Carnets de Géologie [Notebooks on Geology]: Article 2012/03 (CG2012_A03)

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Contents

[1. Introduction] [2. Results and Discussion]
[3. Conclusions] [Bibliographic references]


Inconsistencies in proposed annelid affinities
of early biomineralized organism Cloudina (Ediacaran):
structural and ontogenetic evidences

Olev Vinn

Department of Geology, University of Tartu, Ravila 14A, EE-50411 Tartu (Estonia)

Michał Zatoń

Faculty of Earth Sciences, University of Silesia, Będzińska 60, PL-41-200 Sosnowiec (Poland)

Manuscript online since March 12, 2012
[Editor: Christian Emig]

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Abstract

Cloudina, an important Ediacaran index fossil, is considered as one of the earliest biomineralizing organisms. Its biological affinities have not been fully resolved and phylogenetic links with both annelids and cnidarians have traditionally been suggested. Differences in tube morphology, ultrastructure and biomineralization suggest that Cloudina is not closely related to any recent skeletal annelid (e.g., serpulids, sabellids and cirratulids) and their skeletons are not homologous. The way of asexual reproduction in Cloudina resembles more that of cnidarians. The presence of a closed tube origin (base) in Cloudina is also compatible with the hypothesis of an animal of cnidarian grade.

Key Words

Cloudina; Annelida; Serpulidae; Cnidaria; Ediacaran; biomineralization.

Citation

Vinn O. & Zatoń M. (2012).- Inconsistencies in proposed annelid affinities of early biomineralized organism Cloudina (Ediacaran): structural and ontogenetic evidences.- Carnets de Géologie [Notebooks on Geology], Brest, Article 2012/03 (CG2012_A03), p. 39-47.

Résumé

Incohérences dans les affinités supposées de l'organisme primitif biominéralisé Cloudina (Ediacaran) avec les annélides : preuves relevant de la structure et du développement ontogénétique.- Cloudina, un important fossile édiacarien, est considéré comme l'un des premiers organismes biomineralisés. Ses affinités biologiques n'ont pas encore été entièrement élucidées : des relations phylogénétiques avec les annélides et les cnidaires sont habituellement envisagées. Des différences dans la morphologie, l'ultrastructure et la biominéralisation du tube suggèrent que Cloudina ne puisse Ítre étroitement apparentée à aucun squelette d'annélides actuelles, qu'il s'agisse de serpulidés, de sabellidés ou de cirratulidés ; leurs squelettes ne sont pas homologues. Le mode de reproduction asexuée de Cloudina ressemble davantage à celui des cnidaires. De plus, la configuration fermée de la partie initiale (proximale) du tube chez Cloudina est compatible avec l'hypothèse d'un animal de la catégorie des cnidaires.

Mots-Clefs

Cloudina ; Annelida ; Serpulidae ; Cnidaria ; Édiacarien ; biominéralisation.


1. Introduction

Cloudina is a tube-building metazoan organism of problematic affinities that widely occurs in deposits of the terminal Neoproterozoic Ediacaran Period (Grant, 1990), between 549 ± 1 Ma and 542 ± 1 Ma (Grotzinger et al., 1995; Amthor et al., 2003). Two distinct species are recognized, C. hartmannae Germs, 1972, and C. carinata Cortijo et al., 2010, while rest of species could be junior synonyms of C. hartmannae (Cortijo et al., 2010). It is significant for being among the precursors of biologically controlled mineralization and being an important Ediacaran index fossil (Hua et al., 2005).

The geochemical data suggest that Cloudina formed originally aragonitic skeleton (Callow & Brasier, 2005), however, relatively little is known about the biology of Cloudina. There is a record of drilling predation upon Cloudina (Bengtson & Yue, 1992; Hua et al., 2003). Followed from the location of predatory drill holes, Cloudina organism was presumably able to protect its shell nearest to the aperture and its soft body may have been located in the upper, growing portion of the tube (Hua et al., 2003).

According to traditional point of view, Cloudina was closely related to annelids and especially to serpulids (Germs, 1972; Glaessner, 1976). However, Hahn & Pflug (1985) and Conway Morris et al. (1990) did not support Germ's and Glaessner's proposed relationships, and classified Cloudina just in its own family, Cloudinidae. The occurrence of dichotomous branching in C. hartmannae, which implies asexual reproduction led Grant (1990) to classify Cloudina as a coral-like cnidarian. Recently, dichotomous branching has also been found in C. carinata Cortijo et al., 2010, from the Ediacaran of Spain (Cortijo et al., 2010). In contrary, as a result of their thorough review on biology of Cloudina, Hua et al. (2005) found that Cloudina's morphology, skeletogenesis, and asexual reproduction are broadly similar to modern serpulid annelids, indicating possible phylogenetic relationships or morphological convergence. They also concluded that traditional hypothesis of Cloudina's annelid affinities remains plausible.

The earliest definitive annelids with biomineral skeletons (calcitic) were machaeridians in the Early Ordovician, which had a body covered with the calcareous plates (Vinther et al., 2008), but they did not build calcareous tubes. The earliest hitherto known calcareous annelid tubeworms are serpulids (Serpulidae) and their definitive representatives are known from the Triassic (Vinn et al., 2008c, 2008a; Vinn & Mutvei, 2009). The calcareous tubes also occur in sabellid (Sabellidae) and cirratulid (Cirratulidae) polychaetes, since the Early Jurassic (Jäger, 2004; Vinn et al., 2008a) and the Oligocene respectively (Fischer et al., 2000; Vinn, 2009). Recent discoveries on the skeletal structures and biomineralization of calcareous polychaetes (Weedon, 1994; Vinn, 2005, 2007, 2008, 2009; Vinn et al., 2008c, 2008a, 2008b, 2008d, 2009; Sanfilippo, 2009; Vinn & Mutvei, 2009; Tanur et al., 2010) allows us for the first time to make a complete comparison with the skeletal structures and skeletogenesis of problematic tubicolous fossils such as Cloudina.

The aims of this paper are: 

  1. to compare the skeletal structures and skeletogenesis of Cloudina with those of the calcareous polychaete tubeworms (e.g., serpulids, sabellids and cirratulids) in order to test its annelid affinities, and 
  2. to discuss the zoological affinities of Cloudina.

2. Results and Discussion

Cloudina hartmannae tube has a closed origin (Hua et al., 2003, 2005: fig. 1B): Fig. 1 . C. hartmannae (Hua et al., 2003, 2005: fig. 1A-B) and C. carinata (Cortijo et al., 2010: figs. 4-6) tubes do not have flattened attachment surfaces. The diameter of C. hartmannae shell could increase relatively rapidly after dichotomous branching (Hua et al., 2003: fig. 3E, 2005: fig. 1P): Fig. 2 . The tube diameter of both daughter tubes could be about equal and smaller than the diameter of parent tube (Hua et al., 2005: fig. 1K-L, 2007: fig. 6.5) in C. hartmannae (Figs. 2 - 3 ) and different in C. carinata (Cortijo et al., 2010: fig. 8). The shape of C. hartmannae tube cross section changes during dichotomous branching from circular (parent tube) to semi-circular, both daughter tubes (Hua et al., 2005: fig. 1L): Fig. 3 . Growth lamellae of C. hartmannae tube are long and straight in longitudinal section - it lacks chevron shaped growth lamellae - (Hua et al., 2005: fig. 1C): Fig. 4 . Tube wall has a microgranular homogeneous ultrastructure (Feng et al., 2003; Hua et al., 2003: fig. 3O, 2005: fig. 1H): Fig. 5a .

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fig 1
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Figure 1: Cloudina hartmannae from Dengying Formation, closed bulbous basal end (SEM photo reprinted by permission of publisher from Hua et al. (2005: fig. 1A).

Figure 2: Cloudina hartmannae from Dengying Formation, dichotomous branching, showing rapid increase of daughter tubes diameter (arrows), drawn after Hua et al. (2003: fig. 3E).

fig 3
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Figure 3: Cross section of daughter tubes within the parent tube, note the semicircular cross section of daughter tubes (SEM photo reprinted by permission of publisher from Hua et al. (2005: fig. 1L).

a. Discussion of characters

Cloudina has a tubicolous shell that somewhat resembles tubes of calcareous polychaete annelids (e.g., serpulids, sabellids and cirratulids) in its probably calcareous original composition, smooth tube lumen and presence of peristome-like structures on the shells external surface (Figs. 1 - 2 ). Cloudina (Fig. 2 ) also resembles some serpulids (Fig. 6 ) and calcareous Cirratulidae (Fisher et al., 2000) by its occurrence of asexual reproduction (Pernet, 2001; ten Hove & Kupriyanova, 2009). Hua et al. (2005) found that there are following differences between Cloudina and serpulids: a) serpulid tube walls are thicker and solid, and they do not consist of nested funnels; b) the dichotomous branches of serpulids are not as deeply nested within the parent tube as in Cloudina. In addition, we found several other important differences between the calcareous polychaete tubes and Cloudina:

1) Ultrastructure - Annelids do not have microgranular tube ultrastructure. Their primitive tube ultrastructure is either spherulitic - sabellids - (Vinn et al., 2008a), spherulitic prismatic - sabellids and cirratulids - (Vinn et al., 2008a; Vinn, 2009) or composed of irregularly oriented elongate prisms - serpulids - (Vinn et al., 2008c, 2008b). The presence of microgranular tube structure in serpulids is an artifact of sample natural breakage surface. Unpolished and not etched samples of serpulids with irregularly oriented prismatic structure seem to be composed of homogeneous fine granules under SEM (O. Vinn, pers. obs.). The tube ultrastructure of asexually reproducing Salmacina and Filograna, compared to Cloudina by Hua et al. (2005), is not fine microgranular, but composed of irregularly oriented elongate prisms in a homogeneous matrix (see Vinn et al., 2008b): Fig. 5b . However, ultrastructure of organic-rich tabulae (= transverse cross walls) inside the Serpula vermicularis tube is indeed similar to that of Cloudina, but they are formed in a different process than the tube wall (Vinn et al., 2008b). However, the original structure of Cloudina may have not been microgranular, as different phosphatized calcareous skeletons and organic substrates could show this kind of fabric.

fig 4
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Figure 4: Schematic line drawings of Cloudina and serpulid tubes, showing morphology of growth lamellae and tube base.

fig 5
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Figure 5: a.- Microgranular ultrastructure of Cloudina sinensis, Gaojiashan Member of Dengying formation, Ningqiang, Shaanxi, China (after Feng et al., 2003: fig. 1b). b.- Irregularly oriented prismatic structure in cross section in Salmacina incrustans, ZMA V.Pol.3814, Costa Brava, Spain.

2) Biomineralization - Hua et al. (2005) found that Cloudina tubes do not show radial fibrous microstructure or palisade orientation of crystals, crystal nucleation and growth on a sheeted organic or inorganic substrate did not play a significant role in Cloudina skeletogenesis. They concluded that crystals were probably precipitated by skeleton-secreting organs and mixed with an organic matrix, what is similar to serpulids (Hedley, 1958; Neff, 1971; Nott & Parker, 1975). However, standard granular secretion model of serpulids (Hedley, 1958; Neff, 1971) has recently been cast in doubt by the discovery of complex oriented tube structure in Pomatoceros americanus (Vinn et al., 2009) on which the model of serpulid secretion was based. Several other discoveries on the skeletal ultrastructures in serpulids contradict the traditional point of view on their biomineralization (Vinn et al., 2008a, 2008b, 2008d). New evidence on the skeletal structures of serpulids suggests that serpulids were organic matrix-mediated biomineralizers similar to that of molluscs (Vinn et al., 2008a, 2008b, 2008d, 2009; Tanur et al., 2010). The biomineralization of sabellids (Fig. 7 ) and cirratulids produces oriented prismatic structures, perpendicular to organic sheets, which cannot be achieved in a granular secretion process, as well (Vinn et al., 2008a; Vinn, 2009).

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fig 7
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Figure 6: Salmacina amphidentata (Serpulidae), Indian River Lagoon in the vicinity of Fort Pierce Inlet, Florida. Detail of an aggregation showing periodic branching of the tubes. Note that diameter of the daughter tubes increases very slowly after branching (arrows). Drawn after Pernet (2001: p. 110, fig. 1B).

Figure 7: Glomerula piloseta (Sabellidae), Recent, Lizard Island, Australia, polished and etched longitudinal section, showing aragonitic spherulitic prismatic structure. Arrows point to long subparallel to tube walls growth lamellae.

3) Morphology of growth lamellae - Growth lamellae are much longer than in serpulids (Weedon, 1994; Sanfilippo, 1996; Vinn & Furrer, 2008) in the longitudinal section, resembling those of tubicolous molluscs such as vermetid gastropods or scaphopods. Unlike the straight growth lamellae of Cloudina, most of serpulids have chevron shaped growth lamellae (Weedon, 1994; Vinn & Furrer, 2008): Fig. 8 . Thus, tube formation in Cloudina should have been different from that of anterior accretion of serpulid tubes. However, growth lamellae of sabellids - Glomerula - (Fig. 7 ) and cirratulids can be much longer in longitudinal section than in serpulids and thus resemble more those of Cloudina. The growth lamellae of Yangtzitubus (Ediacaran) are slightly similar to those of Cloudina (Liu et al., 2009).

fig 8
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Figure 8: Pomatoceros triqueter (Serpulidae), Recent, Tjärnö, Sweden, polished section treated with Mutvei solution, showing chevron shaped growth lamellae.

4) Morphology of tube origin - Embryonic serpulid tubes are opened at both ends (ten Hove & van den Hurk, 1993; Taylor & Vinn, 2006): Figs. 4 & 9 , in contrast to closed tube origin of C. hartmannae (Hua et al., 2003, 2005): Figs. 1 & 4 . In C. carinata tube origin is reported to be open, but this was based on a fragmentary material, which may not represent complete tubes (Cortijo et al., 2010). Serpulid tubes are often closed off by the tabulae (see Sanfilippo, 2009, and references therein). Similarly, tubes of Glomerula (Sabellidae) have presumably an open origin because of similar tube formation. It is likely that also calcareous cirratulid tubes are not closed at their origin. Thus, the beginning of tube formation in Cloudina should fundamentally differ from that of serpulids and probably also from the other calcareous polychaetes.

fig 9
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Figure 9: Serpulid Spirorbis spirorbis, substrate cemented side, showing an open tube apex (arrow), Recent, North Sea.

5) Shape of tube cross section - Semicircular cross section of daughter tubes lumen inside the parent tube in Cloudina (Fig. 3 ) differs from that of circular lumen cross section of serpulid and sabellid tubes. Tubes with semicircular cross section occur in Yangtzitubus semiteres Liu et al. (2009) from the Ediacaran (Doushantuo Formation) of southern China (Liu et al., 2009), but differently from Cloudina, their tubes are never circular in cross section. A semicircular cross section is also known in Conotubus Zhang & Lin in Zhang (1986) from the Dengying Formation (Ediacaran) of southern China (Hua et al., 2007; Liu et al., 2009).

6) Expansion of the tube - Rapid increase of tube diameter after dichotomous branching in Cloudina (Fig. 2 ) is different from that of slow increase in serpulids (see Pernet, 2001: figs. 1B & 4A): Fig. 6 . Cloudina could have a tube divergence angle about 30° that is not possible in case of serpulid or any other calcareous polychaete tubes (personal obs. O. Vinn). Such a rapid increase in diameter of tube, probably reflecting the increase of soft body volume would have prevented the deep retraction of soft body into the tube possibly in all calcareous polychaete tubeworms. Rapid increase of tube diameter after dichotomous branching in Cloudina somewhat resembles Ramitubus increscens (Liu et al., 2008: pl. 1, fig. 6) interpreted as cnidarian (Chen et al., 2002; Liu et al., 2008) or alternatively as algae (Bengtson, 2005).

7) Change of tube diameter - Diameter of both daughter tubes is smaller than that of parent tube (before branching) after the dichotomous branching in Cloudina (Hua et al., 2005: fig. 1K-L, 2007: fig. 6.5). It is different from that of serpulids where parent tube diameter does not decrease after budding (Pernet, 2001: fig. 4A). Similarly to Cloudina tube diameter of both daughter tubes is smaller than the parent one in Ramitubus increscens (Liu et al., 2008: pl. 1, fig. 6).

8) Attachment surfaces - A lack of flattened attachment surfaces in Cloudina tube differs from that of tubes of calcareous polychaetes. Almost all known calcareous polychaetes begin their growth cemented to the substrate with the exception of serpulid Ditrupa (ten Hove & Smith, 1990). However, the tube of Ditrupa is opened from both ends and it has chevron shaped growth lamellae, two layered tube with outer layer having an oriented ultrastructure (Vinn et al., 2008d). Phylogenetically, Ditrupa is among the most derived serpulids and does not represent the plesiomorphic condition for serpulids (ten Hove, 2008, personal comm.). The plesiomorphic serpulids were all substrate cemented at least in the beginning of their growth.

b. Affinities of Cloudina

Only tubicolous shell, smooth lumen and presence of peristomes in Cloudina are unequivocally similar to that of serpulids (Table 1). Zhuravlev et al. (2011) found some similarity between sabellid tubes constructed of thin organic films and aragonitic layers. However, there are strong differences between Cloudina and other calcareous polychaetes (e.g., sabellids and cirratulids). Cloudina differs from serpulids in the tube ultrastructure, proposed type of biomineralization, closed tube origin (base), semicircular cross section of daughter tubes, rapid increase of the tube diameter after dichotomous branching, change of tube diameter, and lack of attachment surfaces. These differences in tube morphology, ultrastructure and biomineralization indicate that Cloudina is not closely related to any recent skeletal annelid (e.g., serpulids, sabellids and cirratulids) and their skeletons are not homologous (Table 1). However, taking into account that annelids are a very diverse group of invertebrates and biomineralization can appear and disappear several times within the phyla (Taylor, 2008) it is impossible to entirely rule out the annelids as potential close relatives to Cloudina.

Characters
Cloudina Calcareous polychaetes
(Serpulidae, Sabellidae, Cirratulidae)
Cnidaria
Tubicolous shell x x x
Smooth lumen x x x
Peristomes x x x
Asexual reproduction x x x
Granular microstructure x - x
Closed tube base x - x
Semicircular tube cross section x - x
Rapid increase of the tube diameter x - x
Diameter of daughter tubes about equal x - x
Attachment surfaces lacking x - x

Table 1: Comparison of Cloudina characters with calcareous polychaetes and Cnidaria [ x : character present; - : character absent]

The following characters are easiest to understand if one assumes a cnidarian affinity for Cloudina (Table 1):

Thus, the way of asexual reproduction in Cloudina resembles closely that of cnidarians, especially anthozoans. Zhuravlev et al. (2011) found that pattern of asexual reproduction of Cloudina that has been observed by Hua et al. (2005: fig. 1K-R) matches well to intercalar budding of cnidarians but not to serpulid budding with a bud tube development at the surface of the parental one but not inside it (Pernet, 2001). The closed tube origin of Cloudina is also compatible with the hypothesis of an animal of cnidarian grade. There is a coral with conical shell (Cothonion) known from the Early Cambrian of Australia and North Greenland (Peel, 2011). It shares some characters with the Cloudina, such as conical shape, closed base and fast increase of the diameter.

Alternatively, Zhuravlev et al. (2011) found that the presence of both 'hemispherical basal end' and tabulae could favour a microconchid lophophorate affiliation for Cloudina. However, microconchids are evolutionarily derived encrusting tentaculitoid tubeworms, that appeared first in the Late Ordovician (Vinn, 2010), and so not the best candidates among tentaculitoids for comparison with Cloudina. The earliest known tentaculitoids were cornulitids, that presumably appeared in the Middle Ordovician (Vinn & Mutvei, 2009). If tentaculitoid tubeworms are indeed the stem group phoronids as proposed by Taylor et al. (2010), they may well have been present at least as early as in the Early Cambrian. However, early tentaculitoids probably had a plesiomorphic substrate cemented life mode (Vinn & Mutvei, 2009) that differs from life mode of unattached Cloudina. In addition, skeletal ultrastructures of tentaculitoids are much more advanced than that of Cloudina.

In contrast, the simple ultrastructure in Cloudina (Feng et al., 2003; Hua et al., 2005) does not give many clues for comparison with any particular invertebrate phylum as they all could have had such a plesiomorphic condition in the Ediacaran. In addition to Cloudina, tubes could branch in a few other Ediacaran tubicolous fossils (Liu et al., 2009). These are Ramitubus, Yangtzitubus and Waltheria Gaucher et Sprechmann, 1999. Yangtzitubus has also slightly similar wall structure, and it lacks cross walls (Liu et al., 2009). Thus, among the non-biomineralizing tubicolous fossils of Ediacaran, Yangtzitubus could phylogenetically be most closely linked to Cloudina.

c. Paleobiology of Cloudina

Hua et al. (2003) found that predatory borings in Cloudina are located at relatively uniform distance from the shell apertures that points to either control by the life orientation of the shells, such as the position of the sediment surface, or, more likely, an avoidance response by the predator to protective measures located near the aperture.They hypothesized that absence of boreholes further from the aperture implicates one or more of the following:

  1. the older part of the shell was typically embedded in the substrate;
  2. the predator responded to a sensory trigger by drilling nearer to the aperture than the apex; or
  3. the predator was programmed to know that soft tissues were located in the upper, growing portion of the tube.

Cloudina is envisioned here as an animal that is not capable for much moving back and forwards in its tube, or not moving at all, because of the fast increase of tube diameter after the dichotomous branching. The Cloudina animal was probably also entirely attached to the tube wall with its soft body surface and it changed shape of its soft body cross section from circular before the asexual reproduction to semicircular after the asexual reproduction. Presumably, Cloudina was not retracting into the tube in asexual reproduction, but it was divided by lateral fission into two daughter animals which thereafter laterally secreted new tube walls around their soft body inside the parent tube (e.g., almost equal split of a cylindrical funnel into two half-cylinders in C. hartmannae).

3. Conclusions

  1. Cloudina does not share affinities with any extant calcareous tubicolous annelids. 
  2. Cloudina characters are easier to understand if one assumes its cnidarian affinity.

Acknowledgements

We are grateful to the Paleontological Society for a Sepkoski Grant, to Estonian Science Foundation for grant ETF9064 and to the Estonian Ministry of Education and Science for the target project SF0180051s08. We thank Brian Pratt and an anonymous reviewer for constructive reviews.

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