TESTING the PROTOZOAN HYPOTHESIS for EDIACARAN FOSSILS: a DEVELOPMENTAL ANALYSIS of PALAEOPASCICHNUS by JONATHAN B

Home , Allogromiida, Palaeopascichnus, Palaeophragmodictya

[Palaeontology, Vol. 54, Part 5, 2011, pp. 1157–1175]

TESTING THE PROTOZOAN HYPOTHESIS FOR EDIACARAN FOSSILS: A DEVELOPMENTAL ANALYSIS OF PALAEOPASCICHNUS by JONATHAN B. ANTCLIFFE1, ANDREW J. GOODAY2 and MARTIN D. BRASIER3 1Department of Earth Sciences, University of Bristol, Wills Memorial Building, Queen’s Road, Bristol BS81RJ, UK; e-mail: [email protected] 2National Oceanography Centre, Southampton, University of Southampton Waterfront Campus, European Way, Southampton SO14 3ZH, UK; e-mail: [email protected] 3Department of Earth Sciences, Oxford University, South Parks Road, Oxford OX1 3AN, UK; e-mail: [email protected]

Typescript received 21 October 2009; accepted in revised form 16 May 2011

Abstract: The hypothesis that the Ediacara biota were giant isms usually referred to the Ediacara biota, such as Charnia protozoans is tested by considering the external morphology, and Dickinsonia. Developmental analysis of the Palaeopascich- internal organization, suggested fossil representatives and nus – central to the xenophyophore hypothesis – reveals unu- molecular phylogeny of the xenophyophores. From this anal- sual, protozoan features, including evidence for chaotic repair ysis, we find no case to support a direct relationship. Rather, structures, for mergence of coeval forms, as well as complex the xenophyophores are here regarded as a group of recently bifurcations. These observations suggest that Palaeopascichnus evolved Foraminifera and are hence unlikely to have a record is a body fossil of an unidentified protozoan but is unrepre- from the Ediacaran Period. Further from the growth dynam- sentative of Ediacaran body construction, in general. ics of Foraminifera, they are also unlikely to be related to the Palaeopascichnus organism. We also find significant distinc- Key words: Palaeopascichnus, Ediacara biota, Protozoa, xeno- tions in the growth dynamics of Palaeopascichnus and organ- phyophores, development, evolution.

The fossil record contains a great conundrum; the mod- 1994), who questioned the evidence for continuity ern animal phyla appear already distinguished as fossils between the Ediacara biota and succeeding Cambrian within the Cambrian System (Brasier 1979). This system metazoans. Seilacher (1989) also challenged the taxonomy lies immediately above the recently named Ediacaran Sys- by stating that many Ediacaran organisms share a com- tem (Knoll et al. 2004). From the time of Darwin to the mon construction. This was taken to imply that they are, discovery of the global Ediacara biota (Gu¨rich 1933; for the most part, a single clade unrelated to modern Sprigg 1947; Ford 1958), the ancestry of animals has groups. A profusion of taxonomic affinities has followed remained one of the most exciting mysteries in science. (e.g. Dzik 2003; Gehling 1991; Jenkins 1992; Valentine Indeed, Darwin (1859) stated that one of the greatest flaws 1992; Seilacher 2003; Seilacher et al. 2003; Peterson et al. in his hypothesis was the lack of demonstrable ancestry to 2003; Narbonne 2005). These taxonomies were based the recognized phyla that appear distinct at the base of the upon simple morphological, ecological and functional known fossil record (then ‘Silurian’, now the base of the comparisons. Latterly, this has been shown to be insuffi- Cambrian). After the great antiquity of the Ediacara biota cient as a rationale (see Antcliffe and Brasier 2008; Brasier had been realized (Ford 1958), then the Ediacara biota and Antcliffe 2009). was interpreted as primitive metazoans (Glaessner 1966, To date, there has been only one attempt at a cladistic 1984; Glaessner and Daily 1959; Glaessner and Wade analysis of the features of Ediacaran body fossils (Brasier 1966; Wade 1972; Jenkins 1984, 1985, 1992, 1995; Jenkins and Antcliffe 2009). Cladistic analysis arose from a con- and Gehling 1978; McMenamin 1986, 1998; Bengtson sideration of the flaws that can arise when relationships 2003), thereby providing putative solutions to the long are inferred from the use of functional analogues alone. posed problem regarding animal ancestry. Cladists argue that we must seek homologies instead (see This view of Ediacaran palaeobiology was refocused by Patterson 1982 for a complete discussion of the nature of Seilacher (1984, 1985, 1989, 1992; also Buss and Seilacher homology; see also De Beer 1971). It is clear from such

ª The Palaeontological Association doi: 10.1111/j.1475-4983.2011.01058.x 1157 1158 PALAEONTOLOGY, VOLUME 54 methods that the establishment of relationships based not been demonstrated) to prove that they are related only on ecological and functional comparisons will be (i.e. both single-celled xenophyophores). These assump- ambiguous at best and misleading at worst. We have tions therefore entail the conclusions. That being so, then explored this question of homology at length elsewhere the potential xenophyophore affinities of the Ediacara (Brasier and Antcliffe 2004; Antcliffe and Brasier 2007b, biota appear to be questionable. Further, the basis for 2008), and we emphasize that for enigmatic fossils, such these assumptions can also be regarded as questionable. as the Ediacara biota, the most convincing route to estab- For example, there is now good evidence that many lish the hypotheses of biological affinity is likely to arise members of the frondose Ediacara biota (e.g. Charnia) from attempts to understand their developmental pro- lived at a great variety of water depths (Dalrymple and gramme. Narbonne 1996; Wood et al. 2003). Their abundance below the photic zone has therefore led Narbonne (1998, 2005) to dismiss the suggestion of McMenamin (1986, THE XENOPHYOPHORE HYPOTHESIS 1998) that such fronds housed photoautotrophic endosymbionts in a manner similar to modern cnidarians. Seilacher et al. (2003), following the conception by Zhu- Further to this, all known xenophyophores currently inha- ravlev (1993), suggested that many members of the Edia- bit the deep sea (500–8000 m; Lemche et al. 1976), making cara biota could be regarded as relatives of an extant it highly unlikely that the architecture of their tests is con- group of amoeboid protozoans, the xenophyophores. The nected to housing photoautotrophic endosymbionts. latter group was established by Schulze (1906) and has The Ediacaran fossil Palaeopascichnus, found in Austra- been placed at different taxonomic levels from a family to lia, northern Norway, Avalonia (Newfoundland Canada, a phylum (Tendal 1996). Seilacher et al. (2003) suggested, Wales, Central England) and the Ukraine, has hitherto for the first time, that a protozoan organization is appro- been central to the xenophyophore hypothesis. Below, the priate for the Ediacara biota. It is important to note that morphology and development of this fossil is analysed these authors exempted the following Ediacaran organ- and contrasted with that of foraminiferan groups and, in isms from xenophyophore affinity: Kimberella, which is particular, with xenophyophores. Finally, we will examine regarded as ‘probably a mollusc’ (following Fedonkin and whether other members of the Ediacara biota were proto- Waggoner 1997), and Arkarua Gehling, seen sceptically zoan. as ‘a possible echinoderm’ (following Glaessner 1984; Gehling 1987). An affinity between the many remaining Ediacaran fos- DEVELOPMENTAL ANALYSIS OF sils and the xenophyophores was based on the following PALAEOPASCICHNUS line of reasoning, here summarized from the study by Seilacher et al. (2003). First, the external morphology of The fossil Palaeopascichnus Palij, 1976 was first described the xenophyophores closely resembles that of certain Edi- as an ichnofossil (Palij et al. 1979) from the Ediacaran acaran ‘trace fossil’ genera such as Yelovichus, Palaeopasc- (Vendian) of the Ukraine. Fedonkin (1978) considered ichnus, Neonerites and Intrites. Secondly, the Ediacara these specimens to represent the traces made by alternate biota shows structural features that are ‘similar’ to those right and left movements of an animal feeding appendage seen in the xenophyophores, argued to be adaptations for upon the bedding plane. Comparable, but poorly pre- unicellular gigantism. These adaptations include ‘similar- served material was discovered in Australia in the late ity in cell shape, subdivision of the cell and the nature of 1980s, but this was considered by Haines (1987 unpub- the fill skeletons.’ Finally, these authors inferred the pres- lished thesis, 1990) to represent algal body fossils rather ence of photoautotrophic endosymbionts, much as seen than animal traces. Haines (2000) later examined better in many extant larger benthic Foraminifera that divide a preserved material from Australia, inferring it to be of giant cell into compartments, to create smaller chamber- algal (possibly of phaeophyte) affinity based on simple lets for the housing of symbionts (e.g. Alveolina, Nummu- morphological comparisons with the extant calcareous lites and Fusulina; Armstrong and Brasier 2004). brown alga Padina. By this time, Jenkins (1995) had It is important to note here that xenophyophores are already argued that these Australian specimens were recognized and classified into families and genera partly meandering trace fossils of unknown affinity. Gehling on the basis of their internal organization, meaning their et al. (2000) dismissed this view because of taphonomic fossil record can be expected to be problematic. The features that were not, unfortunately, described. Jensen problem here is that Seilacher et al. (2003) have inferred (2003) analysed the material of Palaeopascichnus, Yelovich- a shared evolutionary constraint (i.e. how to make a small nus and Neonereites and considered these forms to be cell bigger) based on the assumption that they are similar taphomorphs that can occasionally be seen to grade into (i.e. assuming that they are both single celled, which has each other if preservation style permits. Further, the ANTCLIFFE ET AL.: EDIACARAN FOSSILS: DEVELOPMENT OF PALAEOPASCICHNUS 1159

‘meandering’ structures in Yelovichnus are not truly pascichnus is a horizontally spreading structure that is meandering but instead form closed ovals in a series; typically thin and flat. It comprises a linear array of though, this is not always apparent. This appearance of curved depressions (here, for convenience, called cham- meandering is caused by the ‘close juxtaposition of the bers) that are always wider than long and convex towards oval units,’ (Jensen 2003, p. 223) the very same oval units the direction of growth (Text-fig. 3A). These chambers do that comprise Palaeopascichnus. Jensen (2003, p. 223) goes not appear to have any perforations or foramina of the on to state that ‘it is clear that a trace fossil origin must kind typically seen in foraminiferan tests preserved be abandoned for Palaeopascichnus.’ Dong et al. (2008) suggested synonymy of Palaeopascichnus with Horodiskya, based on the material of Palaeopascichnus sp. recently dis- A covered in China. This material will not be further discussed here, yet we find it interesting to note that the Palaeopascichnus of Dong et al. (2008) is an order of magnitude smaller than those found elsewhere in the world and is found in a different taphonomic regime. Following these arguments, it remains to be stated that these fossils are, indeed, body fossils, an idea pursued by Seilacher et al. (2003). The latter have compared these forms with giant Foraminifera, an idea recently reiterated by Dong et al. (2008). Specimens illustrated here (Text-fig. 1A–C) were col- lected from the Wonoka Formation by Haines (2000) at Parachilna Gorge in the Flinders Ranges, South Australia. They lie some 700 m below the classic Ediacara biota- bearing member of the Rawnsley Quartzite (after Haines B 2000). Examples of Palaeopascichnus delicatus associated with Aspidella have also been examined by us from the top surfaces of bedding plains in the Fermeuse Forma- tion, at Ferryland in SE Newfoundland (cf. Gehling et al. 2000), as well as in the beds beneath the base of the Cambrian in the Manndraperelva Member of the Stappogiedde Formation of the Digermul Peninsula of northern Norway (see Crimes and McIlroy 1999), the latter now housed in Oxford University Museum. The range of morphological and developmental feature seen in these fossils is illustrated in Text-figure 2. Palaeo-

TEXT-FIG. 1. A, an example of the Palaeopascichnus sp. from C the Wonoka Formation, South Australia. Material is held in the South Australian Museum, SAM-P36854. View is 15 cm across. B, the details of the fossil are picked out with overlay, and the black lines are placed at the front crest of a chamber. C, view with seemingly different individuals highlighted in different colours. Labels 8 and 10 refer to features described in Table 1. These are: 8. Converging chambers can merge (coeval forms of the same strain); 10. Chambers of noncoeval forms overlie each other (post-mortem). The colours help delineate the places where various forms are seen to be merging and diverging. For instance, in the top left of the ﬁgure, the light blue form and the yellow form merge to produce the green form. This green form then merges with a dark blue form to produce a turquoise form. The yellow form appears to emerge from the junction where the red and orange forms have been colliding. The chambers are convex towards the direction of growth. 1160 PALAEONTOLOGY, VOLUME 54

sive chambers in Palaeopascichnus can often be seen to increase gradually in the growth direction (Text-fig. 3A), although chamber widths can also remain unchanged (Text-fig. 3B) or even decrease (Text-fig. 3E) in the growth direction, but seemingly only after bifurcation. The length of successive chambers tends to remain nearly constant (Text-fig. 3B). Even so, both width and length can vary from one specimen to another. Palaeopaschichnus demonstrates that a variety of growth irregularities can be transmitted from one chamber to the next (Text-fig. 3D) Several specimens also show chaotic chambers that may be the result of chamber repair after damage (Text-fig. 4D). Other specimens can have chambers that show faint transverse partitions, perhaps because the growth programme had become disorganized in some way (Text-fig. 4E), although this may potentially be a taphonomic artefact. Bifurcations in the organism seem to occur at a point where chamber width has approached a certain critical mass or width; though, this threshold seems to vary from specimen to specimen (Text-fig. 3E). Some forms overlie each other (Text-fig. 4C), in what appears to be a post-mortem succession. The chambers in coeval – but separate – forms in some cases merge com- pletely, to form a combined organism of much greater TEXT-FIG. 2. A schematic diagram illustrating the chamber width (Text-fig. 4A). Chamber length seems to developmental features here observed in Palaeopascichnus sp. be little affected by this merging. Interestingly, when such Labels refer to features described in Table 1. 1. Arcuate coeval forms are seen to merge, they are nearly always of chambers are wider than long and convex forwards. 2. Chambers have a constant length. 3. Chamber depth is comparable dimensions. No instances have been found unknown but is thought to have been thin and flat. 4. Width of where small and large forms can be observed to merge. In chambers increases with growth. 5. Growth irregularities can be Text-figure 4B, it can be seen that overcrowding of coeval transmitted to next chamber. 6. Chambers branch when they specimens was followed by the termination of one branch, approach a certain critical mass ⁄ width. 7. Branching is preceded while a second continued to grow and to occupy its living by a partition wall in the parent chamber. 8. Converging space (assuming, of course, they are coeval). Interestingly, chambers can merge. 9. Growth is terminated by overcrowding the large form always seems to have taken precedence in some forms. 10. Chambers of noncoeval forms overlie each over the small form. other (see Text-fig. 1). 11. Damaged forms can show rather Four parameters that were measured from these Palaeo- chaotic chambers. 12. Some chambers show transverse partitions pascichnus specimens from the Wonoka Formation, South as though the growth programme has been confused. 13. Australia, are illustrated in Text-figure 5. These parameters Chambers do not appear to have any perforations. 14. Small and large forms never merge. See text and Table 1 for the are as follows: W1 is the width of the first chamber in the significance of these features. specimen as measured; W2 is the width of the last chamber in the specimen as measured; L is the length of the specimen as measured, taken to be from the back of throughout the Phanerozoic (cf. Armstrong and Brasier the first chamber to the front of the last chamber; and n is 2004). The chamber depth is also unknown but it appears the number of chambers. The data gathered across seven to have been slight (Text-fig. 3C). It should be noted that slabs containing Palaeopascichnus specimens are shown in there are two main taphotypes of Palaeopascichnus: the the Appendix S1. It is unclear whether Palaeopascichnus first is that of the Wonoka Formation where the fossil had deterministic growth (i.e. a programmed termination forms a shallow depression (negative hyporelief); the sec- of growth); thus, it is not certain what could be consid- ond is that found elsewhere (Avalonia and northern Nor- ered a fully mature specimen. Thus, no complete ontoge- way in this study) where the fossil develops a slight ridge netic map can be produced; though, we are still able to (positive epirelief). This is very much in line with the take measurements from different stages of ontogeny and general preservation difference expected between these form a picture of the growth dynamics of organisms. sites and can be observed in many other taxa across these The width ratio (W2 ⁄ W1) varies between 1 and 4.67; two regimes (see Brasier et al. 2011). The width of succes- though, the 1st and 9th deciles are 1.37 and 2.86 respec- ANTCLIFFE ET AL.: EDIACARAN FOSSILS: DEVELOPMENT OF PALAEOPASCICHNUS 1161

B 2

A 1 and 4

D 5

C 3 E 6

TEXT-FIG. 3. Developmental features of Palaeopascichnus illustrated in the schematic Text-figure 2, as exemplified by the Wonoka Formation material, South Australia Museum, all from specimens catalogued under SAM36864. The numbers relate to features seen in Text-figure 2 and Table 1 though given again here for convenience. 1. Arcuate chambers are wider than long and convex forwards. 2. Chambers have a constant length. 3. Chamber is thought to have been shallow and flat. 4. Width of chambers increases with growth. 5. Growth irregularities can be transmitted to next chamber. 6. Chambers branch when they approach a certain critical mass ⁄ width (see arrow for branching point). See text and Table 1 for the significance of these features. All segment lengths (the length of one sausage shaped unit) are approximately 1.5 mm. 1162 PALAEONTOLOGY, VOLUME 54

A 8 B 9

C 10 D 11 E 12

TEXT-FIG. 4. Further developmental features of Palaeopascichnus illustrated in the schematic Text-figure 2, as exemplified by the Wonoka Formation material, South Australia Museum, all from specimens catalogued under SAM-P36854. The numbers relate to features seen in Text-figure 2 and Table 1 though given again here for convenience. 8. Converging chambers can merge. 9. Growth is terminated by overcrowding in some forms. 10. Chambers of noncoeval forms overlie each other. 11. Damaged forms can show rather chaotic chambers. 12. Some chambers show transverse partitions (arrow) as though the growth programme has been confused. All segment lengths (the length of one sausage shaped unit) are approximately 1.5 mm. tively, indicating that although low values are common, That is to say, large specimens do not seem to be expand- expansion ratios beyond 3 are comparatively rare. Text- ing at a rate that is different from that in small speci-

figure 6A shows a plot of W1 vs W2 with an expansion mens. The amount of expansion (W2)W1), when plotted ratio of 1.65, showing good correlation. Specimens were (Text-fig. 6C) against specimen length, shows that in no not measured across a bifurcation as this would tend to specimen does the amount of expansion exceed length. conceal alteration in parameters, because only the first This again indicates the likely presence of a controlled and last chambers were studied. This correlation indicates morphogenetic programme, presumably formed in such a that, to some extent, initial size determines final size. way that the arc of a chamber does not cause any signifi- Consequently, the expansion rate does not vary greatly cant overlap with a previously formed chamber. This with growth. This pattern is further corroborated by the might be taken to imply that all of the chambers con- fact that a plot of expansion rate versus length (W2 ⁄ W1 tained living tissue at the same time and that old cham- vs L), as shown in Text-figure 6B, shows no correlation. bers were not abandoned, at least not immediately. ANTCLIFFE ET AL.: EDIACARAN FOSSILS: DEVELOPMENT OF PALAEOPASCICHNUS 1163

W2 explain the ability of forms to merge with their neighbours, as shown in feature 8 of Text-ﬁgures 2 and 4A. We ﬁnd that all slabs show good correlations (R2 ‡ 0.8), except for slab 6, which appears to show a bimodal pattern. The latter may be taken to imply that two strains were living in close proximity on a single bedding plane. This curious suite of L constructional and developmental features is only seen in Palaeopascichnus. It seems to be unique to this genus.

THE XENOPHYOPHORES W1 Tendal (1972, 1996) and Gooday and Tendal (2003) provide a complete review of this protozoan group. For many years, the study of xenophyophores was hindered by the delicate nature of many species and the difficulties TEXT-FIG. 5. Illustration of the four parameters measured for involved in sampling them in relatively inaccessible deep- each specimen of Palaeopascichnus, three of which are labelled. sea habitats (Text-fig. 7A). In recent years, however, W is the width of the first chamber in the specimen as 1 intact specimens recovered in box cores and multicores measured. W is the width of the last chamber in the specimen 2 and by manned and unmanned submersibles, as well as as measured. L is the length of the specimen as measured, taken to be from the back of the first chamber to the front of the last those photographed by remote camera systems, have chamber. The final parameter is the number of chambers, n. For greatly advanced understanding of the group. In the fol- the specimen here, n = 8. lowing, we briefly review their external morphology and internal organization before examining their phylogenetic The absolute values of width versus length show that relationships and fossil record. the length of the specimens typically exceeds width. In only one of 60 specimens did W1 exceed the length of the specimen, and in only a further nine of 60 specimens did Xenophyophore external morphology W2 exceed length (Text-fig. 6D). In these few specimens, it may be that the whole body of the specimen was not Xenophyophore tests range in size from several millime- visible to us, or not accounted for, perhaps owing to tres to 200 mm (Stannophyllum). The test is usually taphonomy. The final biometric consideration here con- agglutinated, often incorporating the tests of planktonic cerns the number of chambers plotted against the overall foraminiferans, radiolarians and sponge spicules, as well length of the specimen (n vs L). First of all, it is impor- as mineral grains. Many forms preferentially agglutinate tant to note that our measuring error is taken to be particular grain types (Tendal 1972; Kamenskaya 2005). approximately (and maybe rather generously) 0.05 cm. It The test form is basically monothalamous but highly was originally intended by us that the length of the indi- diverse and includes spherical, tubular, flat plate-like, vidual chambers would also be measured, but it emerged folded or contorted plate-like and reticulated morpho- that the pattern of variation was less than the typical types. Two orders are recognized by Tendal (1972, 1996). expected error range of 1 mm. Thus, it must be con- The test is rigid in the Psamminida but flexible and cluded that the length of individual chambers can be held incorporates proteinaceous fibres (linellae) in the Stanno- to be (at least to a reasonable first approximation) a con- mida. Such xenophyophores have been regarded variously stant. This means that the length of a specimen is primar- as Foraminifera, sponges or members of a distinct protis- ily controlled by the number of segments added and not tan group. However, as discussed elsewhere in the article, by the size of the chambers added. This is shown by the molecular evidence indicates that at least some species of value of L ⁄ n (i.e. the gradient of a plot of n vs L), which xenophyophore nest within the Foraminifera (see Rich- reveals almost no variation in specimens across a particu- ardson 2001; Pawlowski et al. 2003a; Lecroq et al. 2009; lar slab. Slabs 1 and 3 are particularly remarkable in this Gooday et al. 2011). regard, and their plots are shown in Text-figure 6E, F, respectively. Therefore, the ratio does seem to vary between slabs. This variation can be taken to imply that Internal organization the specimens on one slab are more alike that specimens on different slab. This may indicate that the specimens on Xenophyophores have a distinctive internal organization a given slab were cogenetic and that may then begin to (see Tendal 1972; Gooday and Nott 1982). In some gen- 1164 PALAEONTOLOGY, VOLUME 54

2.50 AB5.00 4.50 2.00 4.00 3.50 1.50 3.00 2 R = 0.8144 2.50 1.00 2.00 Width ratio 1.50 Maximum width 0.50 1.00 0.50 0.00 0.00 0.00 0.20 0.40 0.60 0.80 1.00 1.20 1.40 1.60 0.00 0.50 1.00 1.50 2.00 2.50 Minimum width Length of specimen

1.00 CD 0.90 2.50 0.80 0.70 2.00 0.60 1.50 0.50 0.40 Width Expansion 1.00 0.30 0.20 0.50 0.10 0.00 0.00 0.00 0.50 1.00 1.50 2.00 2.50 0.00 0.50 1.00 1.50 2.00 2.50 Length Length

3.00 EF1.40

2.50 1.20 2 R = 0.915 1.00 2.00 2 R = 0.9687 0.80 1.50 0.60 Length Length 1.00 0.40

0.50 0.20

0.00 0.00 0 2 4 6 8 1012141618 02468101214 Number of segments Number of segments

TEXT-FIG. 6. A, biometry of Palaeopascichnus, showing a plot of W1 vs W2 for all specimens. A fair degree of correlation is found for a trend line with gradient 1.65. This indicates that a typical rate of chamber of expansion is in the region of 1.65. B, plot of 2 W2 ⁄ W1 vs L for all specimens. The best polynomial regression that can be plotted (shown pale blue) only has an R value of 5 per cent, indicating almost no confidence in this correlation. As discussed in the text, this supports the idea that size is controlled by the relatively constant expansion rate and not the length of the organism. C, a plot of L vs W2)W1 for all specimens. The diagonal line marks where these two quantities equate. As can be seen, no specimens plot above this line and as such L always exceeds W2)W1.D, Plot of L vs W1 and W2 variables for all specimens. W1 is shown with blue diamonds, note the one outlier at (L, W) fi (1.03, 1.37). 2 W2 is shown with green squares. E, Plot of n vs L for Slab 1. The R value of 0.915 is for a correlation with gradient 0.128. Note that this regression automatically maps to the origin, which biologically makes sense – a specimen with no chambers should have no length. Error bars show ½ mm measuring error. F, Plot of n vs L for Slab 3. The R2 value of 0.969 is for a correlation with gradient 0.102, note quite different gradient from Slab 1. Note also that this regression automatically maps to the origin, which biologically makes sense – a specimen with no chambers should have no length. Error bars show ½ mm measuring error. era, the test interior is hollow, but otherwise it is filled at which are dark in colour, occupy the interior, often weav- least partly with agglutinated particles. Two other ele- ing between the internal agglutinated particles. The ments, the protoplasm, which is light in colour, and multinucleate protoplasm is contained within an organic masses of stercomata (waste pellets) called stercomare, sheath and forms a branching network (see below; ANTCLIFFE ET AL.: EDIACARAN FOSSILS: DEVELOPMENT OF PALAEOPASCICHNUS 1165

A B

TEXT-FIG. 7. Recent xenophyophores. A, living specimens photographed on the seaﬂoor (4300 m water depth in the Nazare´ canyon, Portuguese continental margin). The reticulated species is Reticulammina cerebreformis (diameter 7.5 cm); the bush-like species is Aschemonella ramuliformis. B, internal organisation of Aschemonella ramuliformis; the stippled structures are stercomare masses, the white structures are the granellare (cytoplasmic) strands. The specimen is about 8 mm long. Reproduced with permission from Gooday, A.J. and Nott, J.A., 1982. Intracellular barite crystals in two xenophyophores, Aschemonella ramuliformis and Galatheammina sp. (Protozoa: Rhizopoda) with comments on the taxonomy of A. ramuliformis. Journal of the Marine Biological Association, UK, 62, 595–605. C, undescribed xenophyophore from the eastern equatorial Paciﬁc (4150 m depth) with well-developed ‘growth lines’; the test is 9 cm wide. D, side view of test of Reticulammina cerebreformis from Nazare´ canyon (width 5.5 cm); note the ‘growth lines’ on one of the plate-like test elements.

Text-fig. 7B) that occupies <5 per cent by volume of the their ancient nature, by implying their survival in a deep- test (Levin and Gooday 1992). It contains crystals of sea refuge after competitive displacement from shallower barium sulphate (BaSO4), 2–5 lm in size, the origin and water depths. This, coupled with the presence of a ‘primi- function of which remains obscure (see Gooday and tive’, basically monothalamous agglutinated test, easily Nott 1982; Hopwood et al. 1997). The protoplasm and its suggests the notion that the xenophyophores are an associated organic sheath are known as the granellare ancient group – perhaps diverging early from more typi- system. Anastomosing, granuloreticulate pseudopodia cal Foraminifera in their internal organization. McIlroy have been observed in one species, Syringammina corbic- et al. (2000) have discussed the fossil record of early ula, suggesting a close relationship with the Foraminifera Foraminifera and concluded that early Cambrian aggluti- (Richardson 2001). The stercomare is contained within nated forms were probably descended from an Ediacaran organic sheets and forms strands and more equidimen- stock of simple, unilocular, naked to loosely agglutinated sional masses. forms (Allogromiida). Molecular evidence (Pawlowski et al. 2003b) has suggested that the Foraminifera most likely evolved from a gromiid-like cercozoan ancestor in THE XENOPHYOPHORE FOSSIL the Neoproterozoic. Some indirect evidence for the exis- RECORD tence of gromiids (testate protozoa related to the Forami- nifera) in the Neoproterozoic comes from the recent The bathyal, abyssal and hadal habitats of living xeno- suggestion of Matz et al. (2008) that bilaterally symmetri- phyophores (Gooday 1996) could be taken to indicate cal tracks in the rocks of this antiquity and greater could 1166 PALAEONTOLOGY, VOLUME 54 be made by gromiid-like protozoa. Pawlowski et al. tively similar structures. As outlined earlier, external (2003b), Bernhard et al. (2006) and Pawlowski and Goo- morphology is unlikely to provide such a framework day (2008) have all emphasized the likely existence and owing to the existence of comparable but unrelated mor- possible ecological importance of primitive Foraminifera photypes. and related protists in Neoproterozoic benthic eco- The conclusion that xenophyophores have no convinc- systems. ing fossil record seems inescapable. Indeed, it is difficult These arguments suggest that xenophyophores could to see how a fossil form could be reliably assigned to the have origins stretching back into the late Neoproterozoic. group. Even if certain Ediacaran fossils were, indeed, xen- There have been two concerted attempts to establish a ophyophores, there remains the puzzle of a 545-Ma fossil history for the xenophyophores. The first was by silence in their history. This silence may be explained in Swinbanks (1982), who reinterpreted the trace fossil Pa- one of two ways. Either their absence from the fossil leodictyon (early Cambrian to Recent) as a tubular, reticu- record is taphonomic (as implied by Zhuravlev 1993; Seil- lated xenophyophore. This argument was based, however, acher et al. 2003). Or their absence is evolutionary, as we on the external morphology of xenophyophores and on explore in the section below. ecological analogy, features that should be regarded as unsatisfactory for taxonomic discrimination in these groups. Levin (1994, p. 38) was also highly critical of XENOPHYOPHORE PHYLOGENY Swinbanks (1982) hypothesis because ‘Paleodictyon like traces reveal no evidence of xenophyae (the agglutinated Brady (1883) described Syringammina fragillissima as a particles) and modern xenophyophores fail to exhibit the foraminiferan, an assignment accepted by some later perfect hexagonal symmetry of Paleodictyon.’ In short, the authors including Loeblich and Tappan (1987). Haeckel trace fossil Paleodictyon shows no defining characters of (1889) regarded Stannophyllum as a species of sponge. the xenophyophores, and it may also display other fea- Following Schulze (1906), however, most authors have tures that are incongruent with that interpretation. Rona placed the xenophyophores within a separate protozoan et al. (2009) described modern Paleodictyon and hypothe- group, varying in rank from class to phylum. Tendal sized a sponge affinity. Molecular evidence from their (1972) compared the characteristics of xenophyophores specimens was inconclusive, so it may have been that the with those of other protistan taxa and concluded that specimens were dead or that it is, indeed, a trace and not they were most similar to the Granuloreticulosea, a group a body fossil. The connection of Paleodictyon with the that included the Foraminifera. There is a particular simi- xenophyophores or any members of the Ediacaran biota larity between many xenophyophores and the foraminif- (Rona et al. 2009 suggest a possible connection with the eran Rhizammina algaeformis, a species that also possesses Edicaran form Palaeophragmodictya) seem speculative at the characteristics of a komokiacean foraminiferan (Goo- best, being based on very loose morphological analogies. day and Cartwright, 1987). The discoidal growth rings of Further, the relationship of these modern Paleodictyon some xenophyophores (e.g. Text-fig. 7C) are also reminis- specimens with all fossil structures presently ascribed to cent of growth in some larger benthic Foraminifera, such this genus is currently very uncertain. as Peneroplis and Archaias (Gooday et al. 1993). The second suggestion was that certain Carboniferous Using molecular data, Pawlowski et al. (2003a) demon- ‘phylloid algae’ are the remains of xenophyophores (May- strated that the psamminid xenophyophore Syringammina bury and Evans 1994, 1996). This was based on supposed fragillissima is, indeed, a foraminiferan. Subsequently, morphological similarities in cross-section and the pres- Pawlowski et al. (2003b) presented a phylogeny of Fora- ence of the element barium (but not BaSO4. as in living minifera that placed S. corbicula within the radiation of xenophyophores) in the fossil alga material. Torres ‘primitive’ monothalamous Foraminifera, within a clade (1996), however, criticized the interpretations of Maybury that included the agglutinated taxa Hippocrepinella alba and Evans (1994, 1996) because the calcite fabric of the and Rhizammina spp. (see also Lecroq et al. 2009; ‘phylloid algae’ is more of a kind characteristic of algae Gooday et al. 2011). These molecular analyses, when cou- and because the elemental barium was shown to have pled with the lack of a demonstrable fossil record, leads substituted into the calcite lattice later, during diagenesis. us towards the hypothesis that xenophyophores are a The chemical analyses of Maybury and Evans (1994, group of derived monothalalmous agglutinated Forami- 1996) omitted to measure the surrounding matrix, mean- nifera that originated in the geologically recent past. ing that they had not provided satisfactory contextual Although it seems likely that all psamminids are true analysis for the biogeochemical claims for xenophyo- Foraminifera, there are, currently, no molecular data for phores in the Carboniferous. A large part of the problem stannomid xenophyophores such as Stannopyllum, in here is that no satisfactory framework exists for discrimi- which the test is soft and traversed by proteinaceous nating between fossil xenophyophores and other puta- fibres. The presence of the unique granellare and sterco- ANTCLIFFE ET AL.: EDIACARAN FOSSILS: DEVELOPMENT OF PALAEOPASCICHNUS 1167 mare systems could provide unifying synapomorphies (as rather high level of tissue compatibility and ⁄ or a low level postulated by Levine et al. 1980) that are derived states of individuality, perhaps of the kind encountered in some from similar features in the Komokiacea. However, it is protozoans and some sponges. Further to this, none of possible that these features reflect convergence and that at the body chambers in Palaeopascichnus show signs of per- least two groups of Foraminifera have recently undergone forations or other connections (such as tubes). The only ‘xenophyophorization.’ If that were so, the xenophyo- way in which fluid could be exchanged around the body phores would be a polyphyletic group that evolved by at would be osmotic diffusion through the agglutinated walls least two iterations from more ‘conventional’ monothala- of the chambers (as in many simple Foraminifera) or fil- mous agglutinated foraminiferans. Further molecular tration through tiny pores (perhaps like the endolithic sequencing is necessary to distinguish between these two sponge Cliona). Therefore, we find no evidence for such scenarios. pores as yet. Provisionally, this seems to preclude a Some xenophyophores exhibit superficial similarities to sponge affinity. larger calcareous Foraminifera such as Nummulites and Alveolina, particularly large test size and a flattened, discoidal test morphology (Tendal 1972). Moreover, a simi- The development of Foraminifera lar tendency towards compartmentalization of the test is observed in a few species, notably Psammina zonaria We turn now to the possibility that Palaeopaschichnus (Tendal, 1994). However, in contrast to these calcareous was a protozoan and more specifically a ‘nonxenophyoph- taxa, these adaptations are not associated with photosym- orean’ foraminiferan. Here, the difficulties are merely sug- biosis because they are a deep-sea group. Interestingly, gestive rather than compelling. The presence of large neither the deep-sea milioline Discospirina (Miocene to chambers that are wider than they are long is a distinctive Recent), nor the deep-sea textulariine Cyclammina feature for larger calcareous benthic Foraminifera (Bou- (Eocene to Recent) shows any hint of photosymbiotic Dagher-Fadel 2008). But the evolution of this feature is adaptations of the test wall (Brasier 1984a, b), despite remarkably well documented in Foraminifera because morphologies consistent with this life mode. It is possible such forms have very high biostratigraphic utility. There- that the morphologies are also advantageous for coping fore, this shape of chamber is a highly derived one and with a large mass of multinucleate cytoplasm that must not met in any studied foraminiferan group until the be efficiently moved around the cell or that some other middle Devonian (see Brasier 1982a, b). By contrast, form of endosymbiosis is involved. primitive Foraminifera tend to be either monothalamous or have tubular tests that are longer than wide. So pro- nounced is this pattern that it has been used as a tool for WHAT WAS PALAEOPASCICHNUS?THE decoding the early evolution of the group (Brasier 1984a, COMPARATIVE DEVELOPMENT OF b; Loeblich and Tappan 1987). The earliest attributed POSSIBLE AFFILIATES Foraminifera such as the large agglutinated foraminiferan Platysolenites antiquissimus, which comes from the basal When the above points are considered, it seems unlikely Cambrian layers of Avalonia and Baltica, clearly exempli- that Palaeopascichnus could have been a xenophyophore. fies this pattern. It has a long tubular chamber without Other possible biological affinities remain, which can be septal partitions (McIlroy et al. 2000). seen from our studies of the growth and development of Further objections can be raised concerning the possi- Palaeopascichnus. These features, and their associated ble foraminiferan affinities of Palaeopaschichnus. The inferences, are summarized in Tables 1 and 2. chambers of the latter do not show any visible perfora- Two kinds of affinity seem to us extremely unlikely – tions or foramina of the kind usually seen in Foraminif- prokaryote and metazoan. A prokaryotic affinity can be era. Clearly, there must have been some means for the discounted because the chambers show regularity in cytoplasm of Palaeopaschichnus to spread beyond the length that is unparalleled in stromatolitic communities. chamber wall; otherwise, the organism would have been The laminae formed within stromatolites are largely phys- unable to grow. We cannot preclude the possibility that ically (not biologically) controlled by factors such as sedi- cytoplasmic streaming took place between sediment parti- ment input, and light levels, which are highly variable cles within the chamber walls. But the absence of diagnos- and not highly regular. Thus, a bacterial colony is not tic foramina means that it becomes hard to place this known to have the ability to generate the kinds of con- fossil within the Foraminifera. trolled morphology across the range of environments in To summarize, the difficulties in placing Palaeopascich- which this fossil is found. A metazoan affinity is also dee- nus within the Foraminifera are as follows. First, it never ply unlikely. The phenomenon of merging seen between shows a proloculus. This is a nepionic (juvenile) stage coeval and adjacent specimens suggests the presence of a that is preserved within almost all foraminiferan tests. 1168 AAOTLG,VLM 54 VOLUME PALAEONTOLOGY,

TABLE 1. Summary of key developmental features observed in the specimens of Palaeopascichnus. ANTCLIFFE TAL. ET DAAA OSL:DVLPETO PALAEOPASCICHNUS OF DEVELOPMENT FOSSILS: EDIACARAN :

The numbers of features shown in the left column correspond to the numbers for Text-ﬁgures 2–4. Green highlight indicates that this feature provides a potential for constraint on phylogenetic afﬁnity; amber indicates that this feature is merely suggestive of constraint; red does not help to constrain phylogeny. 1169 1170 PALAEONTOLOGY, VOLUME 54

TABLE 2. Summary of key developmental features in Palaeopascichnus and how they are used to constrain phylogenetic hypotheses relating to it.

Character numbers correspond to those given in Text-ﬁgures 2–4, and Table 1.

Second, the ‘chambers’ show no evidence of being inter- The sections in Avalonia are argued to be substantially connected by pores or foramina, as is usual in the poly- below the photic zone, based on a legion of sedimento- thalamous Foraminifera (in some simple living forms, the logical and stratigraphic evidence (Wood et al. 2003), and cytoplasm may exchange between agglutinated grains; Palaeopasichnus is well represented at numerous localities. though, there is no evidence that Palaeopascichnus was It should be noted that the Palaeopascichnus material agglutinated). Third, no foraminiferan is known to have described by Haines (2000) is from the Wonoka Forma- chambers that are wider than are long until the tion from South Australia that in part is a deeper water mid-Devonian (Brasier 1982a, b, 1984a, b). Finally, mul- formation than the classic Ediacaran biota Rawnsley tilocular Foraminifera did not evolve until much later; Quartzite as it represents ‘a shallowing upward sequence Pawlowski et al. (2003b) suggested an origin of around from deep shelf... to shallow water cycles at the top’ 350 Ma ago for the multilocular Foraminifera. (Haines 2000, p. 99). Although taken alone, stratigraphic data could not preclude a photoautotrophic habit for the Australian specimens, yet taken in concert with known Other possible candidates Palaeopascichnus material from deep water Avalonia, this life strategy seems unlikely. Comparisons between Palaeopaschichnus and the modern The fact that bifurcation of Palaeopascichnus could take phaeophyte alga Padina (Haines 2000) seem to us superfi- place, especially when the chamber approached a certain cial because there we find no evidence for the overlapping critical threshold of mass or width, seems to us to imply of thalli, of carbonaceous compressions, nor of structures some degree of determinism in the growth programme. for attachment that such an affinity would predict. Addi- The even more remarkable phenomenon of converging tionally, there is no evidence for in situ enlargement of chambers seems equally telling. It might be taken to the kind that is typically seen during the growth of living imply that these coeval forms were either compatible, and algae such as Padina and Halimeda. Nor do either of the hence of the same genetic strain, or that they were geneti- latter show evidence for the merging of adjacent and coe- cally different and indulging in sexual conjugation, like val individuals, of the kind seen in Palaeopaschichnus. fungi. We observed such accidental merging of the cyto- Further to this, the primary growth vector of Padina and plasm as examples of the former case, within the larger allies is vertical, i.e. perpendicular to the sea floor, while benthic foraminiferan Archaias, although it is rare. Con- all taphonomic evidence shows that Palaeopascichnus grew versely, the lack of merging between early Cambrian along the sediment surface with no appreciable vertical archaeocyathan cups has been used to argue for a level vector. Finally, there is no evidence that this organism organization at least of sponge grade (Brasier 1976). Even was restricted to photic zone conditions, as would be so, such ‘allorecognition’ phenomenon shows no consis- expected for an alga. tent relationship with level of complexity of an organism ANTCLIFFE ET AL.: EDIACARAN FOSSILS: DEVELOPMENT OF PALAEOPASCICHNUS 1171 and is a feature which needs to be used with great whole range of the animal kingdom. Even the lowermost caution. animals, the sponges, interact competitively or even It is also interesting that when chambers in adjacent aggressively. It seems likely that this feature can be taken specimens merge, they are always of comparable dimen- as evidence for a grade of organization that ranges from sions. There are no instances where small and large forms fungoids, such as myxomycophytes (slime moulds) and have been observed to merge – the large form always mycophycophytes (lichens), to ascomycotids (yeasts and takes precedence over the small form, presumably to the their multicellular relatives). Each of these possibilities detriment or even fatality of the smaller form. Such com- has both merits and weaknesses that warrant further petitive interactions are well documented from across the investigation and require further material for analysis,

TEXT-FIG. 8. The larger benthic milioline foraminiferan Discospirina. A, a complete test of D. tenuissima viewed through a transmitted light microscope. The complex growth programme passes through at least three distinct modes of growth (Brasier 1984a, b). Field of view is 4 mm across. B, this specimen shows the regeneration capabilities of this taxon, comparable with that in many other larger benthic Foraminifera. A complete Discospirina specimen has repaired itself and regained its growth programme from a small fragment of an outer chamber. Instead of trying to build a whole test again from the start, regeneration proceeds from the last stage reached. In this case, the fragment builds annular chambers. Field of view is 3 mm across.

B 1172 PALAEONTOLOGY, VOLUME 54 and no affinity can be utterly accepted or refuted on the the biological affinities of Ediacaran rangeomorphs or, evidence so far gathered. It seems likely that Palaeopasc- indeed, of most other larger Ediacaran body fossils. ichnus was a eukaryotic colony ⁄ organism, which was Indeed, they seem to be constructed so differently and interacting with the widespread bacterial biofilms at this develop in such distinct ways that we should be confident time. There is the possibility of a major role for osmo- about affirming their biological distinction. trophic organisms in the Ediacaran oceans (e.g. Brasier et al. 2010). Such a feeding mode could be suggested for the ecology of Palaeopascichnus as it spread across bio- PERSPECTIVE films on the seafloor, from which it could perhaps have imbibed food and nutrients. The biological affinities of the majority of Ediacaran fossils are probably now more open than at any time since their discovery in 1946. Happily, the wealth of modern The comparative development of Palaeopascichnus and the analytical techniques and sixty years of progress within Ediacara biota palaeontology and biology may yet come to the aid of this long posed problem. As this study of Palaeopascich- Our rejection of foraminiferan affinities for Palaeopaschic- nus shows, the analysis of the development and growth of nus should not be taken to imply our rejection of all pro- a fossil is a promising tool that can reveal much about tozoan affinities for this or members of the Ediacara likely biological relations, rejecting some affinities and biota. The problem here is that many features of proto- narrowing the likelihoods of others. Although different zoan grade organisms are not particularly useful as dis- authors will argue about the interpretations of such analy- criminators, owing to their low level of organization. For ses, the observations made herein are intended to be of the demonstration of protozoan affinities in the (contro- the kind that are central to the identification of homolo- versial) case of the Ediacara biota, we would expect to see gies in enigmatic fossil groups. Ultimately, this should evidence for a protozoan-like growth and regeneration provide a firmer basis for classification. programme, such as that illustrated by the modern large The study of Palaeopascichnus remains critical to milioline Discospirina (see Text-fig. 8), and for Cambrian understanding the biology of the Ediacaran Period. This Platysolenites (McIlroy et al. 2000). While several exam- is because the form is very widespread and it gives us an ples of Dickinsonia from the Ediacara biota have been opportunity to assess the effect of the widely different illustrated (e.g. Dzik 2003; Fedonkin 2003; Brasier and taphonomic regimes found in different environmental set- Antcliffe 2008) as showing damage and subsequent repair tings. It is therefore likely to play an increasingly impor- during life, there is no evidence as yet that this taxon tant role in the understanding of the Ediacara Biota could behave in the manner of living foraminiferan Disco- globally, even though it is likely not biologically affiliated spirina. This lack of evidence leads us to suspect that a with the rangeomorphs. giant single-celled hypothesis for most Ediacaran macro- fossils is probably inappropriate. Acknowledgements. Thanks to Professors Jim Gehling, Guy Nar- Of critical importance to this debate is our finding of bonne and Duncan McIlroy for help with access to materials of substantial difference in the developmental programmes Palaeopascichnus from Australia, Newfoundland and northern between the Ediacara biota (Brasier and Antcliffe 2008, Norway, respectively. Thanks also to Professors Jan Pawlowski, 2009) and that seen in Palaeopascichnus as studied herein. Lynn Margulis and Tom Cavalier-Smith for constructive discussion on theoretical aspects of the work. Prof. Søren Jensen as well The growth scheme seen in the Avalonian rangeomorphs as two anonymous reviewers provided vital critical feedback on (e.g. Charnia, Bradgatia, Charniodiscus, Fractofusus and the manuscript for which they have our thanks. AJG’s research Beothukis) is one where smaller new chambers are added on xenophyophores received funding from the European Com- by terminal (apical) addition, while previous chambers munity’s 6th Framework Programme (FP6 ⁄ 2002-2006) under the inflate and move along like a conveyor belt towards the HERMES project, contract number GOCE-CT-2005-511234, and base of the organism (Antcliffe and Brasier 2007a, 2008; the 7th Framework Programme (FP7 ⁄ 2007-2013) under the Brasier and Antcliffe 2009.) The growth programme for HERMIONE project, grant agreement no 226354. Palaeopascichnus is here shown to be one in which larger Editor. Svend Stouge new chambers are added by terminal addition, while previous chambers remain unaltered and are potentially left unoccupied after growth. Furthermore, we regard the SUPPORTING INFORMATION phenomena of bifurcation and mergence in Palaeopascich- nus as entirely unmatched in any other Ediacaran form of Additional Supporting Information may be found in the online which we are aware. Thus, regardless of the biological version of this article: affinity of Palaeopascichnus, it arguably tells us little about ANTCLIFFE ET AL.: EDIACARAN FOSSILS: DEVELOPMENT OF PALAEOPASCICHNUS 1173

Appendix S1. Measurements taken from the Palaeopascichnus —— and ANTCLIFFE, J. B. 2004. Decoding the Ediacara material held in the typotech facility of the South Australia enigma. Science, 305, 1115–1117. Museum, Adelaide. —— —— 2008. Dickinsonia from Ediacara: a new look at mor- Please note: Wiley-Blackwell are not responsible for the con- phology and body construction. Palaeogeography, Palaeoclima- tent or functionality of any supporting materials supplied by the tography, Palaeoecology, 270, 311–323. authors. Any queries (other than missing material) should be —— —— 2009. Evolutionary relationships within the Avalonian directed to the corresponding author for the article. Ediacara biota: new insights from laser analysis. Journal of the Geological Society of London, 166, 363–384. —— —— and CALLOW, R. 2011. Taphonomy in the Ediaca- REFERENCES ran interval. In ALLISON, P. A. and BOTTJER, D. J. (eds). Taphonomy: bias and process through time. Springer, ANTCLIFFE, J. B. and BRASIER, M. D. 2007a. Charnia and Heidelberg, 599 pp. Sea Pens are poles apart. Journal of the Geological Society of —— CALLOW, R., MENON, L. R. and LIU, A. G. 2010. London, 164, 49–51. Osmotrophic biofilms: from modern to ancient. In SECK- ————2007b. Towards a morphospace model for the Ediacara BACH, J. and OREN, A. (eds). Microbial mats: modern and biota. In VICKERS-RICH, P. and KOMAROWER, P. ancient in Microorganisms in Stratified Systems, Cellular Ori- (eds). The rise and fall of the Ediacaran Biota. Geological Soci- gin, Life in Extreme Habitats and Astrobiology, 14, 131–148. ety London, Special Publication, 286, 377–386. BUSS, L. W. and SEILACHER, A. 1994. The phylum Vend- —— —— 2008. Charnia at 50: developmental analysis of Ediaca- obionta: a sister group to the Eumetazoa. Palaeobiology, 20, 1–4. ran fronds. Palaeontology, 51, 11–26. CRIMES, P. T. and M C ILROY, D. 1999. A biota of Ediacaran ARMSTRONG, H. A. and BRASIER, M. D. 2004. Micro- aspect from lower Cambrian strata on the Digermul Peninsula, fossils, Second edition. Blackwell Science Ltd., Oxford, 304 pp. Arctic Norway. Geological Magazine, 136, 633–642. BENGTSON, S. 2003. Tracing metazoan roots in the fossil DALRYMPLE, R. W. and NARBONNE, G. M. 1996. Conti- record. 289–300. In LEGAKIS, A., SFENTHOURAKIS, nental slope sedimentation in the Sheepbed Formation S., POLYMENI, R. and THESSALOU-LEAKI, M. (eds). (Neoproterozoic; Windermere Supergroup), Mackenzie Moun- The new panorama of animal evolution: proceedings of the tains, N.W.T. Canadian Journal of Earth Sciences, 33, 848–862. XVIII International congress of zoology. Pensoft Publishers, DARWIN, C. 1859. The origin of species by means of natural Sofia, 724 pp. selection or the preservation of favoured races in the struggle for BERNHARD, J. M., HABURA, A. and BOWSER, S. S. life. John Murray, London, 512 pp. 2006. An endobiont-bearing allogromiid from the Santa De BEER, G. 1971. Homology: an unsolved problem. Oxford Barbara Basin: implications for the early diversification of Biology Reader, 11, 16. Foraminifera. Journal of Geophysical Research, 111, G03002, DONG, L., XIAO, S., SHEN, S. and ZHOU, C. 2008. Silici- doi:10.1029/2005JG000158. fied Horodyskia and Palaeopascichnus from Upper Ediacaran BOUDAGHER-FADEL, M. K. 2008. Evolution and geological cherts in South China: tentative phylogenetic interpretation significance of larger benthic Foraminifera. Developments in and implications for evolutionary stasis. Journal of the Geologi- palaeontology and stratigraphy, volume 21. Elsevier, Amster- cal Society, 165, 367–378. dam, 544 pp. DZIK, J. 2003. Anatomical information content in the Ediaca- BRADY, H. B. 1883. Note on Syringammina, a new type of are- ran fossils and their possible zoological affinities. Integrative naceous Rhizopoda. Proceedings of the Royal Society of London, and Comparative Biology, 43, 114–126. 35, 155–161. FEDONKIN, M. A. 1978. The behavioural evolution of BRASIER, M. D. 1976. Early Cambrian intergrowths of mudeaters [title translated from Russian]. Paleontologicheskii Archaeocyathids, Renalcis, and pseudostromatolites from Zhurnal, 2, 106–112. South Australia. Palaeontology, 19, 223–245. ——2003. The origin of the Metazoa in the light of the Protero- ——1979. The Cambrian radiation event. 103–159. In HOUSE, zoic fossil record. Palaeontological Research, 7, 9–41. M. R. (ed.). Origin of major invertebrate groups. Systematics Asso- —— and WAGGONER, B. M. 1997. The late Precambrian ciation special volume 12, Academic Press, New York, 525 pp. fossil Kimberella is a mollusc like bilaterian organism. Nature, —— 1982a. Architecture and evolution of the foraminiferid test 388, 868–871. – a theoretical approach. 1–41. In BANNER, F. T. and FORD, T. E. 1958. Precambrian fossils from Charnwood LORD, A. R. (eds). Aspects of Micropalaeontology. George, Forest. Proceedings of the Yorkshire Geological Society, 31, Allen and Unwin, Oxford, 362 pp. 211–217. —— 1982b. Foraminiferid architectural history; a review using GEHLING, J. G. 1987. Earliest known echinoderm – a new the MinLOC and PI methods. Journal of Micropalaeontology, Ediacaran fossil from the Pound Subgroup of South Australia. 1, 95–105. Alcheringa, 11, 337–345. —— 1984a. Discospirina and the pattern of evolution in forami- —— 1991. The case for the Ediacaran fossil roots to the Meta- niferid architecture. Second International Symposium on Ben- zoan Tree. Geological Society of India Memoir, 20, 181–224. thic Foraminifera, Pau, April 1983. Elf Aquitaine, 87–90. —— NARBONNE, G. M. and ANDERSON, M. M. 2000. —— 1984b. Microfossils and small shelly fossils from the Lower The first named Ediacaran body fossil, Aspidella terranovica. Cambrian Hyolithes Limestone at Nuneaton, English Mid- Palaeontology, 43, 427–456. lands. Geological Magazine, 121, 229–253. 1174 PALAEONTOLOGY, VOLUME 54

GLAESSNER, M. F. 1966. Precambrian Palaeontology. Earth ——1992. Functional and ecological aspects of Ediacaran assem- Science Reviews, 1, 29–50. blages. 131–176. In LIPPS, J. H. and SIGNOR, P. W. (eds). —— 1984. The dawn of animal life: a biohistorical study. Cam- Origins and early evolution of the Metazoa. Plenum Press, New bridge University Press, Cambridge, 256 pp. York, NY. —— and DAILY, B. 1959. The geology and late Precambrian ——1995. The problems and potential of using animal and trace fauna of the Ediacara fossil reserve. Records of the South fossils in terminal Proterozoic biostratigraphy. Precambrian Australian Museum, 13, 369–410. Research, 73, 51–69. —— and WADE, M. 1966. The late Precambrian fossils from —— and GEHLING, J. G. R. 1978. A review of the frond like Ediacara, South Australia. Palaeontology, 9, 599–628. fossils of the Ediacara assemblage. Records South Australia GOODAY, A. J. 1996. Xenophyophorea (Protista), including Museum, 17, 347–359. two new species, from two abyssal sites in the North Atlantic JENSEN, S. 2003. The Proterozoic and early Cambrian trace Ocean. Journal of Foraminiferal Research, 26, 193–208. fossil record; patterns, problems and perspectives. Integrative —— and CARTWRIGHT, N. 1987. Rhizammina algae- and Comparative Biology, 43, 219–228. formis: a giant komokiacean foraminifer? Deep Sea Newsletter, KAMENSKAYA, O. E. 2005. Spiculammina delicata gen. et sp. 13, 13–15. n., a new xenophyophore from the eastern Pacific (Psammini- —— and NOTT, J. A. 1982. Intracellular barite crystals in two dae). Invertebrate Zoology, 2, 23–27. Xenophyophores, Aschemonella ramuliformis and Galatheam- KNOLL, A. H., WALTER, M. R., NARBONNE, G. M. and mina sp. (Protozoa: Rhizopoda) with comments on the taxon- CHRISTIS-BLICK, N. 2004. A new period for the geologic omy of A. ramuliformis. Journal of the Marine Biology time scale. Science, 305, 621–622. Association, 62, 595–605. LECROQ, B., GOODAY, A. J., TSUCHIYA, M. and —— and TENDAL, O. S. 2003. Class Xenophyophorea. 1086– PAWLOWSKI, J. 2009. A new genus of xenophyophores 1097. In LEE, J. J., LEEDALE, G. F. and BRADBURY, P. (Foraminifera) from Japan Trench: morphological description, (eds). An illustrated guide to the Protozoa: organism tradition- molecular phylogeny and elemental analysis. Zoological Journal ally referred to Protozoa, or newly discovered groups, Second of the Linnean Society, 156, 455–464. edition, Lawrence, Kansas, 689 pp. LEMCHE, H., HANSEN, B., MADSEN, F. J., TENDAL, ——ARANDA DA SILVA, A. and PAWLOWSKI, J. 2011. O. S. and WOLFF, T. 1976. Hadal life as analysed from pho- Xenophyophores (Rhizaria, Foraminifera) from the Nazare´ tographs. Videnskabelige Meddelelser Fra Dansk Naturhistorisk Canyon (Portuguese margin, NE Atlantic). Deep-sea Research Forening, 139, 263–336. II, doi:10.1016/j.dsr2.2011.04.005. LEVINE, N. D., CORLISS, J. O., COX, F. E. G., DEROUX, —— BETT, B. J. and PRATT, D. N. 1993. Direct observation G., GRAIN, J., HONINBERG, B. M., LEEDALE, G. F., of episodic growth in an abyssal Xenophyophore (Protista). LOEBLICH, R. H., LOM, J., LYNN, D., MERINFELD, Deep-Sea Research I, 40, 2131–2143. E. G., PAGE, F. C., POLJANSKY, G., SPRAGUE, V., VA- GU¨ RICH, G. 1933. Schragschichtungsbogen und zapfenformige VRA, J. and WALLACE, F. C. 1980. A newly revised classifi- Flieswulste im flagstone van Pretoria und ahnliche Vor- cation of the Protozoa. Journal of Protozoology, 27, 37–58. komnisse in Quartzit von Kuibis, Sudwest-Afrika, dem Schleif- LEVIN, L. A. 1994. Paleoecology and ecology of Xenophyo- sandstein von Maulbronn. Zeitschrift der Deutsche geologischen phores. Palaios, 9, 32–41. Gesellschaft, 85, 652–654. —— and GOODAY, A. J., 1992. Possible roles for xenophyo- HAECKEL, E. 1889. Report on the deep-sea Keratosa. Reports phores in deep-sea carbon cycling. 93–104. In ROWE, G. T. of the Challenger, 32, 1–92. and PARIENTE, V. (eds): Deep-sea food chains and the glo- HAINES, P. W. 1987. Carbonate shelf and basin sedimenta- bal carbon cycle. Kluwer Academic Publishers, The Nether- tion, late Proterozoic Wonoka Formation, South Australia. lands, 412 pp. Unpublished PhD Thesis, University of Adelaide, Adelaide, LOEBLICH, A. R. Jr and TAPPAN, H. 1987. Foraminiferal South Australia, 152 pp. genera and their classification. Van Nostrand Reinhold Com- —— 1990. A late Proterozoic storm-dominated carbonate shelf pany, New York, 980 pp. sequence: the Wonoka Formation in central and southern MATZ, M. V., FRANK, T. M., MARSHALL, N. J., WID- Flinders Ranges, South Australia. Special Publication of the DER, E. A. and JOHNSEN, S. 2008. Giant deep-sea protist Geological Society of South Australia, 16, 177–198. produces bilaterian-like traces. Current Biology, 18, 1849–1854. —— 2000. Problematic fossils in the late Neoproterozoic MAYBURY, C. A. and EVANS, K. R. 1994. Pennsylvanian Wonoka Formation, South Australia. Precambrian Research, phylloid algae interpreted as shallow water xenophyophores. 100, 97–108. Lethaia, 27, 29–33. HOPWOOD, J. D., MANN, S. and GOODAY, A. J. 1997. —— —— 1996. Pennsylvanian phylloid algae interpreted as shal- The crystallography and possible origin of barium sulphate in low water xenophyophores; reply. Lethaia, 29, 299–300. deep sea Rhizopod protists (Xenophyophorea). Journal of McILROY, D., GREEN, O. R. and BRASIER, M. D. 2000. Marine Biology Association, 77, 969–987. Palaeobiology and evolution of the earliest agglutinated Fora- JENKINS, R. J. F. 1984. Interpreting the oldest fossil cnidari- minifera: Platysolenites, Spirosolenites and related forms. ans. Palaeontology American, 54, 95–104. Lethaia, 34, 13–29. —— 1985. The enigmatic Ediacaran (late Precambrian) genus McMENAMIN, M. A. S. 1986. The Garden of Ediacara. Palai- Rangea and related forms. Palaeobiology, 11, 336–359. os, 1, 178–182. ANTCLIFFE ET AL.: EDIACARAN FOSSILS: DEVELOPMENT OF PALAEOPASCICHNUS 1175

—— 1998. The Garden of Ediacara. Cambridge University Press, SEILACHER, A. 1984. Late Precambrian and Early Cambrian Cambridge, 368 pp. Metazoa: preservational or real extinctions? 159–168. In NARBONNE, G. 1998. The Ediacaran biota: a terminal Neopro- HOLLAND, H. D. and TRENDAL, A. F. (eds). Patterns of terozoic experiment in the evolution of life. GSA Today, 8, 1–6. change in Earth evolution. Springer Verlag, Berlin, 450 pp. —— 2005. The Ediacara Biota: Neoproterozoic origin of animals —— 1985. Discussion of Precambrian Metazoa. Philosophical and their ecosystems. Annual Review of Earth and Planetary Transactions of the Royal Society London B, 311, 47–48. Sciences, 33, 421–442. —— 1989. Vendozoa biosphere: organismic construction in the PALIJ, V. M. 1976. Ostatki besskeltnoj fauny i sledy zhiznedey- Proterozoic biosphere. Lethaia, 22, 229–239. atelnosti iz otlozhenij verkhnego dokembriya i nizhnego —— 1992. Vendobionta and Psammocorallia: lost constructions Kembriya Podolii. In Paleontologiya i stratigrafiya verkhnego of Precambrian evolution. Journal of the Geological Society of dokembriya i nizhnego paleozoya jugo-zapdna vostochno-evropej- London, 149, 607–613. skoj platformy, 63–77. Naukova Dumka, Kiev. —— 2003. Vendobionts (Precambrian evolution). McGraw Hill —— POSTI, E. and FENDONKIN, M. A. 1979. Soft-bodied Yearbook 2003, 458–461. Metazoa and trace fossils in Vendian and Lower Cambrian. —— GRAZHDANKIN, D. and LEGOUTA, A. 2003. Ediac- 49–82. In KELLER, B. M. and ROZANOV, Y. YU. (eds). aran biota: the dawn of animal life in the shadow of giant Paleontologiya Verkhenedokembrijskikh i Kembrijkikh Otlozhenij protists. Paleontological Research, 7, 43–54. Vostochno-Evropejskoj Platformy. Nauka, Moscow [title trans- SPRIGG, R. C. 1947. Early Cambrian (?) jellyfishes from the lated from Russian]. Flinders Ranges, South Australia. Transactions of the Royal PATTERSON, C. 1982. Morphological characters and homol- Society of South Australia, 71, 212–224. ogy. 21–74. In JOYSEY, K. A. and FRIDAY, A. E. (eds). SWINBANKS, D. D. 1982. Paleodictyon: traces of infaunal Problems of phylogenetic reconstruction. Academic Press, Xenophyophores? Science, 218, 47–49. London and New York, 442 pp. TENDAL, O. S. 1972. A monograph of the Xenophyophora. PAWLOWSKI, J. and GOODAY, A. J. 2008. Precambrian Galathea Report, 12, 7–103. biota: protistan origin of trace fossils? Current Biology, 19, 28–30. —— 1994. Protozoa Xenophyophorea Granuloreticulosa: Psam- —— HOLZMANN, M., FAHRNI, J. and RICHARDSON, mina zonaria sp. nov. from the West Pacific and some aspects of S. L. 2003a. Small subunit ribosomal DNA suggests that the the growth of xenophyophores. In CROSNIER, A. (ed.). Xenophyophorean Syringammina corbicula is a foraminiferan. Re´sultats des Campagnes MUSORSTOM, volume 12, Me´moires Journal of Eukaryotic Microbiology, 50, 483–487. du Museúm national d’Histoire naturelle, 161, 49–54. —— —— BERNEY, C., FAHRNI, J., GOODAY, A. J., —— 1996. Synoptic checklist and bibliography of the Xenophyo- CEDHAGEN, T., HABURA, A. and BOWSER, S. S. phorea (Protista), with a zoogeographical survey of the group. 2003b. The evolution of early Foraminifera. Proceedings of the Galathea Report, 17, 79–101. National Academy of Science, 100, 11494–11498. TORRES, A. M. 1996. Fossil algae were very different from PETERSON, K. J., WAGGONER, B. and HAGADORN, J. xenophyophores. Lethaia, 29, 287–288. W. 2003. A fungal analog for Newfoundland Ediacaran VALENTINE, J. W. 1992. Dickinsonia as a polyploidy organ- Fronds. Integrative Comparative Biology, 43, 127–136. ism. Paleobiology, 18, 378–382. RICHARDSON, S. L. 2001. Syringammina corbicula sp. nov. WADE, M. 1972. Hydrozoa and Scyphozoa and other medu- (Xenophyophorea) from the Cape Verde Plateau, E. Atlantic. soids from the Precambrian Ediacara fauna, South Australia. Journal of Foraminiferal Research, 31, 201–209. Palaeontology, 15, 197–225. RONA, P. A., SEILACHER, A., VARGAS, C., GOODAY, WOOD, D. A., DALRYMPLE, R. W., NARBONNE, G. M., A. J., BERNHARD, J. M., BOWSER, S., VETRIANI, C., GEHLING, J. G. and CLAPHAM, M. E. 2003. Paleoenvi- WIRSEN, C. O., MULLINEAUX, L., SHERRELL, R., ronmental analysis of the late Neoproterozoic Mistaken Point GRASSLE, J. F., LOWH, S. and LUTZ, R. A. 2009. Paleo- and Trepassey formations, southeastern Newfoundland. Cana- dictyon nodosum: a living fossil on the deep-sea floor. Deep dian Journal of Earth Sciences, 40, 1375–1391. Sea Research II, 56, 1700–1712. ZHURAVLEV, A. Yu. 1993. Were the Ediacaran Vendobionta SCHULZE, F. E. 1906. Die Xenophyophoren der ‘‘Siboga’’ multicellulars? Neus Jahrbuch fur Geologie und Palaontologie expedition. Siboga-expedition. Monographie, IV, 1–18. Abhandlungen, 190, 299–314.