Earliest ontogeny of Early Palaeozoic Craniiformea: compelling evidence for lecithotrophy
Abstract
The early ontogeny of Palaeozoic Craniiformea (Brachiopoda) remains controversial, with conflicting reports of evidence indicating lecithotrophic versus planktotrophic larval stages. Further compelling evidence for lecithotrophy in Palaeozoic craniiforms is described here. Newly obtained, well-preserved Silurian specimens of craniiforms, including Craniops (Craniopsida), and Lepidocrania? and Orthisocrania (Craniida) from Gotland and the St. Petersburg region, form the basis for this study. The new material demonstrates that the characters of shell structure and shell formation provide evidence of early differentiation of an adult dorsal mantle, and the presence of a distinctive primary layer with a characteristic lath-like pattern indicates that these craniiforms underwent a lecithotrophic larval stage, more or less identical to that of living.
Keywords
Following the pioneering studies by Nielsen (1991), it is well-established that the larva of the Recent craniiform brachiopod Novocrania is lecithotrophic and has a very short pelagic stage. It has been inferred (Holmer et al. 1995; Williams et al. 1997) that lecithotrophy evolved early in craniiforms and represents a potential synapomorphy of brachiopods with calcareous shell mineralization. However, Freeman & Lundelius (2005) later demonstrated that the lecithotrophic larval habit of rhynchonelliforms probably did not evolve earlier than the Mid Ordovician. Subsequent studies give further confirmation that the larva in the Billingsellida was planktotrophic (Popov et al. 2007). Earlier, Madison (2004) also reported evidence of a possible planktotrophic larval habit at least in some Mid Ordovician orthides.
However, the feeding habit of Palaeozoic craniiforms remains a subject of controversy. Freeman & Lundelius (1999, 2011) suggested that the larva of craniopsides was most probably planktotrophic, and that a lecithotrophic larva evolved in craniides not earlier than the Jurassic. Alternatively Popov et al. (2010) argued that lecithotrophic larva evolved in craniiforms already by the Late Ordovician, and probably represent an apomorphic character of the clade. The major objective of this article is to demonstrate further compelling evidence indicative of a lecithotrophic habit of craniide and craniopside larvae, as preserved in newly discovered, exceptionally well-preserved material from the Silurian of Gotland and from the Ordovician of the St Petersburg region.
Materials and methods
The following brachiopods were studied: (1) Craniops implicatus (Sowerby 1839) from the Silurian, Wenlock, Mulde Formation, Eksta, Fröjel Parish, Gotland, Sweden; (2) Craniidae gen. et sp. indet. 1, Silurian, lower Wenlock, Upper Visby Formation, Häftingsklint, Hangvar, Gotland; (3) Craniidae gen. et sp. indet. 2, Silurian, upper Wenlock, Slite Group, Solklint, Hangvar, Gotland; (4) Lepidocrania? sp., Silurian, upper Wenlock, Slite Group, Solklint, Othems, Gotland; (5) Orthisocrania curvicostae (Huene 1899), Upper Ordovician, Sandbian, Gryazno Formation, Klyasino Quarry, western St Petersburg region, Russia (locality K-2 of Zuykov inZuykov & Butts 2008). Figured specimens are housed in the National Museum of Wales (NMW) and Naturhistoriska Riksmuseet, Stockholm (RM).
All studied brachiopod specimens were isolated and picked from residues after washing and sieving of soft argillaceous rock in water; no chemicals were applied in the process. For detailed examination of shell fabrics, specimens were cleaned ultrasonically and subsequently etched in 2% EDTA for 5 min. After coating with gold palladium they were studied under a scanning electron microscope using a Cam Scan MaXim 2040S SEM (Obducat Camscan Electron Optics Ltd) with variable vacuum chamber.
New evidence for lecithotrophy
Craniopsida
Notwithstanding recent comments by Freeman & Lundelius (2011), the newly studied specimens of Craniops implicatus (Sowerby) exhibit a clearly visible lath pattern (Fig. 1C–E). In the dorsal valve, radially arranged laths are formed just outside the halo (Fig. 1B); they cross the brephic shell from the umbo to the margins of the first growth lamella (Fig 1C), and are present also on the outer regions of the shell. The protegulum is dome-shaped, almost circular in area at the umbo, and 90–120 μm across (Fig. 1A–C). In a few exceptionally well-preserved specimens, a fine structure can be observed in the protegulum (Fig. 1B); it comprises sub-triangular lamellae about 50–55 μm long and 15–20 μm wide, which radiate from the centre of the dome as small, irregular tablets. This pattern most probably reflects the surface structure of the secondary layer below the protegulum, and probably records the secretion of a differentiated secondary layer. A further important point is that the protegulum is a rigid structure, which does not show any evidence of compression or lobation. In shape and size, it is similar to the inferred protegulum (‘median mound’) of the paterinide Micromitra (Williams et al. 1998), the gonambonitid Oslogonites (Popov et al. 2007; fig. 1A,D) and the siphonotretide Siphonobolus (Popov et al. 2009; fig. 6J,K), but in both these latter taxa it is surrounded by two pairs of inflated lobes that indicate the position of the mantle setal sacs (Williams et al. 1998); these characters suggest that there was continuous peripheral growth of the larval shell before the end of metamorphosis in the two latter genera, but not in Craniops.

The ventral valve of Craniops preserves a button-shaped initial attachment scar about 90–100 μm across (Fig. 1D,F). It is surrounded by a ‘smooth’ area about 250 μm across. Radially arranged laths become apparent around the margins of this area, but the transition is not accentuated by a distinct growth mark. A lath-like pattern is well expressed across the whole of the cicatrix attachment and continues into outer parts of the shell, where it is superimposed on dense growth lamellae (Fig. 1E,F).
The initial attachment scar marks a transition to the attachment of the animal by the ventral side of the body, but it does not represent a protegulum. More probably, this feature replicates a colleplax-like organic pad, such as that found in chileides (Homer et al. 2011). The presence of the ‘smooth’ area may suggest that the adult mantle differentiation, as well as the secretion of primary and secondary shell layers, were delayed considerably in Craniops.
Our new observations suggest that the ontogeny of Craniops is comparable with that of Recent Novocrania. Both became attached to the substratum by the ventral side of the body shortly after settlement. Differentiation of the ventral mantle and secretion of a mineralized ventral valve in both taxa was subsequent to the secretion of the dorsal protegulum. It is relevant to note that the protegular width in Craniops (90–120 μm) is greater than in Novocrania (70 μm), whereas the full grown metamorphic shell of Novocrania is considerably larger (240 μm). It is probable that metamorphosis in Craniops occurred within a shorter time than in Novocrania, and that larval setae were lost shortly after settlement, or possibly immediately prior to settlement.
Freeman & Lundelius (1999) did not provide any other evidence than shell size in support of their view that the protegulum of Craniops indeed represents the embryonic shell. However, their interpretation is not supported by our observations of early shell formation in Craniops, because the lath pattern and the underlying secondary layer on the surface of cicatrix attachment could not have been secreted simultaneously at attachment, but must have been produced only at the time of onset of adult accretionary shell growth (Williams et al. 1997). The appearance of the lath pattern immediately outside the halo suggests that the metamorphosis of Craniops was completed shortly after the secretion of the protegulum. The protegulum was a rigid and probably mineralized structure, and apparently it did not grow accretionally before metamorphosis was completed. All these data support the view that the formation of the protegulum took place post-embryonically, and that the larva of Craniops was lecithotrophic.
Craniida
The craniide Lepidocrania? sp. is readily recognized because of its strong concentric ornament, with closely spaced lamellae that preserve an irregular outline consistent with an encrusting mode of life. The metamorphic shell of Lepidocrania? sp. is about 175–180 μm across. It is inflated in the central area, somewhat flattened along the periphery, and delineated by a distinct halo. It is possible that the inflated area of the metamorphic shell represents a protegulum and it shows evidence of peripheral growth for some time before metamorphosis was completed. The etched surface of the protegular area exhibits a central cluster of irregular tablets, surrounded by radiating subtriangular lamellae (Fig. 2G), which are suggestive of the pattern described earlier for Craniops (Fig. 1B). A major growth lamella was formed when the shell grew up to 300 μm across. Its outline shows a distinct irregular pattern, suggesting that the animal was already encrusting on an uneven substrate at that stage in growth (and probably sometime before; Fig. 2F,G). Thus, we interpret the metamorphic protegulum in Lepidocrania? sp. as post-embryonic, and the Lepidocrania larva was most probably lecithotrophic.

We have also examined another craniide taxon (Craniidae gen. et sp. indet. 2), which has yet to be named formally. It is characterized by a low conical dorsal valve with distinctive tubular ribs. The apical region, about 735–740 μm across, lacks radial ornament and is delineated by a distinct halo (Fig. 2C,E). The halo has an irregular outline suggesting an encrusting habit of the animal during its earliest stage, when this feature was formed. There is a distinct area about 175–180 μm across at the umbo which is ornamented with a mosaic of irregular tablets (Fig. 2D,E). It is comparable in size with the full grown metamorphic shell of Lepidocrania? sp., but it lacks the characteristic peripheral belt of sub-triangular tablets. The margin of this area, which we interpret as the metamorphic shell, is delineated by a weak growth line. The lath pattern appears immediately outside this growth mark. In places the laths are worn, exposing a lower, re-crystallized secondary shell layer (Fig. 2D). This reveals that the lath-like surface is not an artefact of preservation, but is a genuine representation of the primary shell layer, which can be traced consistently in fossil craniides and craniopsides. Moreover, the significant part of the area in the dorsal valve umbonal area bears distinct radiating laths, and was thus not secreted simultaneously along the whole surface of the mantle, but was formed by accretionary growth after metamorphosis was completed.
A single ventral valve from the same locality and horizon (Craniidae gen. et sp. indet. 1; Fig. 2A,B), may be conspecific with the dorsal valves described above, but this cannot be confirmed positively. The ventral valve is flat and smooth, lacking any radial ornament. A cicatrix attachment area about 850 μm across is present in the central part of the shell: it lacks any sign of growth and is ornamented by a mosaic of irregular tablets (Fig. 2A,B). The cicatrix is delineated by an indistinct halo, outside which the first growth lamella is present. The lamellose outer region of the valve bears characteristic laths. No primary attachment scar can be observed in the central area of the valve. By analogy with Orthisocrania (Popov et al. 2010) it can be inferred that mineralization of the ventral valve in Silurian craniides was delayed substantially.
In our specimens of Ordovician Orthisocrania curvicostae, there is a similar, almost smooth umbonal area 750–800 μm across, representing a post-metamorphic shell. The pattern with laths is preserved on the surface of the brephic shell (Popov et al. 2010; fig. 1E,G), but it is not as well expressed as in the Silurian shells. However, the brephic shell exhibits a remarkable variation in shape, and is often asymmetrical to various degrees. In particular, the brephic shell illustrated by Popov et al. (2010), Fig. 1G) displays an almost flat, steeply inclined right hand side (left on Fig. 1G) bounded by an almost straight growth line, whereas on the opposite side of the brephic shell, it is distinctly wider and broadly rounded (right on the photograph). This pattern was developed probably after settlement and resulted from encrusting attachment of the shell. Another specimen (Fig. 1H,I) preserves a very narrow, elongate brephic shell, which is strongly convex medially, becoming flattened laterally. The ventral valve of this specimen was illustrated by Popov et al. (2010), fig. 2D), illustrating that the shell was growing over a cylindrical object, and the unusual, elongate shape of the dorsal brephic shell is a direct reflection of the uneven surface on the hard substrate used for attachment on settlement. Even if the presence of laths in Orthisocrania can be questioned from our previous illustrations (as interpreted by Freeman & Lundelius 2011), the asymmetrical shape of the dorsal brephic shell in combination with distinct growth marks suggests that it was formed by accretionary growth after settlement, as in Silurian craniides.
The juvenile craniide illustrated by Madison (2007), pl. 5, figs 1, 2) is also clearly asymmetrical. This feature was not discussed in that publication, but a certain degree of asymmetry in craniide brephic shells suggests that they were formed after settlement, and that most probably they were post-metamorphic.
Discussion
Discrimination of metamorphic and post-metamorphic shell
Following the pioneering studies of Freeman & Lundelius (1999, 2005), the size of the ‘protegulum’ has been used as a major criterion for inferring planktotrophy or lecithotrophy in extinct brachiopods. This criterion is based on the assumption that the protegulum of the lecithotrophic larva does not exceed the maximum size of the brachiopod egg (220 μm). With this simple approach it is important to be able to discriminate and measure growth marks as preserved on the umbonal area of the shell; these are assumed to delineate discontinuities in shell growth related to major changes in life habit (Chuang 1977). In linguliform brachiopods, the transition from a metamorphic to a brephic shell is accentuated frequently by a correlative change in surface micro-ornament (Holmer 1989; Williams 2003). However, the application of this method to rhynchonelliform and craniiform shells is not straightforward, partly because of their calcareous composition, which was subjected to substantially different taphonomic pathways by comparison with the better-preserved linguliforms. In particular, calcareous shell fabrics may have been partially or completely re-crystallized, especially in shells composed of aragonite and high magnesium calcite. The micro-granular layer characteristic of the metamorphic shell in Recent rhynchonelliforms is rarely fossilized to any degree.
Further complications were also described by Nielsen (1991), who clearly demonstrated that the metamorphic protegulum in Novocrania is just about 70–80 μm wide, and that it is practically indistinguishable from the full-grown metamorphic shell at the end of metamorphosis, which is 240 μm in diameter. Observations on the dorsal umbonal region of Novocrania (Popov et al. 2010; Williams & Cusack 2007) suggest that only the outer boundary of the full grown metamorphic shell is defined by a distinct halo. Thus, if only the ‘protegulum’ criterion is applied, the metamorphic shell of Novocrania can be misinterpreted easily as belonging to planktotrophic larvae.
Furthermore, Stricker & Reed (1985a, b), demonstrated that the shell of Recent Terebratalia transversa begins to show evidence of accretionary growth up to 4 days before the initiation of the continuous secretion of the fibrous secondary layer. Thus, the size of a fully grown metamorphic shell comprising micro-granular calcite and outlined by a halo in T. transversa exceeds the size of the protegulum, which is defined as having been secreted simultaneously across the whole surface of the larval mantle (Williams et al. 1997). Moreover, Lüter & Hoffmann (2010) demonstrated that Recent thecideide species have an exceptionally large protegular size (up to 580 μm wide in Thecidellina meyeriHoffmann & Lüter 2009), because of post-attachment contraction, which flattens the animal. It was also documented by the same authors that the protegulum of such large size is secreted within seconds after attachment. This may suggest that the protegular size in rhynchonelliforms mainly reflects the size of the larval mantle, and there is no strict correlation with the feeding habit of the larva.
However, other criteria can be applied. The end of metamorphosis in craniiform and rhynchonelliform brachiopods coincides with differentiation of the adult mantle, when a so-called ‘conveyer belt’ mode of secondary shell secretion commenced. The area of the metamorphic shell is delineated not only by a halo, but also shows significant difference in the nature of its secondary shell fabric, which can be revealed by brief etching of the shell surface with EDTA. The shell fabric inside the halo (delineating the metamorphic shell) was secreted simultaneously by the outer epithelium at the termination of metamorphosis; it comprises an irregular mosaic of tablets, whereas the surface outside the halo shows fibrous or laminar structure developed as a result of accretionary growth (Popov et al. 2007; Bassett et al. 2008b).
The original shell structure in Palaeozoic craniiforms is affected invariably by secondary alterations; however, in well-preserved specimens, the outer shell surface replicates a distinctive pattern of primary shell layer, which is expressed as radially arranged laths (Popov et al. 2007; Williams & Cusack 2007, p. 2486). The appearance of the lath pattern outside the halo can be taken as a clear indication of the commencement of post-metamorphic shell secretion.
Discrimination of embryonic shell
Precise discrimination of the embryonic protegulum is also not straightforward. In fact, Recent Lingula is the only brachiopod with a well-defined embryonic protegulum (Yatsu 1901), whereas in Recent discinoids, craniides, rhychonellides, thecideides and terebratulides, the protegulum is secreted post-embryonically (Williams et al. 1997; Williams et al. 2001). Thus, the embryonic shell in lingulids is more probably a derived novelty, but the time of origin of this particular character is unclear. The problem is that the thin-shelled umbonal region even in juvenile lingulides is often abraded, especially in the ventral valve, probably by the pedicle in vivo. The ‘embryonic’ protegulum of the Devonian lingulide illustrated by Balinsky (1997) preserves radial ornament, which can be produced only around the adult marginal mantle setae and it was thus formed most probably post-embryonically, as has been demonstrated for discinids (Chuang 1977). It is also important to note that the discinid protegulum illustrated by Chuang (1977) is well within the size of the brachiopod egg and metamorphic shell of similar size in fossil discinoids, and can be misinterpreted as embryonic. Therefore, the presence of an embryonic shell outside of the Linguliformea is difficult to prove. There is always a reasonable probability that the protegulum was formed post-embryonically, during the free-swimming stage or later, after settlement.
The inferred presence of an embryonic shell in extinct craniides and craniopsides (Freeman & Lundelius 1999) is highly speculative and remains weakly founded. Currently, the presence of an embryonic shell is documented convincingly only in living lingulids, where it most probably represents a derived character, which evolved late in lingulate evolution. The possible presence of a truly embryonic shell in Palaeozoic linguliforms requires further study and confirmation.
Planktotrophic versus lecithotrophic larvae in Palaeozoic brachiopods
There is indeed good evidence that not only linguliforms, but a large majority of Cambrian and Ordovician rhynchonelliforms (probably including all strophomenates) had planktotrophic larvae. The type of planktotrophic larva that was first described in paterinides (see Williams et al. 1997) may represent a plesiomorphic character, which was inherited also by rhynchonelliforms, including most strophomenates, gonambonitids (Bassett et al. 2008a, b; Popov et al. 2007), orthoids (e.g. Madison 2004), siphonotretides (Popov et al. 2010), the enigmatic Salanygolina (Holmer et al. 2009) and probably also the earliest lingulides (Balthasar 2009); it can be traced also down to the stem group brachiopods (Balthasar 2004; Holmer & Popov 2007). The dorsal metamorphic shell in the ‘paterinide’ type of larva exhibits a median mound, which can be interpreted as a metamorphic protegulum, together with two pairs of inflated lobes, which most probably correspond to the position of the larval setal sacs (Williams et al. 1998; text-fig. 3). It is possible that ventral mantle differentiation and secretion of the ventral valve was delayed in both strophomenates and Salanygolina, but they also preserve other basic features characteristic of the ‘paterinide’ larva (Holmer et al. 2009). Another important feature in all these groups is that the metamorphic shell was possibly very weakly mineralized, but most probably entirely organic in composition, and secretion of the mineralized shell started at the end of metamorphosis, unlike in the lecithotrophic larva of rhynchonelliforms. Therefore, the rigid and probably mineralized protegulum (within a maximum brachiopod egg size) can be taken as evidence of a lecithotrophic larval habit.
Currently, lingulids are the only known brachiopods to have an embryonic protegulum. However, Lingula is the only brachiopod in which almost all metamorphic changes are completed at the embryonic stage (Yatsu 1901). Shortly after hatching, the juvenile Lingula exhibits all main features of an adult animal, and it lacks embryonic setae, but has ‘adult’ mantle setae; moreover, the bivalved, mineralized shell is secreted by a fully differentiated ‘adult’ mantle. Thus, it is most closely comparable (in terms of shell morphology and anatomy) not with the larva, but with the post-metamorphic (brephic) shell of rhynchonelliform and craniiform juveniles. The discinids diverged from the linguloids sometime before the end of the Cambrian, and they differ from linguloids in retaining a pair of larval setal sacs, which form at the beginning of a free-swimming stage, but are lost and replaced by adult setae (Lüter 2001, 2007). The protegulum of Recent discinids is formed post-embryonically. It is probable that heterochrony was involved early in linguloid evolution. In that respect the discinids appear to be less derived as compared with the lingulides, and a basically discinide type of ontogeny appears to have been present in the paterulids as early as the late Cambrian (Ghobadi-Pour et al. 2011). It is interesting to note also that, in phylogenetic analyses (Holmer & Popov 2000; fig. 38; Williams 2003, text-fig. 6), paterulids invariably emerge as the sister group of discinoids. It is possible that the type of ontogeny observed in paterulids and discinoids represents a plesiomorphic character, which evolved in their common ancestor before the Furongian.
Conclusions
Our new data from Ordovician and Silurian craniides and craniopsides indicate clearly that they did not have a planktotrophic larva, in contradiction to the recent suggestions of Freeman & Lundelius (1999, 2011). Evidence for a lecithotrophic larva in these groups can be inferred from detailed studies of shell structure and shell formation/growth, which include early differentiation of an adult dorsal mantle, the presence of a primary layer with a characteristic lath-like pattern, and asymmetry of a brephic shell in taxa with an encrusting life strategy.
There is also no evidence for the presence of an embryonic shell in the extinct craniiformeans. An embryonic shell may be a derived feature that evolved in lingulides as late as the Mesozoic.
Detailed comparison of the similarities of the attachment mode in strophomenates and craniiforms does not necessarily indicate that it is an apomorphic character. Similar modes of attachment have been documented also in the early Cambrian chileides and Salanygolina (Holmer et al. 2009), and this type of attachment may have evolved early in brachiopod stem groups.
Acknowledgements
Leonid Popov and Michael Bassett acknowledge logistical and financial support from the National Museum of Wales. The work of Lars Holmer was supported by grants from the Swedish Natural Sciences Research Council (VR). We are grateful to Michal Mergl (University of West Bohemia, Plzen) and anonymous reviewer for useful and constructive comments on the manuscript.
References
Balinsky, A. 1997: Evolution of the embryonic development in lingulid brachiopods. Acta Palaeontologica Polonica 42, 45–56.
Balthasar, U. 2004: Shell structure, ontogeny, and affinities of the Lower Cambrian bivalved problematic fossil Mickwitzia muralensis Walcott, 1913. Lethaia 37, 381–400. https://doi.org/10.1080/00241160410002090.
Balthasar, U. 2009: The brachiopod Eoobolus from the Early Cambrian Mural Formation (Canadian Rocky Mountains). Paläontologische Zeitschrift 83, 407–418.
Bassett, M.G., Popov, L.E. & Egerquist, E. 2008a: Pedicle preservation in a Silurian rhynchonelliformean brachiopod from Herefordshire, England: Soft-tissue or an artefact of interpretation? Earth and Environmental Science Transactions of the Royal Society of Edinburgh 98(for 2007), 303–308.
Bassett, M.G., Popov, L.E. & Egerquist, E. 2008b: Early ontogeny of some Ordovician–Silurian strophomenate brachiopods: Significance for interpreting evolutionary relationships within early Rhynchonelliformea. Fossils and Strata 54, 13–20.
Chuang, S.H. 1977: Larval development in Discinisca (inarticulate brachiopod). American Zoologist 17, 39–54.
Freeman, G. & Lundelius, J.W. 1999: Changes in the timing of mantle formation and larval life history traits in linguliform and craniiform brachiopods. Lethaia 32, 197–217.
Freeman, G. & Lundelius, J.W. 2005: The transition from planktotrophy to lecithotrophy in larvae of Lower Palaeozoic Rhynchonelliform brachiopods. Lethaia 38, 219–54.
Freeman, G. & Lundelius, J.W. 2011: Ontogeny of Early Palaeozoic Craniata. Comment: The evidence that Orthsocrania and Craniops had lecithotrophic larvae is not compelling. Lethaia 44, 245–246.
Ghobadi-Pour, M., Kebriaee-Zadeh, M.R. & Popov, L.E. 2011: Early Ordovician (Tremadocian) brachiopods from Eastern Alborz Mountains, Iran. Estonian Journal of Earth Sciences 60, 65–82.
Hoffmann, J. & Lüter, C. 2009: Shell development, growth and sexual dimorphism in the Recent thecideide brachiopod Thecidellina meyeri sp. nov. from the Lesser Antilles, Caribbean. Journal of the Marine Biological Association of the United Kingdom 89, 469–479.
Holmer, L.E. 1989: Middle Ordovician phosphatic inarticulate brachiopods from Västergötland and Dalarna, Sweden. Fossils and Strata 26, 172.
Holmer, L.E. & Popov, L.E. 2000: Subphylum Linguliformea, 30-146. In Kaesler, R. (ed.): Treatise on Invertebrate Paleontology. Part H Brachiopoda (Revised) 1. Geological Society of America and University of Kansas Press, Boulder and Lawrence, 30–146.
Holmer, L.E. & Popov, L.E. 2007: Stem-group brachiopods. In Selden, P.A. (ed.): Treatise on Invertebrate Paleontology. Part H Brachiopoda (Revised) 6 (Supplement). Geological Society of America and University of Kansas Press, Boulder and Lawrence, 2396–2521. 2580–2590.
Holmer, L.E., Popov, L.E., Bassett, M.G. & Laurie, J. 1995: Phylogenetic analysis and classification of the Brachiopoda. Palaeontology 38, 713–741.
Holmer, L.E., Pettersson Stolk, S., Skovsted, C.B., Balthasar, U. & Popov, L.E. 2009: The enigmatic Early Cambrian Salanygolina– a stem group of rhynchonelliform chileate brachiopods? Palaeontology 52, 1–10.
Homer, L.E., Skovsted, C.B., Brock, G.A. & Popov, L.E. 2011: An early Cambrian chileate brachiopod from South Australia and its phylogenetic significance. Memoirs of the Association of Australasian Palaeontologists 41, 289–294.
Huene, F. 1899: Zur Systematik der Craniaden. Neuen Jahrbuch fur Mineralogie, Geologie und Paleontologie Bd. 1, 138–151.
Lüter, C. 2001: Brachiopod larval setae – a key to the phylum’s ancestral life stile? In Bruton, C.H.C., Cocks, L.R.M.Y. & Long, S.L. (eds): Brachiopods Past and Present. Systematic Association Special Volume Series 63, 46–55.
Lüter, C. 2007: Anatomy. In Selden, P.A. (ed.): Treatise on Invertebrate Paleontology. Part H Brachiopoda (Revised) 6 (Supplement). Geological Society of America and University of Kansas Press, Boulder and Lawrence, 2321–2355.
Lüter, C. & Hoffmann, J. 2010: Protegular secretion in thecideide brachiopods larval size matters. 6th International Brachiopod Congress, Melbourne, Australia, February 2010, Geological Society of Australia, Abstracts 95, 70
Madison, A.A. 2004: The first finds of the larval shells in the Ordovician orthides. Doklady Akademii Nauk 296, 223–226.
Madison, A.A. 2007: Pervyye nakhodki lichinochnykh rakovin kraniid v ordovikie Pskovskoi oblasti. Paleontologicheskii Zhurnal 2007, 16–18.
Nielsen, C. 1991: The development of the brachiopod Crania (Neocrania) anomala (O.F. Müller) and its phylogenetic significance. Acta Zoologica 72, 7–28.
Popov, L.E., Egerquist, E. & Holmer, L.E. 2007: Earliest ontogeny of Middle Ordovician rhynchonelliform brachiopods (Clitambonitoidea and Polytoechioidea): Implications for brachiopod phylogeny. Lethaia 40, 85–96.
Popov, L.E., Bassett, M.G., Holmer, L.E. & Ghobadi Pour, M. 2009: Early ontogeny and soft tissue preservation in siphonotretide brachiopods: New data from the Cambrian-Ordovician of Iran. Gondwana Research 16, 151–161.
Popov, L.E., Bassett, M.G., Holmer, L.E., Skovsted, C.B. & Zuykov, M.A. 2010: Earliest ontogeny of Early Palaeozoic Craniiformea: Implications for brachiopod phylogeny. Lethaia 43, 323–333.
Sowerby, J.D.C. 1839: Shells, 589–712. In Murchison, R.I. (ed.): The Silurian System. John Murray, London, 768 pp.
Stricker, S.A. & Reed, C.G. 1985a: The ontogeny of shell secretion in Terebratalia transversa (Brachiopoda, Articulata): 2. Formation of the protegulum and juvenile shell. Journal of Morphology 183, 251–272.
Stricker, S.A. & Reed, C.G. 1985b: The protegulum and juvenile shell of a recent articulate brachiopod: Patterns of growth and chemical composition. Lethaia 18, 295–303.
Williams, A. 2003: Microscopic imprints on the juvenile shells of Palaeozoic linguliform brachiopods. Palaeontology 46, 67–92.
Williams, A. & Cusack, M. 2007, 2396–2521. In Selden, P. A. (ed.): Treatise on Invertebrate Paleontology, Part H, Brachiopoda (Revised) 6. Geological Society of America and the University of Kansas Press, Boulder and Lawrence.
Williams, A., James, M.A., Emig, C.C., Mackay, S. & Rhodes, M. 1997: Anatomy, 7–188. In Kaesler, R. (ed.): Treatise on Invertebrate Paleontology. Part H Brachiopoda (Revised) 1. Geological Society of America and University of Kansas Press, Boulder and Lawrence.
Williams, A., Lüter, C. & Cusack, M. 2001: The nature of siliceous mosaics forming the first shell of the brachiopod. Discinisca. Journal of Structural Biology 134, 25–34.
Williams, A., Popov, L.E., Holmer, L.E. & Cusack, M. 1998: The diversity and phylogeny of the paterinate brachiopods. Palaeontology 41, 221–262.
Yatsu, N. 1901: On the development of Lingula anatina. Journal of the College of Science, Imperial University, Tokyo, Japan 17, 1–112.
Zuykov, M.A. & Butts, S.H. 2008: Glyptorthis (Foerste, 1914) and Bassettella new genus (Brachiopoda: Orthida) from the Late Ordovician of the East Baltic. Journal of Paleontology 82, 197–200.
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Copyright © 2012 Lethaia Foundation.
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Received: 16 December 2011
Accepted: 16 March 2012
Published online: 2 August 2012
Issue date: 1 October 2012
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