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Synchronous Aggregate Growth in an Abundant New Ediacaran Tubular Organism

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Science  21 Mar 2008:
Vol. 319, Issue 5870, pp. 1660-1662
DOI: 10.1126/science.1152595

Abstract

The most abundant taxon of the Neoproterozoic soft-bodied biota near Ediacara, South Australia, occurs as clusters of similarly sized individuals, which suggests synchronous aggregate growth by spatfall. Tubes of Funisia dorothea gen. et sp. nov. were anchored within the shallow, sandy sea bed and lived in dense, typically monospecific concentrations. Tubes were composed of modular, serially repeating elements. Individuals grew by adding serial elements to the tubular body and by branching of tubes. Their construction and close-packed association imply likely affinity within the Porifera or Cnidaria. These data suggest that several of the most successful marine invertebrate ecological strategies known today were in place in Earth's oldest known metazoan ecosystems before the advent of skeletonization and widespread predation.

Both the structure and associations of Neoproterozoic Ediacaran fossils from near the Flinders Ranges, South Australia, provide information on the complex ecological makeup of Earth's first metazoan habitats (1). The fossil-bearing Ediacara Member of the Rawnsley Quartzite lies 50 to 500 m below a basal Cambrian disconformity and consists of shallow marine thin- to medium-bedded quartz sandstone (2). We excavated beds within the Ediacara Member of the Rawnsley Quartzite at the Ediacara Conservation Park (South Ediacara) and on Nilpena Station of South Australia (fig. S1) to reveal details of the form, diversity, and distribution of these taxa.

A large diversity of fossils in original growth position occurs on successive bedding planes within the more than 150 m2 excavated. Tubular fossils, representing an undescribed structural organization, are more abundant than any other previously described element of the Ediacara biota (1). They occur on nearly all excavated beds and densely on 3 of the 10 beds excavated at Nilpena and 2 of the beds at South Ediacara.

Funisia dorothea gen. et sp. nov. (see supporting online material) is preserved exclusively on the base of beds, as are nearly all fossils in these strata (Fig. 1). Unlike most elements of the Ediacara Biota (3), Funisia is preserved in positive relief, either as flattened casts formed when sand entered the body cavity (Fig. 1, A and D), or as casts of the collapsed body that was impressed into the underlying biomat (Fig. 1, E and G). Collapse and casting is the most common preservation mode because sand rarely fills more than a few centimeters of each tubular body (Fig. 1A). Removal of internal casts leaves an external mold in the overlying bed. In the best-preserved specimens, individual serial units show faint, offset concentric wrinkles that suggest collapse of a thin integument during burial, rather than ornamentation (Fig. 1, E and G).

Fig. 1.

Funisia dorothea gen. et sp. nov. preserved as external casts, internal casts, and external molds on bed bases. (A) Holotype set of subparallel tubes SAM P40725, internal casts, external mold where casts have separated, and as convex casts of collapsed specimens demonstrating various taphonomic variants, including well-preserved serial units, scalloped edge outlines (arrow), and parallel edged outlines. (B) Close-packed set of attachment points (lower left) showing typical convex rim and indented center with or without boss, one with cast of part of tube (arrow); SAM P42681. (C) Growth by branching; SAM P40726. (D) Attachment points with serially constricted tubes; field specimen ES05. (E and G) Specimens showing growth by terminal addition; SAM P41508. (F) Two sets of attachment points demonstrating different stages of development. (H) Enlargement of lower right part of surface in Fig. 2I showing crossed tubes with serial constrictions (arrows). (I) Layered, close-packed specimens radiating from clusters of attachment points (examples marked by arrows); SAM P40309. (J) Densely packed surface with both scalloped and parallel edge preservation; part of very large field specimen, Nilpena. Scale bars, 2 cm.

Funisia is up to 30 cm long and 12 mm in diameter and is divided longitudinally into serial units 6 to 8 mm in length throughout the length of the tube (Figs. 1 and 2). The serial units are defined by constrictions perpendicular or gently oblique to the axis of the tube. Particularly when tubes are bent or curved, constrictions give the tube the appearance of being a spiral, but examination of material preserved nearly in three dimensions (3D) (Fig. 1, D, E, and G) confirms serial segmented construction. In compacted and poorly preserved tubes, or external molds, a scalloped-shaped tube outline, rather than the impression of individual segments, is typically preserved (Fig. 1, A, I, and J). Where F. dorothea covers the surface, the degree of overlapping is such that individual tubes are deformed by composite preservation (Figs. 1, I and J), and under very poor preservation, the sides of the tube appear as parallel lines (Fig. 1A).

Fig. 2.

Reconstruction of Funisia in life position with holdfast beneath mat substrate.

Tube widths range from 2 to 12 mm and are consistent on individual bedding surfaces. These structures were originally interpreted to be strings of fecal pellets (4), but this has since been discounted on the basis of the presence of branching and orientation of specimens (5). Units within the tube taper progressively in width toward the axis, suggestive of growth by terminal addition (6) (Fig. 1, E and G). Individuals can occur within dense assemblages, sometimes greater than 1000/m2 (Fig. 1, I and J). Here, individual tubes of similar size may radiate from a single area of origin (Fig. 1I). In such dense assemblages, tubes completely cover the surface and may overlap or crisscross in a felted manner (Fig. 1, I and J) but most commonly occur in parallel, close-packed groups of 5 to 15 individuals (Fig. 1, A and C). Such groups do not show alignment with current lineations or ripple crests that occur on top of the beds, which suggests that the position of these fossils is not a reflection of transport or reorientation by currents. Rather, they are the result of smothering by sandy event beds in the wake of storm activity (2). Branching is rare, but in such instances, the last common serial unit is expanded and branches remain tightly packed (Fig. 1H).

Tube attachment structures ranging in diameter from 1 to 8 mm are preserved as invaginate bosses on bed soles (Fig. 1, B, C, D, and I). Serially constricted tubes are directly connected to attachment structures (Fig. 1D). The marked modality of size and morphology suggest that different developmental cohorts are preserved (Fig. 1C). Attachment structures of a similar size and developmental stage are spatially clustered within individual bedding surfaces (Fig. 1C). Clustered attachment points are not typically closely packed, but three-dimensionally preserved examples recording the basal several millimeters of the tube demonstrate a hexagonal close packing within millimeters of vertical growth (Fig. 1, B and F). Individual attachments occur without close neighbors but are not common. The size and morphology of attachments range from small knobs 1 to 3 mm in width to well-developed structures that are casts of tube ends with concave hollows (Fig. 1, B, C, D, and I). These structures occur on both ripple crests and troughs and originally extended below the interface between water and substrate. They are clearly attachment discs rather than cross sections through the tubes. Ediacara preservation consists entirely of casts and molds. Cross sections are confined to broken three-dimensionally cast specimens within a bed. Furthermore, there would be some ellipses preserved, and it would not be possible for the tube to be sectioned and still cast by sand.

Like the well-known Ediacaran fronds (7), Funisia tubes are typically preserved without holdfasts attached. In life position (Fig. 2), attachment structures are interpreted to have been situated within or beneath a microbial mat. Where they are cast by sand, the corresponding tube was ripped off by storm activity, allowing sediment to enter the hollow holdfast (Fig. 1C). Alternatively, the holdfast was molded below the mat-bound sediment, and the tube was cast within the overlying sediment or preserved as a collapsed impression at the base of the sediment that engulfed the specimen (Fig. 1B).

The phylogenetic affinity of F. dorothea is problematic. The morphology is consistent throughout all well-preserved specimens and serial units are a 3D character rather than features of external ornamentation. However, the lack of evidence for polypoid openings or pores in the body wall limits our understanding of its taxonomic affinities. Although it is difficult to place these fossils within Metazoa, the morphology and ecology are suggestive of stem-group cnidarians or poriferans. The tightly packed nature of the tubes and attachment structures (Fig. 1I), as well as the rarity of branching, eliminates an algal origin because these characteristics are inconsistent with the maximization of surface area crucial for a photosynthetic habit.

The branching patterns and rarity of branching of Funisia is consistent with metazoan asexual budding. The consistency of tube widths on individual bedding surfaces (Fig. 1, A, I, and J), the densely packed nature of the attachment structures, and the clustering pattern of developmental stages of attachment structures on individual bedding planes suggests that the juveniles settled as aggregates in a series of limited cohorts.

These solitary organisms thus exhibit growth by addition of serial units to tubes and by the division of tubes, and dispersed propagation by the production of spats. Among living organisms, spat production is almost ubiquitously the result of sexual reproduction but is known to occur rarely in association with asexual reproduction (8). Hence, despite its morphological simplicity the Neoproterozoic F. dorothea provides evidence of a variety of growth modes and a complex arrangement for the propagation of new individuals. In living organisms, synchronous aggregate growth may result from a variety of factors—including response to competition, sediment disturbance, and heterogeneity of the substrate—and has the advantage of reducing competition for space between clones and can also decrease gamete wastage (9, 10). It may also reduce vulnerability to predation (9). Borings in the calcified Cloudina may demonstrate predation in the latest Ediacara (11). Furthermore, close packing also imparts protection from current damage and/or high-energy events and allows for selection of most favorable sites for attachment and growth to adulthood (12).

Aggregation is not uncommon among some elements of the Ediacara biota and is present in the frond holdfast Aspidella. These typically occur in dense assemblages, but in contrast to F. dorothea, their size distribution is consistent with continuous recruitment (1, 13, 14) rather than periodic cohort growth. The terminal Neoproterozoic calcified tubes Cloudina and Namacalathus also show evidence of aggregation (15), but there is no indication of distinct cohorts.

These data demonstrate that even morphologically simple Ediacaran organisms had multiple modes of growth and propagation, reminiscent of several of the most successful marine invertebrate ecological strategies today (16). These systems were in place in Earth's oldest known metazoan ecosystems before the ecological pressures that accompanied the advent of skeletonization and extensive predation.

Supporting Online Material

www.sciencemag.org/cgi/content/full/319/5870/1660/DC1

SOM Text

Fig. S1

References and Notes

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