Neorbitolinopsis).
Urgonina – Eopalorbitolina - Palorbitolina – Palorbitolinoides (PZ Barremian 1–Albian 1). The evolutionary trend of this Group (ii)–Group (v) lineage (see Fig. 5) is related to the formation of peripheral, tiered, rectangular chamberlets in two or more series, the shape and position of the embryonic apparatus from a bi-chambered embryo in a clear eccentric position, with a missing peri-embryonic zone in Eopalorbitolina (see Fig. 5), to the development and the increase in size of the peri-embryonic zone to embrace more and more of the embryonic apparatus, surrounding the upper half of the nearly centric embryonic chamber in E. transiens, and becoming completely annular surrounding the upper part of the centric embryonic chamber in Palorbitolina lenticularis (Figs 5, 10). In Palorbitolinoides (e.g. Palorbitolinoides hedini Cherchi and Schroeder , Plate 2, e) the large and flattened embryonic chamber is surrounded by a developed inflated peri-embryonic zone.
Praeorbitolina–Mesorbitolina–Orbitolina–Conicorbitolina (PZ Aptian 1–Cenomanian 3). The main evolutionary characters in this Group (v) lineage are the position of the embryonic apparatus, which is in an eccentric position in earlier forms (e.g. Praeorbitolina), but centrally placed in advanced forms, consisting of the protoconch and the deuteroconch (e.g. Mesorbitolina). In Conicorbitolina (PZ Albian 4–Cenomanian 1) the large proloculus is divided into a protoconch and deuteroconch, with the marginal zone becoming extensively divided by vertical and horizontal partitions (Plate 3, f; Fig. 5). The main evolutionary characters of this Orbitolina (PZ Albian 3–Cenomanian 3) is the increase in size of the apically situated embryonic apparatus, where the deuteroconch becomes about 3 times thicker than the sub-embryonic zone (Figs 5, 9).
On the basis of this study, and using the lineages described, we are able to establish for the first time that there were in fact three distinct paleogeographic provinces for these symbiotic, morphologically complex orbitolinids (see Fig. 7); namely the previously defined American province (including current day Texas, Venezuela, Mexico), a Tethyan province (including Europe and the Flemish Cap off Newfoundland, Arabia, Turkey, Iran, Lebanon, Oman, Syria, Qatar, Tibet), and a newly identified Western Pacific province, which is divided into two sub-provinces; the subprovince of Northwest Pacific, which includes Japan and the Philippine island of Cebu, and a subprovince that includes what is today South East Asia (west of the Wallace Line).
In Tethys, morphologically complex orbitolinids and their precursors are common from the Valanginian (PZ Valanginian 1) to the Cenomanian (PZ Cenomanian 3), and exhibit several of the phylogenetic lineages described, while in the Americas orbitolinids are only found between the early Aptian (PZ Aptian 1) and middle Albian (PZ Albian 2), and are predominantly represented by the Group (v) genera Palorbitolina and Mesorbitolina. In the Western Pacific, unidentified and unconfirmed orbitolinids have been listed in the literature as dating from the late Hauterivian to the early Aptian (see ). These early forms are however contested, but the Group (v) Praeorbitolina–Mesorbitolina lineage is definitely confirmed from PZ Aptian 1 to PZ Albian 1 in Northwest Pacific sub-province and to PZ Albian 4 in the South East Asia sub-province.
From this global pattern, we infer that the original hotspot for the evolution of the complex orbitolinids was Tethys, but as will be described, following migration events in the early Aptian out of Tethys, some lineages of the orbitolinids spread to the other provinces. It seems that the migration stopped after the early Albian, and that the provinces were again isolated. There then developed provincial, parallel, but specifically distinct evolutionary trends, until the subsequent provincial extinctions in the Americas and the West Pacific (see Fig. 11).
Throughout the Tethyan province orbitolinids of Groups (i–v) evolved many lineages. They became morphologically complex and widespread, and are often associated with calcareous algae. Their main Tethyan lineages which evolved from Group (i) include:
Group (ii)–Group (iv) Valdanchella–Paleodictyoconus–Montseciella–Rectodictyoconus–Simplorbitolina–Orbitolinopsis (PZ Valanginian 1–Cenomanian 1);
Group (v): Eopalorbitolina–Palorbitolina–Palorbitolinoides (PZ Barremian 1–Albian 1);
Group (v): Praeorbitolina–Conicorbitolina (PZ Aptian 1–Cenomanian 1).
The orbitolinid assemblages of Western Tethys, the southern Neo-Tethys margin and of southwest Europe are similar to those of the Tibetan carbonate platforms, and they all form a part of the Tethyan realm . All cosmopolitan orbitolinids appeared in the Tethys before spreading to other provinces. For example, in Tethys, P. lenticularis (Plate 2, a; Fig. 10) first occurred in late Barremian (PZ Barremian 3, 127 Ma; ), 2 million years before its first appearance in the American and Western Pacific provinces at the beginning of the Aptian (PZ Aptian 1, 125.0 Ma). The oldest P. lenticularis recorded in what is today the ‘American’ continent was recorded by Schroeder and Cherchi  from the late Barremian of the Flemish Cap, North West Atlantic. From the palaeogeography of the time, however, we infer that at this stage the Flemish Cap was the extreme extension of the north western Tethyan realm and was isolated from the more southerly parts of the American province (see Fig. 7).
The earliest Mesorbitolina (e.g. Mesorbitolina lotzei), likewise, appeared first in Tethys, in PZ Aptian 2. The cosmopolitan Mesorbitolina parva–Mesorbitolina texana first appearing in the late Aptian (PZ Aptian 3, 119.5 Ma), 3 million years earlier than in the American and Western Pacific provinces where their first appearances are recorded in PZ Aptian 4, 116.5 Ma [6, 31, 32, 52]. Subsequent to its first appearance, the Tethyan Mesorbitolina evolved many phylogenetic lineages, which show the typical evolution from having a simple embryonic apparatus to developing a more complicated one. The most common late Aptian–Cenomanian (PZ Aptian 4–Cenomanian 1) lineage being the M. texana–M. aperta lineage (see Plate 1, a–c, 6; Plate 2, d; Fig. 5), where the open deuteroconch in the square embryonic apparatus evolves into a deuteroconch subdivided in the upper part by several partitions of different sizes, whereas the lower part exhibits an irregular network of partitions . No equivalent lineage is found in the other provinces, suggesting that by this stage the provinces were again isolated one from another.
All the main Tethyan orbitolinids became extinct at the end of the Cenomanian, with the exception of rare forms which persist in the Late Cretaceous of the Mediterranean Neo-Tethys, e.g. Pseudorbitolina, Orbitolinella, Calveziconus, Dictyoconella and Dictyoconus which continues to the Oligocene.
The Western Pacific
In the Western Pacific province, orbitolinids limestones, associated mainly with Cretaceous arc volcanics, form two sub-provinces. One occurs north along the Eurasian continental margin to the Philippines and Japan, and the other is to the south, along a belt near the Early Cretaceous margin of Sundaland, in what is today South East Asia [36, 70].
In the Northwest Pacific sub-province, reported occurrences of orbitolinids are patchy with numerous doubtful identifications, but those with certain identification belong to Group (v). Palorbitolina lenticularis is first recorded from the beginning of PZ Aptian 1 (125.0 Ma, 2 million years after its first appearance in Tethys) in the eastern Philippines (Cebu) and Japan [32, 70].
In the South East Asian sub-province, orbitolinids are more common and occur from PZ Aptian 1 (125.0 Ma) to PZ Albian 4 (100.5 Ma). In West Sarawak and Northwest Kalimantan, orbitolinid-rich beds are recorded from the early Aptian (PZ Aptian 1) of Pedawan and Seberoeang Formations . In North-Central Kalimantan orbitolinids are documented from the Aptian to early Albian (PZ Aptian 1–Albian 1) of the Selangkai Formation in the Upper Kapuas River region . Other Early Cretaceous orbitolinid localities include Southeast Kalimantan along the Meratus Mountains front East of Martapura , in South Sumatra, Ratai Bay, Lampung , in the Gumai Mountains , Central Java , and West Sulawesi [76, 77].
The Western Pacific orbitolinids are mainly of Tethyan origin belonging to Group (v). Aptian forms originally described as endemic to the South East Asia sub-province are in fact found to be synonyms to the Tethyan forms. As an example, Orbitolina scutum and Orbitolina trochus originally named as Patellina scutum von Fritsch, 1878 and Patellina trochus von Fritsch, 1878, are both described from Borneo and were assumed to be of Eocene age by von Fritsch , but were later re-identified as the Tethyan species P. lenticularis and M. parva . While P. lenticularis ranges from late Barremian to early Aptian in Tethys, it is only recorded from the Aptian in the Western Pacific.
Sikumbang  recorded quoting Rolf Schroeder's identifications of Meratus Range orbitolinids as P. lenticularis and M. parva, indicating an early late Aptian age. In addition to these forms, we record in this work for the first time the presence of the late Aptian to early Albian (PZ Aptian 3–Albian 1) Tethyan species of Palorbitolinoides orbiculatus (Plate 2, c; Plate 3, d, g) in the early Albian (PZ Albian 1) of the western flank of the Meratus Mountains, Barito Basin, Southeast Kalimantan, Indonesia. The Tethyan genus Conicorbitolina which evolved from Mesorbitolina in Tethys in Albian 3 and ranges to Cenomanian 1 (see Fig. 7) is also recorded here for the first time from the late Albian (PZ Albian 4) of the Barito Basin, Kalimantan, Conicorbitolina sp. (Plate 3, f). Although the shape of the test is similar to the Tethyan Conicorbitolina conica, those from Southeast Kalimantan vary in the shape and number of periembryonic chambers (see Plate 3, f). This is an example of parallel evolution, which gave rise to a similar but distinct form from that found in the Tethyan province. We infer, therefore, that following their initial migration to the Western Pacific, the Mesorbitolina lineage subsequently split into parallel lineages evolving at different rates within the two provinces, apparently with no further gene flow, suggesting that the provinces again became isolated one from another.
The Praeorbitolina–Mesorbitolina lineages are represented in the Western Pacific province by Praeorbitolina cormyi (Plate 2, b), Praeorbitolina wienandsi, Mesorbitolina parva, and M. texana (Plate 1, g–h; Plate 3, a–c), and have been recorded from the late Aptian to early Albian (PZ Aptian 3–Albian 1), again 5.5 million of years after their first appearance in Tethys. Mesorbitolina subconcava (Plate, 1, e; Plate 2, f; Plate 3, e) is recorded here for the first time from the early Albian (PZ Albian 1) of the Barito Basin, Southeast Kalimantan, 3.5 million of years after its first appearance in Tethys.
Groups (i-iv) forms seem to be missing from the Western Pacific province, unlike in the Tethys. Also, unlike the Tethyan realm, the orbitolinids do not survive the Albian-Cenomanian boundary, but disappeared completely from Japan at the end of PZ Albian 1  and, as shown here, from the Barito Basin, Southeast Kalimantan, Indonesia at the end of PZ Albian 4. No orbitolinids are known from east of the Wallace Line in East Indonesia and Australia-New Guinea regions , as these foraminifera required a tropical shallow marine setting, which was not present at this time along the North West Australian margin.
Tethyan orbitolinids belonging to Groups (ii) and (v) seem to have migrated into the American province, however, at a much later date than their first appearance in Tethys.
The American province, unlike the Western Pacific province, contains representatives of the dictyoconines from Group (ii). Paracoskinolina, which first appeared in the Barremian (PZ Barremian 1) (or in the late Hauterivian if «Paracoskinolina» praereicheli Clavel et al. , from the late Hauterivian-early Barremian of the Urgonian platform, South East France, Swiss and French Jura, Swiss Prealps, is considered as a Parakoskinolina) of Tethys, and Dictyoconus, which first appeared in the Aptian (PZ Aptian 1) of Tethys, first appeared in the Albian (PZ Albian 1) of Texas, Mexico, and Venezuela (Maync, 1955 76; Arnaud Vanneau and Sliter, 1995), and range to PZ Albian 2. Species such as Paracoskinolina sunnilandensis  (PZ Albian 2) and Dictyoconus walnutensis (Carsey, 1926) (PZ Albian 1 -2) are unique and indigenous to the American province, and forms recorded as the same as Tethyan species are in fact incorrectly identified. This unique occurrence excludes a West to East migration , and confirms that for most of the Albian the American and Tethyan provinces were ecologically isolated one from another.
The earliest form from Group (v) reported from the American province is P. lenticularis from PZ Aptian 1 (125.0Ma) in deposits of south Mexico, appearing 2.0 million years later than its first occurrence in the late Barremian of Tethys. The Tethyan Mesorbitolina are also widespread in the bank and reef deposits of Texas, New Mexico, Arizona, Guatemala, Honduras and Venezuela (PZ Aptian 4 - Albian 2). The cosmopolitan forms, M. texana–M. parva group occurring from PZ Aptian 3–Albian 1 (119.5-109.8 Ma) in Tethys , are only reported from the PZ Aptian 4–Albian 2 (116.5-109.8 Ma) of Texas, with M. parva only found in the PZ Albian 2 of the Americas.
In the early Albian, species of Mesorbitolina continued to thrive in the Americas but developed provincial specific forms, not found in the Tethys or Western Pacific provinces. Thus, the American lineage Mesorbitolina minuta– Mesorbitolina gracilis–Mesorbitolina crassa of the PZ Albian 1–2 [52, 84] indicates that once the orbitolinids were established in the American province in the latest Aptian, they evolved independently from, yet in a parallel way to, their Tethyan ancestors, by means of gradual development of their embryonic apparatus. Those American species that had been previously reported from the Tethys or the Western Pacific were in fact misidentified. For example, the American M. minuta was reported by Matsumaru and Furusawa , from central Hokkaido, but was re-identified as M. texana by Cherchi and Schroeder .
The Early Cretaceous is believed to have been a greenhouse period, with high atmospheric carbon dioxide concentrations , high global average temperatures with sea surface temperatures exceeding 32°C [87, 88], and a stable climate . The earliest Cretaceous (Berriasian–Hauterivian) was also characterised by a sustained period of global low sea levels, which were replaced in the Barremian by a significant global sea level transgression (see Fig. 6), reaching its maximum at around 129 Ma, Barremian 2. This sea level rise flooded low-lying continental regions and so created new ecological niches around the globe, one of which was filled in Tethys by the evolving orbitolinids.
The globally warm period continued in the mid-Cretaceous and was characterised by an increase in the number of agglutinated foraminiferal forms having large alveoles, such as the lituolid Pseudocyclammina, or forms with internal radial partitions, such as the orbitolinids (see ). This may have been an adaptation to the extreme climatic and oceanic conditions (increases in temperature and oceanic anoxia; e.g. Kerr ) during this interval , linked to an inferred dramatic increase of CO2 in the atmosphere possibly triggered by enhanced global volcanism (e.g. the Ontong Java flood events). The high CO2 levels during this greenhouse period would also have led to increased oceanic acidity , which would have favored the ecological domination of the Textulariida, exemplified by the orbitolinids with their agglutinated tests, over those forms with biogenically precipitated calcitic tests that dominated before and after this period.
Evolving from earlier Valanginian forms, by the late Barremian (PZ Barremian 3), major new lineages of the agglutinated orbitolinids had appeared in Tethys (see ). These robust forms had the ability to survive in many shallow carbonate environments , however, they were most common in the outer platform ([1, 11, 67, 92]; and see Fig. 12).
As noted, we have shown that all cosmopolitan orbitolinids appeared in Tethys before migrating to other provinces. Likewise, we have seen that once established in the American and Western Pacific provinces, local provincial forms evolved, indicating that they were once again subsequently isolated from the Tethyan province. In previous studies of Cenozoic LBF, specifically the lepidocyclinids , the miogypsinids , the nummulitoids [95, 96] and the orthophragminids [97, 98], we have observed similar developments, with periods of migration from one province to another followed by subsequent isolation and development of local provincial linages. In these Cenozoic cases, the periods of inter-provincial migration coincided with major sea level regressions, while the subsequent provincial isolation coincided with global sea level transgressions. As observed in this study, it appears that a similar correlation occurs with the Cretaceous orbitolinids, with migrations from Tethys occurring during the time of Aptian sea level low stands (Fig. 6), followed by isolation when the sea level again rose in the Albian.
Thus, in Tethys, P. lenticularis (Plate 2, a; Fig. 10) first occurred in late Barremian (PZ Barremian 3, 127 Ma), 2 million years before its first appearance in the American and Western Pacific provinces (at the beginning of the Aptian, PZ Aptian 1, 125.0 Ma). This migration coincides with the global sea level regression that marks the beginning of PZ Aptian 1, and which culminates with the global sea level minimum at the end of PZ Aptian 2.
Similarly, the earliest Mesorbitolina (e.g. Mesorbitolina lotzei) appeared first in Tethys, in PZ Aptian 2, but are not recorded until PZ Aptian 3 in the Western Pacific province, and PZ Aptian 4 in the American province.
After the earliest migration in the Aptian, the American Province appears to have been again isolated from Tethys throughout the later Albian and the more advanced lineages of Group (v) (e.g. Orbitolina, Conicorbitolina) of the Tethyan provinces, which appeared in the late Albian, are not found in the Americas. The evolutionary patterns inferred from Tethyan species diverge from those observed in the Americas, confirming that these two provinces were isolated from each other at this time. The progressive changes seen in the different lineages are regarded here as examples of homoplasy, which resulted in the development of morphologically similar yet phylogenetically distinct forms with distinct biostratigraphic and paleogeographic characteristics.
The American orbitolinids became extinct at the end of the PZ Albian 2, 12.8 Ma earlier than those of Tethys (end Cenomanian 3). This event corresponds to the opening of the Western Interior Seaway triggered by sea level rises, and tectonic forces associated with the subduction of the Farallon Plate in the late Albian. This produced, for a period, an epicontinental sea over western North America that linked the tropical seas with a previously separate Artic Ocean. This fully open seaway persisted in the Albian and the Cenomanian, flooding the orbitolinids habitats with cooler deeper waters, and was probably the cause of the orbitolinids extinction in the American province.
In the Western Pacific province, the late Aptian to early Albian larger benthic foraminifera had their origin in Tethys. Following the early Albian migration of the Tethyan foraminifera, however, they seem to have become isolated in the South East Asian sub-province, again correlated with the early Albian sea level recovery. During the late Albian, the lineages evolved independently but in parallel to their Tethyan ancestors. The form Conicorbitolina sp. is similar to but different in specific characters from the Tethyan C. conica (d‘Archiac). This suggests that the migration of Albian foraminifera to the Western Pacific province was only possible for a limited period around the early Albian. Thereafter the orbitolinids of the South East Asian sub-province remained small, rare, and isolated from those in Tethys, as the exclusively Tethyan large species of Orbitolina never appeared in this sub-province. The orbitolinids do not survive the Albian-Cenomanian boundary, but unlike the Tethyan realm, disappeared completely from the Northwest Pacific subprovince at the end of PZ Albian 1  and, from the South East Asian sub-province at the end of PZ Albian 4.
Analysis of new material combined with a synthesis of the published literature has allowed the understanding of the global evolution and paleobiogeographic distribution of mid-Cretaceous orbitolinids within three LBF provinces; namely the Americas, Tethys, and the newly identified Western Pacific province.
We conclude that, unlike previously studied Cenozoic LBF forms, such as the lepidocyclinids , the miogypsinids , the nummulitoids  and the orthophragminids , which evolved first in the Americas and then migrated eastward to Tethys, the Mesozoic orbitolinids originated in the warm tropical shallow platforms of Tethys in the Early Cretaceous, Valanginian (PZ Valanginian 1). The subsequent paleogeographic migration during the global sea level low stands of the Aptian of members from orbitolinid Group (ii) and Group (v) was bidirectional, moving from Tethys westward to the Americas, and also eastward into the Western Pacific region. There is no evidence of a West to East trans-Atlantic migration, nor of migration of Western Pacific forms to Tethys.
We infer that migration stopped after rising sea level in the Albian. As species became geographically isolated, colonising new but ecologically similar habitats, they thrived and evolved similar but distinct parallel lineages, taking advantages of empty niches and optimum conditions. This example of parallel speciation is discussed by Schluter et al. , and probably reflects that all species shared a genetic predisposition to develop mutations of a specific, advantageous type, inherited from their last common ancestor.
The new understanding of the phylogenetic evolution of the Tethyan, Western Pacific and American orbitolinids presented in this paper, when combined with the improved understanding of their biostratigraphic ranges and facies relationships, provides the first global-scale understanding of their development, and so enhances their usefulness as a tool for the study of Early to mid-Cretaceous warm-water carbonate platforms, which are so important in today's hydrocarbon exploration.