A diverse Upper Darriwilian radiolarian assemblage from the Shundy Formation of Kazakhstan: insights into late Middle Ordovician radiolarian biodiversity

A diverse and well-preserved radiolarian assemblage was extracted from a carbonate sample of latest Darriwilian age from the Shundy Formation of the Aksuran Mountain (North Balkhash Region, Kazakhstan). The fauna is represented by 32 species or morphotypes which belong to nine genera, four families and two orders (Spumellaria and Entactinaria), including four new species described herein (Syntagentactinia? angulata n. sp. Pouille & Danelian, Polyentactinia spinulenta n. sp. Pouille & Danelian, Haplotaeniatum circulus n. sp. Pouille & Danelian and H.? giganteum n. sp. Pouille & Danelian). Representatives of the family Inaniguttidae are particularly abundant, representing c. 70% of the studied assemblage, especially genera Triplococcus and Inanihella that dominate the assemblage. Although the studied fauna contains both of the characteristic species and most of the genera of the previously defined Haplentactinia juncta–Inanigutta unica assemblage, differences in the assemblage structure are striking. The studied fauna also establishes that the two characteristic species of the Inanihella bakanasensis–Triplococcus akzhala assemblage are not restricted to the early–mid-Darriwilian, but their age range also extends to the latest Darriwilian.

A new, diverse and rather well-preserved radiolarian assemblage from the uppermost Darriwilian in Kazakhstan is presented here. The radiolarian assemblage is dominated by members of the family Inaniguttidae, represented by five genera (Triplococcus, Inanihella, Inanigutta, Inanibigutta and Kalimnasphaera) and 14 species, which have been documented and discussed recently by Pouille et al. (2013), together with several co-occurring trilobites. This paper focuses essentially on the taxonomic study of the rest of the fauna that includes 18 species and morphotypes that belong to the families Haplentactiniidae, Polyentactinidae and Haplotaeniatidae, including four new species. It allows considerable improvement to our understanding of the radiolarian palaeobiodiversity during the late Darriwilian, a critical interval in the context of the Ordovician diversification (Servais et al., 2008(Servais et al., , 2010.

StratIgraphIc SettIng and age
The radiolarian-bearing sample was collected from locality 112, about 1100 m WSW of the Aksuran Mountain (NW of Lake Balkhash) in the Atasu-Zhamshy Region (47°32'40.77"С, 73°2'47.34"E; Fig. 1). It was sampled from the middle part of the Shundy Formation, which consists of deep-water, black or dark grey bedded limestones intercalated with thin dark grey cherts, which probably accumulated at the base of a slope of a passive continental margin of a Lower Palaeozoic microplate. Details about its geological and stratigraphic setting are provided in Pouille et al. (2013). Graptolites, identified by Tsai (in Apollonov et al., 1990) as Hustedograptus ex gr. teretiusculus, occurring in the same stratigraphic level as the radiolarian-bearing sample 112 suggest a latest Darriwilian age. The trilobites (Endymionia semielliptica, Nambeetella? sp. and Porterfieldia sp. aff. P. delicata) found associated with the sample confirm this age . Moreover, two radiolarian genera commonly present in sample 112 (Syntagentactinia and Kalimnasphaera) are known to first occur in the Haplentactinia juncta-Inanigutta unica assemblage which can be best correlated with the uppermost Darriwilian-lowermost Sandbian (see, for example, the discussion in Nazarov & Ormiston, 1993;Danelian & Popov, 2003;Maletz, 2011). Our assemblage also contains Haplentactinia juncta, one of the characteristic species of the Haplentactinia juncta-Inanigutta unica assemblage. A t a s u -Z h a m s h y t e r r a n e Barshatas R a n g e T a r b a g a t a y C h i n g i z R a n g e  Danelian & Popov, 2003).

MaterIal and MethodS
Radiolarians were extracted from a black to dark grey micritic limestone sample after a standard treatment with 30% diluted acetic acid. Taxonomic study of this assemblage was made on the basis of SEM observation on over 450 specimens. This newly discovered assemblage is highly diverse, with a good state of preservation. All the types described here are housed in the public palaeontological collections of the Earth Sciences Department (SN5) of the university Lille 1 (France).
description. Internal structure consists of a five-to six-rayed primary spicule incorporated in a small latticed inner shell. The primary rays of the initial spicule are prolonged outside into long rod-like spines (up to 200 µm). These primary spines can be straight or slightly curved on their proximal part. A small internal cavity with an irregular outline separates the inner shell from the outer shell. The outer shell structure consists of three to four spongy shell layers of irregular outline and that are closely interconnected by numerous radial beams in a very complex three-dimensional arrangement. The different spongy layers of the shells are hardly distinct. The outer shell is mostly spherical (rarely sub-spherical) and displays a spongy external aspect. Inside the inner cavity, rare apophyses can branch from the primary rays to join the inner shell surface.
remarks. The skeleton structure and dimensions of S. biocculosa are very close to those of S.? sp. cf. S. excelsa Nazarov & Ormiston. However, it differs from it in possessing six long, robust rod-like spines, a less loose latticed inner shell and in having a less distinct inner cavity. It also differs from S. pauca Nazarov in possessing a thick multi-layered spongy outer shell and in its larger size. It also differs from S. afflicta Nazarov & Ormiston in the absence of internal half-closed shells, in the larger size of its inner shell (as compared with the material of Nazarov & Ormiston, 1993) and in its smaller size (for the material illustrated by Kurihara & Sashida, 2000). Material. 29 specimens.
description. The inner framework consists of a distinct spherical to subspherical loosely latticed inner sphere, centrally or slightly eccentrically located inside the internal cavity. The outer shell consists of a thick spherical spongy meshwork formed of three to four latticed shell layers closely interconnected in a three-dimensional way by many radial beams. In some cases it can be very difficult to distinguish the different shell layers, and the outer shell forms a very complex sponge-like ball. The inner shell is connected to the outer shells by a few beams. Primary spines are very thin, weakly developed and commonly not visible outside. The innermost structure is not preserved in our material. remarks. This species differs from the other two Ordovician Syntagentactinia species described by Nazarov & Popov (1980) (S. biocculosa and S. pauca) in possessing a thick multi-layered spongy outer shell, in the absence of rod-like outer spines and in its larger size. Our specimens differ from S. excelsa as described by Nazarov & Ormiston (1993) only in their inner shell dimensions (40-42 µm in Nazarov & Ormiston's material), but correspond relatively well to the dimensions given by Kurihara & Sashida (2000;40-90 µm). The species differs from S. afflicta that co-occurs with S. excelsa in the absence of long, robust, rod-like spines and in its internal half-closed shells. description. Spherical radiolarian with an outer shell structure formed of two (rarely three) spongy shell layers closely interconnected by many radial beams and arranged in a thick spongy three-dimensional way. The thickness of the spongy meshwork is variable. The internal framework consists of a large latticed inner shell with well-defined pores located inside a small hollow cavity. Inner shell is connected to the outer shells by short beams. Six primary rays protrude radially as very thin and short rod-like outer spines outside the outer shells. Thin secondary spines are present on the surface of the outer shell. The innermost framework is broken in every specimen but primary rays have been observed to protrude inside the inner shell.
remarks. It differs from S.? sp. cf. S. excelsa and S. biocculosa in its larger size (see Table 1) and in possessing thin secondary spines on the surface of the outer shell. It differs from S. pauca in its thick spongy outer shell and its larger size. the spicule centre to form a small irregularly latticed inner shell, which is unevenly porous and located inside a hollow cavity. The latter is very irregular in outline and clearly separates the inner and outer shells. The outer shell is formed of different groups of apophyses that branch from the primary rays to form a very thick, irregular and dense spongy meshwork (up to 130 µm thick). The outer shell displays a polygonal to quadrangular outline. Primary rays are disposed in the three rectangular axes and prolonged into thick rod-like outer spines.
remarks. Due to its small size, the inner shell surrounding the primary spicule can be mistaken for a microsphere on unbroken specimens. The primary spicule appears to be point-centred; however, it could also be interpreted as a broken bar-centred spicule, which explains the doubtful generic assignment. This species differs from other species of the genus Syntagentactinia in the polygonal to quadrangular outline of its outer shell, its wide inner cavity, its thick and complex three-dimensional nonlayered meshwork and its much larger size (see Table 2).
description. The spongy outer shell displays an ovoid shape with six primary spines. Two spines are located on the margin of one pole of the shell. The four other horn-like spines are situated on the opposite pole of the shell and are curved inwardly. The outer shell consists of a thick, multi-layered, three-dimensional meshwork. The inner framework consists of a latticed inner shell. The innermost part of the framework is unknown. remarks. It differs from other Syntagentactinia in its ovoid shape, the peculiar position of its primary spines and in the large size of its inner shell. fig. 19) description. This morphotype displays a primary spicule located inside a very small sphere surrounded by an inner and an outer shell. Six or more primary rays originate from the primary spicule aligned with thick rod-like external spines. Numerous beams connect the latticed inner shell with the outer shell. The outer framework consists of two latticed shell layers closely interconnected in a three-dimensional arrangement. The outermost shell layer displays a thick spongy aspect.
remarks. The small sphere inside the inner shell can be distinguished from a microsphere only by the presence of primary rays protruding inside it. As the primary spicule is broken it is difficult to know the exact number of primary rays that originated from it. This morphotype differs from all other species of Syntagentactinia in its regular outline, the presence of a very small sphere surrounding the primary spicule and the presence of numerous beams connecting the inner with the outer shells. It also differs from all the species described in this paper in possessing a much thinner outer shell wall.
Haplentactinia juncta Nazarov, 1975 (Pl. 2, fig. 1  remarks. This species differs from H. armillata in its wider and more loosely constructed mesh, smaller size (shell Ø: 320-400 µm in H. armillata) and absence of a bifurcated primary spine. It also differs from H. infida and H. baltica in its more rounded outline.
In addition, H. infida differs from H. juncta in possessing one spine considerably larger than the others and in having apophyses on this spine located closer to the inner spicule, whereas other apophyses are at equal distance from it.

diagnosis.
A single spherical outer shell displaying a latticed meshwork of interwoven bars, bearing 6 rod-like outer spines, which originate from the primary rays of a short median bar located eccentrically in the internal part of the shell.
description. Internal framework consists of a primary spicule formed of a short median bar (10-15 µm) from which six primary rays originate. The median bar is eccentrically located in the spherical skeleton and it may often appear point-centred depending on its orientation. The six primary rays continue outside the spherical shell as rod-like outer spines that can be straight or slightly curved. They bear a verticil of two perpendicular whorled rays that originate at the level of the cortical shell with which they are connected to the spherical skeleton. The shell is formed from a latticed meshwork with angular meshes formed from interwoven bars of various thicknesses. On well-preserved specimens numerous small simple or bifurcated spinules are present on the shell surface. remarks. This species differs from Astroentactinia in the absence of characteristic pores and of any conical secondary spines on its cortical shell. Its internal frame and its shell structure suggest an assignment to Polyentactinia. P. spinulenta differs from P. offerta Nazarov (an upper Darriwilian species described from the Haplentactinia juncta-Inanigutta unica assemblage) in possessing only 6 thin rod-like external spines and a shell formed from a meshwork of interwoven bars forming angular meshes and covered by small spinules, whereas P. offerta displays a porous latticed shell with more than 12 external spines. It differs from the upper Ordovician species P.? estonica Nazarov in possessing thinner, longer and less numerous outer spines and in its less massive shell structure. It differs from Silurian species P. stelcki and ?P. leeorum in its larger size (c. 200 µm for ?P. leeorum, 70-135 µm for P. stelcki), more angular mesh structure and the presence of interwoven bars. Most Polyentactinia species are described from the Devonian to Permian interval. As concerns the Devonian species, P. spinulenta is easily distinguished from P. kossistekensis, P. rudihispida and P. propinga by its internal structure and number of primary spines (7-8 rays for P. kossistekensis; 7-10 rays for P. propinga and P. rudihispida). P. circumretia differs from P. spinulenta by having a 6-to 7-rayed point-centred spicule centrally located and bi-or trifurcated outer spines. P. spinulenta differs from P. polygonia, P. craticulata and P. leptosphaera in its larger size (90-180 µm in P. polygonia; 115-150 µm in P. craticulata; 160-240 µm in P. leptosphaera). The shell structure of P. spinulenta also differs from P. invenusta and P. tenera, which display a thin and delicate shell structure constructed in a three-dimensional way as thick spongy tissue. description. Internal framework consists of an initial spicule formed of a very short median bar (about 8 µm) eccentrically located that may appear point-centred depending on orientation. Five primary rays emerge from the median bar and turn into thick rod-like outer spines outside the shell surface. Two primary rays are longer than the others and bear at their distal ends two long perpendicular whorled rays connected to the outer shell meshwork. Some of them may emerge from the shell surface as secondary spines. Simple apophyses can be present at the distal end of these whorled rays and be merged with the bars of the shell meshwork. The shell is formed of a loose meshwork of thick straight and curved bars interwoven in a disorderly manner or fused. Numerous simple or bi-to trifurcated spinules are present on the shell surface. remarks. This species differs from P. spinulenta in having much thicker primary rays, a thicker skeleton structure, larger dimension and in the presence of numerous spinules on the shell surface. It also differs from P. spinulenta in possessing whorled rays on only two primary spines and in having only five primary spines and a much shorter median bar.

description.
Internal framework consists of an initial spicule formed of a long median bar (about 60 µm), eccentrically located, from which five (six?) primary rays originate. The primary rays are prolonged into thick rod-like straight outer spines. Two to three perpendicular whorled rays originate at the distal parts of each primary rays and fuse with the spherical skeleton. Some of them emerge from the shell surface as rod-like secondary spines. Apophyses branch from the primary spines to form an irregular spherical loose meshwork consisting of thick straight and curved bars interwoven in a disorderly manner or fused. Numerous simple or bi-to trifurcated spinules are present on the shell surface. remarks. This specimen differs from P. sp. cf. P. spinulenta in possessing up to three whorled rays on the primary spines and also in the larger size of the median bar.
description. The outer shell displays an ovoid outline and is characterized by an intergrowth of strongly fused bars. The skeleton is very compact and made of thick elements. Eight to ten thick rod-like outer spines emerge from the shell surface and can bear small simple apophyses. Numerous thin and long spinules are present on one side of the shell surface. The internal framework is hidden except for a six-rayed point centred spicule visible from a wide opening.

remarks.
Internal framework remains uncertain as the inner structure of the shell is not entirely visible. The six-rayed point-centred spicule may be considered as the initial skeleton but none of the thick rod-like outer spine seems to be connected with the rays of this spicule. Therefore, a more detailed study of the inner-frame is needed to understand the internal structure. Polyentactinia sp. B outer shell structure clearly differs from all other Polyentactinia species in its characteristic intergrowth of strongly fused bars and the more developed long spinules covering the shell surface. This skeletal structure of Polyentactinia sp. B displays some affinities with the Silurian genus Palaeophippium but it differs from it by not showing a saddle-shaped internal spicule with apical and basal hemispheres.
diagnosis. Large spherical spongy outer shell, bearing long and massive rod-like spines, encapsulates 5-6 pseudospongy internal shells displaying a slightly spiraliform arrangement and a small latticed microsphere from which primary spines originate.
description. Haplotaeniatum formed of five to six irregularly circular pseudospongy latticed shells arranged in a slightly spiraliform fashion. Internal framework consists of a small, centrally located, latticed microsphere. Four visible primary rays originate from the microsphere. They are prolonged into long, massive rodlike spines (up to 350 µm or more) outside the shell. Apophyses branch from the primary spines to form the different latticed shells surrounding the microsphere. A few apophyses can be irregularly placed giving the shell a spiraliform arrangement. The shells are connected together by thin beams, irregularly placed, forming a 'cellular-wall'. The shell layer forms numerous halfloops at the points where it is connected to the radial beams. The outermost shell is formed of a three-dimensional spongy meshwork which originates from two to three groups of apophyses branching from the primary spines. The outer shell displays a spherical shape. No secondary spines are present.  . 13. Haplotaeniatum sp. B. fig. 14 H. circulus also differs from H. primordialis? and H. tegimentum in its larger size, which is 194-208 µm in H. primordialis? and 240-264 µm in H. tegimentum, and in its well-developed outer spines (up to 40 µm in H. primordialis?; up to 20 µm in H. tegimentum). It also differs from H. tegimentum in the absence of half-closed shells and conical external spines and in possessing a centrally located microsphere.
description. Shell consisting of a centrally located microsphere surrounded by four to five shells arranged in a spiraliform fashion. Shell layers are interconnected by small and irregularly placed beams. They display a cellular outline, forming numerous half-loops at the point where they are linked to the beams. The outermost shell is egg-shaped and formed of a thin spongy meshwork. At least two primary spines were observed to originate from the microsphere. Outer spines are thick and covered with spongy accretions that accentuate the ellipsoidal shape. No secondary spines are present.
remarks. In its shell structure this morphotype resembles H. circulus. However, it differs from it in its more accentuated spiraliform construction, in its ellipsoidal shape and its weakly developed primary spines. It also resembles H. labyrintheum, but it differs from it in possessing very thin radial beams, weakly developed primary spines, a larger, centrally located, microsphere (Ø: 38-43 µm in H. labyrintheum) and more distinct layering.
description. The internal framework consists of a microsphere surrounded by a complex meshwork of several latticed layers formed from curved to curled bars developed in a spiraliform way. The curled bars give rise to numerous small half-closed loops around the microsphere. No internal cavity appears to be individualized. The microsphere, which is not easily distinct, is, in general, centrally located. Rare beams are present. Three to four primary rays originate from this microsphere but they are rarely developed externally. The outer shell consists of a thick spongy, three-dimensional shell of variable thickness. It displays a spherical to subspherical outline.
remarks. Morphologically this species is very similar to H. tegimentum illustrated by Kurihara (2004), from which it differs in its centrally located microsphere and in the absence of any external spines. It differs from the co-occurring H. circulus and Haplotaeniatum sp. cf. H. circulus in its less distinct and less numerous internal shell layers, its thickest spongy outer shell and its denser layering structure formed of numerous small half-closed loops around the microsphere. It also differs in its smaller outer shell and smaller microsphere. This taxon differs from the upper Ordovician species of the genus Haplotaeniatum in its internal shell structure, its dense and thick three-dimensional spongy outer spherical shell and its large size (outer shell Ø: 104-170 µm in H. spinatum; c. 145 µm in H. fenestratum; 115-291(?) µm in H. prolatum; 180-230 µm in H. ovatum). It is easily distinguished from H. ovatum by its more discernable internal layering and the absence of a pylome. It differs from H. labyrintheum and H. cathenatum in its smaller size (outer shell Ø: 296-354 µm in H. labyrintheum; 308-394 µm in H. cathenatum), in possessing fewer internal shell layers that are more densely constructed, forming numerous half-closed loops of a very small size around the microsphere and a thick spongy three-dimensional outer shell. It also differs from H. labyrintheum in possessing a centrally located microsphere, lacking rod-like external spines and a cellular wall, and from H. cathenatum in lacking a pylome and thin secondary spines. It differs from H. primordialis? in its larger size (outer shell Ø: 194-208 µm in H. primordialis?) and its denser internal shell structure. It differs from H. fissura in possessing a thick spongy outer shell with no distinct pores and the absence of a distinct gap between the microsphere and outer layers of the shell, the absence of a pylome and the weak development of primary spines. It differs from H. aperturatum and H. adobensis in lacking large pores on the outer shell surface, in having a more distinct internal spiraliform structure and lacking a pylome.

diagnosis.
A large, spherical and spongy three-layered outer shell surrounds a much smaller inner latticed shell which encapsulates a microsphere. Six rod-like spines originate from the microsphere; they are covered proximally by numerous branching apophyses that join the outer shell.
description. Internal framework consists of a centrally located, latticed microsphere with uneven pores of variable size. This microsphere is encapsulated in a subspherical to oval inner latticed shell. Six primary rays originate in the microsphere and prolong outside the shell into thick rod-like spines. The inner shell is clearly separated from the outer shell by a large empty cavity. Small and simple apophyses, irregularly placed, can branch from the primary rays between the inner and outer shells. Some apophyses can join the inner shall surface. The outer framework consists of three thinly latticed oval shell layers closely interconnected by numerous short beams in the form of a three-layered wall arrangement. The outer shell surface displays a spongy aspect. Outer spines are covered at their proximal part with numerous apophyses branching to join the outer shell surface which contribute to give the shell a strong ellipsoidal shape. description. This specimen displays a dense three-dimensional mesh of bars which are interwoven in a disorderly manner to form a spherical shell. About 20 thick and short outer spines are irregularly placed on the shell surface. The outer shell displays a subspherical irregular outline. Inner structure is unknown.

dimensions (µm).
Diameter of the outer shell: 313-320; thickness of the base of the outer spines: 20 to 25.
remarks. This species differs from other species of the genus Haplotaeniatum in the presence of numerous outer spines. A high number of outer spines is encountered most often in Oriundogutta which can possess from 8 to 20 external horns. However, Oriundogutta is distinguished by possessing a two-dimensional porous outer shell, whereas our morphotype displays a thick three-dimensional disorderly interwoven meshwork.
description. This specimen displays a roughly spherical test formed of a dense three-dimensional mesh of fine bars. It consists of several three-dimensionally interwoven latticed layers which give the shell a spongy appearance. There are about 20 thin short outer spines present. Apophyses may branch from the proximal Maletz et al. (2009) and 4 species from sample 8807 as studied by Danelian & Popov, 2003). Our assemblage, therefore, confirms that the two characteristic species of the Inanihella bakanasensis-Triplococcus akzhala assemblage are not restricted to the earlymid-Darriwilian but also extend into the latest Darriwilian. Therefore, only the Proventocitum procerulum assemblage can be used to define the upper Dapingian-mid-Darriwilian interval. The uppermost Darriwilian is characterized by the Haplentactinia juncta-Inanigutta unica assemblage. In the light of our new radiolarian assemblage from the Hustedograptus teretisculus Biozone, the uppermost Darriwilian can now be better defined by the cooccurrence of the genera Syntagentactinia, Kalimnasphaera, Inanibigutta, Protoceratoikiscum, which first occur from the Hustedograptus teretisculus Biozone, and the genera Triplococcus and Polyentactinia. It is also characterized by the absence of the genus Proventocitum. It displays the following characteristic species: Haplentactinia juncta, Inanigutta unica, Triplococcus aksuranensis, Kalimnasphaera aperta and Syntagentactinia biocculosa.
This study considerably improves our knowledge of radiolarian species occurring in the upper Darriwilian and provides a much better view of the radiolarian palaeobiodiversity during this critical interval from which well-studied planktonic groups (acritarchs, graptolites or chitinozoans) are known to reach their maximum diversity (Servais et al., 2008(Servais et al., , 2010.

concluSIon
The description of an entirely new assemblage composed of 32 species and morphotypes, including six new species (four described here and two in Pouille et al., 2013) from the Shundy Formation of the Aksuran Mountain, enables us to improve our understanding of the palaeobiodiversity of upper Darriwilian Radiolaria. It also allows us to better define the age range and community structure of Middle Ordovician radiolarian assemblages, including the age range of previously recognized assemblages.
acKnowledgeMentS Lauren Pouille and Taniel Danelian acknowledge support from the university Lille 1 and the CNRS. Leonid Popov acknowledges logistical support from the National Museum of Wales. Philippe Recourt helped with the SEM. Constructive remarks by the two reviewers, Paulian Dumitrica and Jorg Maletz, and the handling editor, Claire Allen, improved the initial manuscript.

Manuscript received 15 april 2014 Manuscript accepted 15 april 2014
Scientific editing by Claire Allen.

reFerenceS
The Lyell Collection One of the largest integrated collections of online Earth science literature in the world For more information visit www.lyellcollection.org

What is the Lyell Collection?
The Lyell Collection is an online collection comprising the Society's journal titles, Special Publications and key book series. Cutting edge science sits alongside important historical material, benefiting from the superb functionality offered by the online host, HighWire Press.
With 260,000 peer-reviewed pages, 26,000 articles and 1,000 volumes, the Lyell Collection is an invaluable tool for the researcher and student alike.

Special Publication archives
The first 300 volumes of the Geological Society's Special Publications Online Archive are available as a one-off purchase with perpetual access.

The Geological Society
The Geological Society of London was founded in 1807 and is the UK national society for geosciences. It is a global leader in Earth science publishing, dedicated to providing high-quality content and service throughout the world.

Geofacets-GSL Millennium Edition
Elsevier and the Geological Society of London (GSL) have collaborated to provide GSL members with a unique opportunity to gain individual access to 24,000+ geological maps from the renowned Lyell Collection through the Geofacets platform.
The Geofacets platform is an innovative map-based research tool designed for geoscientists. These maps are downloadable, geo-referenced, and accompanied by metadata, article abstracts and links to original source articles.