Exceptionally well-preserved Permocalculus cf. tenellus (Pia) (Gymnocodiaceae) from Upper Permian Khuff Formation limestones, Saudi Arabia

An exceptionally well-preserved specimen of the articulated rhodophyte Permocalculus, compared with P. tenellus sensu Elliott, 1955, is described from fine-grained Upper Permian limestones of the Khuff Formation of Saudi Arabia. Longitudinal medullary and sheaf-like cortical filaments extend through the uniserial series of elongate-globular, concave- and convex-terminating, interlocking segments for which they are interpreted to have functioned in articulation. The filaments tend to splay and branch laterally into the cortex where they terminate at the pores. At the terminal aperture, the filaments extend as bifurcating and possibly trifurcating branches and may serve as the origin of a new segment. Numerous elongate-globular chambers, up to five in each row and intimately involved with the filaments, are developed in the outer medulla and are considered to represent reproductive sporangia. The specimen is considered to have occupied predominantly low-energy, normal to slightly elevated salinity, shallow conditions within the subtidal regime of a lagoon.


Geological background
The Khuff Formation (Steineke & Bramkamp 1952;Steineke et al. 1958;Powers 1968;Insalaco et al. 2006;Hughes 2008;Maurier et al. 2009) represents the product of one major, but complex, marine depositional cycle that transgressed over the Arabian Platform during the Capitanian/Midian Stage of the middle Permian . Predominantly shallow carbonate deposition, with interbedded siliciclastics and evaporites, continued until the Scythian/Induan Stage of the Early Triassic and the formation contains microfossil and isotopic evidence for the Permo-Triassic extinction. Four members have been mapped in the outcrop (Le Nindre et al. 1990) and include, in ascending stratigraphical order, the Huqayl, Duhaysan, Midhnab and Khartam. In the subsurface of Saudi Arabia, a reservoir classification scheme has been established that consists of the Khuff D, C, B and A units based on four major repeated carbonate evaporite cycles, of which the evaporite forms the seal for the underlying carbonate reservoir (Hughes 2008) ( Table 1). The calcareous alga here discussed was collected from the Khuff C carbonate, equivalent to the Duhaysan and Midhnab members  according to Gaillot & Vachard (2007, Fig. 4) and dated as the Wuchiapingian Stage of the Upper Permian.

Biostratigraphy of the Khuff Formation
Micropalaeontological analysis of field samples and published data from water well SHD-1 (Le Nindre et al. 1990), reappraised by Vachard et al. (2005) and Gaillot & Vachard (2007), have provided comprehensive records of calcareous algae and foraminifera that have been used to date the four members of the Khuff Formation, as recognized in the outcrop belt. Conodont evidence, unfortunately from reworked beds in the lower Midhnab, provides a late Capitanian age, while preliminary Sr isotope determinations suggest a late Capitanian to early Wuchiapingian age (Nicora et al. 2006). The presence of the nautiloid Tirolonautilus gr.
hoernesi Stache from the lower Midhnab (Chirat et al. 2006 (Hughes 2005b). Carbon isotope ( δ13 C carb ) analysis in Oman (Krystyn et al. 2003) displays a strong negative shift from 4 to 0.4‰ across the Permian-Triassic boundary. Similar shifts have been noted in the Saudi Arabian Khuff, in the lower part of the Khuff B reservoir (Al-Jallal 1995). Plant and palynological biostratigraphy of the Khuff is described by Lemoigne (1981a, b) and Stephenson et al. (2003).

Permocalculus systematics
The specimen here described displays remarkably and unusually well-preserved internal microstructures, especially of the internal filaments and organelles, that have survived biodegradation and other changes associated with diagenesis that are typical of the Khuff. To the author's knowledge, no similarly well-preserved specimens have been previously photographed or documented. The presence of well-preserved internal reproductive organs in the studied specimen provides clear evidence for assignment to the Gymnocodiacea, following Mu (1991). Riding & Guo (1991, p. 457) conclude that 'the most likely affinity of the Gymnocodiaceae is with the red algae' following the initial interpretation of Pia (1937).
The specimen here described is assigned to the Family Gymnocodiaceae, of which the candidate Permian genera are Gymnocodium, as defined by Pia (1920), and Permocalculus, as defined by Elliott (1955a). Differentiation of these genera was made by Elliott (1955a, p. 85), for which he described Gymnocodium as hollow calcareous segments, cylindrical, oval or cone-shaped, circular or oval in cross section, rarely bifurcating, the walls perforated by pores which radiate oblique-distally and widen markedly outward; the segment interior may be empty, or may show calcified traces of the plant-fibres that filled it in life, in the form of longitudinal-oblique streaks; sporangia ovoid, in terminal segments. Segments usually smaller than Permocalculus, and the perforations usually coarser. Elliott (1955a, p. 85) defined Permocalculus as segments and units of variable form; spherical, ovoid or barrelshaped segments, or elongate-irregular, finger-like or 'waxingand-waning' units. Calcification varying from very thin to massive or solid; pores small and cortical. Sporangia cortical or medullary. Segments or units usually larger, and the pores finer, than those of Gymnocodium.
The studied specimen is, therefore, assigned to the genus Permocalculus Elliott, 1955a. Permocalculus consists of a succession of uniserially arranged and articulated perforated calcareous segments. The segments are joined by organic fibres that extend out through a terminal aperture into the succeeding segment and are flexible enough to enable the segments to bend with the current. Within the segments, the central axial region is termed the medulla. From this central zone radiate successions of chambered tubes that are directed to the outer layer, or cortex. These form the reproductive organs termed sporangia, as described by Elliott (1961).
The specimen was first illustrated by Hughes (2005a, pl . 1, fig. 9) and consists of five and a half segments arranged uniserially in a slight curve without any indication of branching (Fig. 1) and with a maximum length of 10.5 mm. The segment profiles vary from squatcylindrical to elongate cylindrical, and tend to resemble the 'keg' Fig. 4. Detail of segment 4 of Permocalculus from the Khuff C mudstone. Note the concave proximal part of the segment and the ramifying character of the filaments/microtubules extending from the proximal junction to the peripheral pores. The reproductive bodies, or sporophytes, are clearly visible, of which the proximal ones are filled with organic material; the sporophytes seem to have formed as a necklace-like series as the result of expansion or differentiation of a single filament/microtubule. The distal aperture at the convex end of the segment is not visible owing to the oblique longitudinal section.
shape described for Permocalculus tenellus by Elliott (1955a). There is no indication of the 'waxing and waning' segment profile. The segments interlock with a distal convex part fitting into the proximal concave part of the succeeding chamber. In the following discussion, the specimen is considered to consist of six segments, and these are numbered consecutively from the oldest to the youngest. The rate of chamber enlargement is low, but this may be a function of the thin section probably cutting obliquely through the specimen (Table 3). These oblique longitudinal sections have provided insights into the three-dimensional arrangements of the internal organelles of the segments. The biometrics of this specimen closely resemble those of P. tenellus, but the pores are slightly wider.
Calcification of the red algae typically preserves the outer, cortical, region but the central, or medullary, region is typically poorly calcified and commonly filled with sediment or cement (Flügel 2004). In this specimen, the medullar region is unusually and exceptionally well-preserved owing to carbonization of organelles and filaments arranged along the medullary axis. The outer filaments tend to splay toward the cortex where they ramify and anastomose with each branch terminating at the peripheral cortical pores. These filaments extend along the entire length of each segment, but increase in density at the proximal and distal ends, where they are considered to be involved in articulation of the segments and must, therefore, extend from one segment to the next. Similar medullary filaments have been described from the Gymnocodiaceae by Elliott (1955a), The youngest segment, number 6, displays the free bifurcating, possibly trifurcating, branched terminations of the medullary filaments (Figs 2 and 3). Presumably these extensions provide a foundation for subsequent segment construction.
Medullar filaments seem to tend to develop into a sheaf-like arrangement of globular-ovoid bodies, up to five in a row (Fig. 3). Such organs have been described from Gymnocodium bellerophontis (Rothpletz), with a transverse diameter of 0.29 mm; they represent reproductive organs termed sporangia (Elliott 1955a(Elliott , 1961. Similar organs have been described by Wray (1977) and from other Permocalculus species by Elliott (1961), the Lower Cretaceous Permocalculus? halimaedaformis described by Bucur (1994, especially pl. 6) and the Upper Cretaceous Permocalculus gosaviensis Schlagintweit, 1991by Schlagintweit (2010. Many of the sporangia in the studied specimen have been replaced by calcite and appear colourless, while others (Figs 3 and 4) have been preserved by carbon and are clearly visible.
Segment 4 of the Permocalculus specimen (Figs 3 and 4) shows many interesting aspects of the internal microstructure, in which one can see well-preserved ramifying filaments and microtubules extending from the proximal junction to the peripheral pores. The sporophytes seem to have formed as a necklace-like chain of chambers as the result of expansion or differentiation of a single filament/microtubule.
In summary, and based on the various oblique and near-axial longitudinal sections visible in Figures 1, 3 and 4, the central axis of each segment is considered to consist of medullar filaments. They extend from the aperture at the distal convex end of the previous segment into the aperture at the concave proximal end of the succeeding segment. At the distal aperture of the youngest segment, the filaments extend as branched tufts. These are considered to be essential in both the vascular system of the individual and also as the flexible connective organelle to enable articulation between the individual segments. The filaments also develop into components of the outer, or cortical, region where they bifurcate and terminate at the pores of the segment wall. Although not clearly visible in the specimens, it is highly likely that these filaments are hollow and should be termed microtubules. Within the outer part of the medulla and extending into the cortex, the filaments seem to develop swollen sections, up to five in series, representing the reproductive organs here considered to be the sporangia.

Biofacies and palaeoenvironments
A moderately shallow-marine palaeoenvironment for Permocalculus has been suggested for Upper Permian carbonates of southern Iran (Insalaco et al. 2006, fig. 42). They observed a clearly defined onshore-to-offshore transition of calcareous algae across a carbonate ramp from nearshore Mizzia to Permocalculus to offshore Gymnocodium. A similar trend has been recorded by Lai et al. (2008), where they observe replacement of the robust forms Macroporella, Permocalculus solidus and phylloid algae by the more fragile Gymnocodium bellerophontis. This transition is considered to possibly represent hydraulic energy level decrease due to palaeobathymetric variation. This trend was not, however, observed in the Middle-Late Permian of Greece by Vachard et al. (2003) where Permocalculus and Mizzia were considered lagoonal genera and Gymnocodium to be associated with high-energy shoreline facies.
The Permocalculus-bearing sample was collected from mudstones barren of other microfossils. It is considered to represent an episode of highstand progradation of lagoon muds over an ooid shoal flank that is interpreted as the maximum flooding zone of this depositional sequence, the top of which is c. 30 ft below the Permocalculus event. The prograding succession overlying the ooid grainstones commenced with lagoon sediments shoreward of the ooid bank, rapidly grading up-section from packstones through wackestones containing brachiopod fragments, ostracods, echinoid fragments and the foraminifera Geinitzina postcarbonica Spandel, Hemigordius schlumbergeri (Howchin), Protonodosaria rauserae Gerke, Globivalvulina spp. and Nankinella simplex (Chen). This microfacies is overlain by the Permocalculus-bearing mudstone, which is considered to have been deposited in a low-energy lagoon protected by the ooid grainstone shoal. Absence of other microfossils would tend to suggest adverse conditions, of which elevated salinity could be a factor. The presence of rare specimens of Agathammina and Hemigordius species of miliolid foraminifera in a sample 5 ft (1.52 m) below the Permocalculus sample would tend to support this sequence stratigraphic interpretation (Hughes 2005a(Hughes , b, 2008. The exceptionally well-preserved organic microorganelles in the specimen suggest that rapid burial by mud in anoxic conditions that inhibited bacterial degradation.

Conclusions
An exceptionally well-preserved specimen of a rhodophyte calcareous alga, identified as a species of Permocalculus that bears similarity to P. tenellus, has been recorded in a thin section from the Upper Permian Khuff C limestone of Saudi Arabia. Numerous organic filaments are clearly preserved within the calcareous acuminate cylindrical segments. A group of medullar filaments extend through the segment from the proximal to distal aperture from which they protrude from the youngest segment. They are considered to have both vascular and articular-supporting functions. Some medullar filaments extend in a sheaf-like fashion from the central or axial zone into the cortex where they terminate at the surficial pores. It is highly likely that these filaments are hollow and should be termed microtubules. Some of the lateral filaments seem to expand into a series of up to five bulbous structures that are considered to be the reproductive organs and termed sporangia. The preservation of such a delicate specimen is considered to represent deposition in a low-energy lagoon setting. Absence of associated microfossils suggests elevated salinity conditions, and the exceptionally well-preserved internal organic organelles suggest rapid burial in an anoxic setting. Table 3. Biometrics and comments on each segment of the Khuff Permocalculus specimen (cf. Fig. 1