© 2003 by The Society for Integrative and Comparative Biology
A Fungal Analog for Newfoundland Ediacaran Fossils?1
1 Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755 USA
2 Department of Biology, University of Central Arkansas, Conway, Arkansas 72035-5003 USA
3 Department of Geology, Amherst College, Amherst, Massachusetts 01002 USA
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We propose that some of the more conspicuous Ediacaran fossils from the Avalon Peninsula of Newfoundland, including Aspidella, Charnia, and Charniodiscus, were biologically similar to members of the Kingdom Fungi. These organisms were multicellular or multinuclear, lived below the photic zone, could not move or defoul themselves, did not exhibit taphonomic shrinkage, and were not transported or moved. Aspidella, in particular, appears to exhibit indeterminate growth without a maximum size constraint, and appears to show growth zonations similar to modern mycelia. Other fossils from this deposit exhibit a fractal-like growth pattern. Together, these features falsify algal, lichen, and metazoan interpretations of these fossils, yet reflect characteristics of modern fungal mycelia. We emphasize that although no Mistaken Point fossil appears to be a metazoan, not all of the Mistaken Point taxa, and not all of the Ediacaran organisms in general, can reasonably be interpreted using a fungal analogy. Furthermore, the hypothesis that these fossils were functionally fungus-like need not imply that the organisms were members of the crown-group Fungi. We propose further tests for evaluating both this functional hypothesis and the phylogenetic hypothesis that these organisms were members of the total-group Fungi.
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Named for the Ediacara Hills of south Australia, the "Ediacara biota" is a suite of fossils known from about thirty localities on six continents (see Narbonne, 1998
for review). Most of the fossils, classified into about 70 genus-level taxa in all, are restricted to the latest Neoproterozoic, although a few "holdovers" persist into the Cambrian (Jensen et al., 1998; Hagadorn et al., 2000). Despite their local abundance and global distribution, and the fact that they have been studied for over 50 years, most Ediacaran taxa continue to defy taxonomic placement. Traditionally identified as metazoans (usually cnidarian or of cnidarian-grade, e.g., Gehling, 1991), Ediacaran organisms have also been proposed to be lichens (Retallack, 1994), giant protists (Zhuravlev, 1993), colonial bacteria or protozoa (Grazhdankin, 2001), and members of extinct kingdoms (Seilacher, 1989).
Some of the most important localities for studying Ediacaran fossils are on the Avalon Peninsula of Newfoundland. The Avalon section contains two assemblages of Ediacaran fossils: the older Mistaken Point assemblage and the younger Fermeuse assemblage (Narbonne et al., 2001). The Mistaken Point assemblage ranges through a 
3,000 m thick stratigraphic section that spans three formations. Its fossils have not yet been formally described, but have been figured many times and documented in detail (e.g., Misra, 1969, 1971; Anderson and Conway Morris, 1982; Jenkins, 1985, 1992; Clapham and Narbonne, 2002), and similar specimens from central England have been formally named (Ford, 1958; Boynton and Ford, 1995). Some of the more typical Mistaken Point taxa include the stalked fronds Charnia and Charniodiscus, the "bushlike" form Bradgatia, the discoidal Ivesia, and unnamed forms known as "spindles," "ornamented discs" or "pizza discs," "pectinate" forms, "triangles," and "network" forms. The younger Fermeuse assemblage is overwhelmingly dominated by the discoidal fossil Aspidella (Gehling et al., 2000). The Mistaken Point assemblage has been dated at one horizon at 565 Ma (Benus, 1988), making this assemblage older than most of the "classic" Ediacaran assemblages whose ages range from 559 to 543 Ma (Grotzinger et al., 1995; Martin et al., 2000; Compston et al., 2002).
Here we propose, based on our own and others' field observations both in Newfoundland and elsewhere, that the biology of most, if not all, of the Ediacaran organisms from the Avalon Peninsula of Newfoundland cannot be understood using metazoans as analogs. Furthermore, we suggest that the biology of some of the more locally abundant and geographically widespread taxa, including Charnia, Charniodiscus, and Aspidella, is best understood using modern fungi for comparison. We suggest several independent tests for the hypothesis that these Ediacaran organisms functioned like fungal mycelia, and also propose tests to evaluate the separate hypothesis that the Ediacaran organisms are close phylogenetic relatives of modern fungi. We emphasize at the outset that we are not attempting to "shoehorn" every Ediacaran fossil into the Fungi; there are many Ediacaran fossils for which a fungal model is clearly inappropriate. We also stress that no Mistaken Point taxon can be reasonably interpreted as belonging to the crown-group Fungi (i.e., the last common ancestor of all living fungi plus all of its descendants living or extinct). At best, some of the Mistaken Point taxa might be very basal stem-group fungal forms (i.e., more closely related to Fungi than to Metazoa). However, we draw a line between phylogenetic questions (e.g., to whom are Ediacaran organisms related?) and functional questions (e.g., how did Ediacaran organisms grow, move, reproduce, feed, and senesce?). Even if some or all of the Ediacaran fossils were members of an extinct kingdom or (more likely) kingdoms (e.g., Seilacher, 1989, 1992; McMenamin, 1998; but see Runnegar, 1995), comparisons with extant organisms can still provide insights into the biology of Ediacaran organisms. Perhaps more importantly, comparisons between the Ediacaran organisms and extant taxa are constrained by what the living taxa are capable of; correct or not, such approaches yield more testable, tractable hypotheses than does the creation of extinct kingdoms of life.
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The morphological complexity of the Mistaken Point taxa, and the absence of stromatolite layers or other microbial structures (e.g., Hagadorn and Bottjer, 1997
) in disc-like forms such as Aspidella, indicate that they are multicellular/multinuclear, and are not, for example, colonies of single-celled organisms (as suggested by Bergström, 1991; Duval and Margulis, 1995; Grazhdankin, 2001; Steiner and Reitner, 2001). Zhuravlev (1993) proposed that the Ediacara organisms were giant single protists, analogous with, if not related to, extant xenophyophores (see also Leguta and Seilacher, 2001). However, structural studies of Ediacaran fossils have thus far failed to reveal traces of an agglutinated, mineralized, or sclerotized shell or test, whose presence is implied by this hypothesis (Waggoner, 1998; B.W., personal observations). This leaves the myxobacteria and actinomycetes among the "prokaryotes," and the slime molds, complex multicellular algae, metaphytes, fungi, and animals among the eukaryotes, as the only modern analogs which can be reasonably considered for the Mistaken Point taxa.
Most of these analogs can be ruled out quickly. Neither myxobacteria, actinomycetes, nor slime molds are known to make structures as large or as complex as a frondlike Ediacaran fossil (the fruiting bodies of all three are in the millimeter to submillimeter size range). The Avalon biota was wholly benthic (Seilacher, 1992), and unlike most Ediacaran deposits, lived well below the photic zone, having been buried in situ (Landing et al., 1988) more than a kilometer below the ocean surface (Misra, 1971, 1981; see also correction of Dalrymple et al., 1999 in Narbonne et al., 2001). Together with autochthonous Ediacaran assemblages from other deep-slope deposits (Ford, 1958; Cope, 1977; Gibson et al., 1984; Narbonne and Aitken, 1990; Ferguson and Simony, 1991), the depositional environment of the Mistaken Point fossils refutes the hypothesis that these taxa were photoautotrophic or harbored photosymbionts (e.g., Retallack, 1994; McMenamin, 1998), and thus the fossils are not algae, metaphytes or lichens.
The most likely possibilities are that the Avalon fossils were animal-like or fungus-like. We hypothesize that Mistaken Point taxa are not metazoans, and that some are best understood using modern fungi as analogs. We can support this hypothesis by using these fossils' distinctive modes of preservation and growth.
Preservation
The Mistaken Point taxa are typically preserved underneath ash beds (Anderson, 1978; Jenkins, 1992; and Fig. 1). Curiously, although the organisms in Figure 1 are buried under only a few millimeters of ash, there is no disturbance of either the overlying ash or the underlying sediment that would indicate that they attempted to escape or defoul themselves in any way during burial. These fossils are not unique: regardless of the amount or composition of smothering sediment, not a single fossil in the Newfoundland sequence exhibits any evidence of escape behavior or defouling. Furthermore, unlike Australian and White Sea Ediacaran fossils (Runnegar, 1982; Seilacher, 1989; Gehling, 1991; Ivantsov and Fedonkin, 2001), Newfoundland fossils never show any signs of contraction. Even more startling, although there are perhaps hundreds of thousands of fossils preserved on thousands of layers throughout 3,200 m of section, there is not one trace fossil in the entire sequence which represents active movement of an organism (cf., Gehling et al., 2000; Leguta and Seilacher, 2001).
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Despite these observations, all of the commonly proposed metazoan analogs for Mistaken Point fossils are capable of pre- and post-burial movement, particularly when seeking to avoid deleterious conditions (e.g., Collins et al., 2000
). For example, colonial anthozoan cnidarians, in particular the Pennatulacea or "sea pens" (the group most commonly considered to be phylogenetically related to the fronds: Jenkins and Gehling, 1978; Jenkins, 1985; Conway Morris, 1993) are quite capable of moving, defouling themselves, and burrowing both upwards and downwards. Pennatulaceans may bioturbate the sediment significantly and produce preservable traces (Bradley, 1980, 1981; Seilacher-Drexler and Seilacher, 1999; Hagadorn et al., 2002). Given: 1) the thousands of census populations that were buried in situ by thin veneers of ash; and 2) the abundance of sedimentary facies which are optimal for the preservation of trace fossils (i.e., interbedded sand and silt-dominated layers characterized by scour- and/or fill-events), it is surprising that none of the organisms living on the Mistaken Point seafloor attempted to move or defoul whatever respiratory or feeding systems they may have had during a fairly innocuous burial event.
If the Mistaken Point organisms were metazoans, then the lack of escape or locomotive traces would only be expected if they were of poriferan-grade. The hypothesis that they are sponges is difficult to refute as preservation of such detail is not found at Mistaken Point. Nonetheless, we see no evidence for spicules or fibers, despite their presence in other Neoproterozoic fossils and deposits (Gehling and Rigby, 1996; Brasier et al., 1997; Li et al., 1998; Chen et al., 2000), nor do the Mistaken Point fossils show any structures that plausibly resemble intake pores or oscula. Furthermore, several of the Mistaken Point taxa, such as the "pizza and bubble discs," lived embedded in sediment. This is shown by their preservation in layers 1 mm-2 cm below ash beds, rather than on ash-bearing bed interfaces (Fig. 1A, C), and by frondose fossils (preserved at bed interfaces) which drape the topographic bumps and troughs of underlying (buried) pizza/bubble discs. Similar evidence illustrated by Gehling et al. (2000) for Aspidella indicates that these organisms lived through multiple episodes of sediment accretion, presumably deposited under "normal" marine conditions, and continued to grow as long as they were not completely buried. Most filter-feeding sponges cannot live embedded within sediment, refuting the hypothesis that even the most basal metazoan clades can serve as analogs for Mistaken Point fossils.
A second preservational consideration is that Newfoundland Ediacaran taxa never show signs of shrinkage or compaction. Expanding upon taphonomic observations first reported by Seilacher (1989, 1992), Retallack (1994) argued that Ediacaran taxa were as resistant to compaction as woody plants, and proposed a lichen affinity for most Ediacaran fossils. Compaction resistance by itself does not indicate a lichen or fungal affinity for these fossils. Even "flimsy" cnidarians such as jellyfish may be surprisingly tough (Waggoner, 1995; Hagadorn et al., 2002), and microbially-mediated precipitation of minerals around a soft-bodied carcass can affect its potential for compaction, even in coarse siliciclastic sediments (e.g., Gehling, 1999). Despite these considerations, we agree with Retallack (1994) that the consistent lack of taphonomic shrinkage in a wide range of depositional environments suggests that these organisms maintained a degree of structural stability even after the loss of hydrostatic pressure, and most likely accomplished this with the possession of cell walls. Cell walls are found in modern plants, most algae, lichens and fungi, but the water depth at which these organisms lived rule out an affinity with all except the Fungi as the only reasonable modern analog for the Newfoundland Ediacaran taxa. One alternative is that the Newfoundland Ediacaran organisms had internal or external skeletons that could flex but not contract; this might be expected if the fossils were related to colonial cnidarians, such as gorgonians, antipatharians or pennatulaceans, which have internal supports. However, the Newfoundland frond-like fossils never show traces of individual zooids, mouths, or other features which would suggest that they had a body plan similar to that of colonial cnidarians. Furthermore, the kind of structural heterogeneity, in which some layers or zones of the body are not only firm but separable from the softer parts, as seen in Kimberella (Fedonkin and Waggoner, 1997), is not present in the Mistaken Point fossils.
One final preservation consideration is the relationship between the fossils and microbial mats. Several of the Mistaken Point frondose fossils, notably Aspidella, Charnia and Charniodiscus, have unusually wide geographical and environmental ranges in contrast to most other Ediacaran taxa (Narbonne, 1998; Waggoner, 1999a, 2003). These organisms lived at depths ranging from shallow subtidal to deep slope environments, and in facies dominated by a variety of lithologies, ranging from very fine to coarse clastics and fine carbonates. They also extended over 130° of paleolatitude, including both equatorial and polar localities (Waggoner, 1999a, 2003). These organisms would have lived in environments spanning the full range of light regimes, ranging from shallow waters with nearly even daylengths to dramatic seasonal variations in daylengths, to lightless, deep-water continental slopes. Presumably, these organisms would also have spanned a wide range of temperature regimes, from constant near-freezing temperatures to variable and relatively warm temperatures. Thus, the biogeographic distribution of these taxa appears to be independent of light, water depth, sediment type, and temperature. The only constant among all of these deposits is the presence of associated microbial mats (reviewed in Gehling, 1999; see also Gehling et al., 2000, and Wood et al., 2001).
The fact that the organisms lived upon or within microbial mats raises an interesting question: why is there no evidence of transport? The flatter forms, such as the "spindles," are randomly distributed on the substrate with no preferential alignment (Seilacher, 1992, 1999); they lack drag marks or any other trace of having been transported, they are never washed together, and only rarely are they folded over (Seilacher, 1992, 1999; Narbonne et al., 2001). Even more puzzling, no fragments of torn specimens have been noted. Schopf and Baumiller (1998) suggested various ways in which relatively flat Ediacaran fossils could have stayed in place on the sediment, and one possibility is that these fossils were very dense. However, high density cannot explain the preservation of the "frondlike" taxa Charnia and Charniodiscus at Mistaken Point. These fronds have been felled by directional currents and are aligned with the paleocurrent direction (Landing et al., 1988; Seilacher, 1992, 1999), yet: (1) show no signs of having been ripped up; (2) have the holdfast and frond preserved on the same bedding plane (showing that the "holdfast" did not penetrate or lie within the underlying sediment; cf., Seilacher-Drexler and Seilacher, 1999); and (3) have a relatively high-drag design that should have resulted in great mechanical stress on the organisms during current flow, regardless of how dense they were. "Giant" Charnia specimens from the Drook Formation are 
1 m in length but have a holdfast only 
4 cm in diameter (Narbonne et al., 2001), and it is doubtful whether these structures, if they functioned like modern sea pen holdfasts, could actually keep such forms anchored to the sediment given the abundance of turbid flows and contour currents (Benus, 1988; Landing et al., 1988; Seilacher, 1999). In fact, recent descriptions of organic remains of charniid-like fossils from the White Sea demonstrate that the holdfast was not an attachment bulb but a flat, circular membrane attached to a microbial mat (Steiner and Reitner, 2001; see also Seilacher, 1989, 1999; and Fig. 3B). Furthermore, the "bush" form Bradgatia lived attached to the sediment, had a relatively high-drag design that stuck several cm up into the water column, and exhibits no signs of transport—yet it has no visible holdfast at all (Jenkins, 1992; Fig. 1B). We suggest that something too small to be preserved at Mistaken Point was anchoring these organisms to the bottom (Schopf and Baumiller, 1998; Seilacher, 1999). Our hypothesis is that the "anchors" were hypha-like filaments.
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In summary: the Mistaken Point organisms were not capable of movement; they either grew embedded within sediments or attached themselves to soft substrates but never burrowed into them; and they may have possessed cell walls. We conclude that they were not metazoans. The only major clade of multicellular organisms that fits all of these criteria, and is not photoautotrophic, is the Fungi.
Growth
No frondlike fossils have yet been described from the Fermeuse assemblage, which is overwhelmingly dominated by the highly variable discoidal fossil Aspidella. Two aspects of Aspidella growth also point to a fungal analogy. The first concerns the size distribution of Aspidella specimens. Aspidella is extremely common in the Fermeuse Formation, with densities of specimens on surveyed surfaces approaching 4,000 per m2 (Gehling et al., 2000). Conway Morris (1989) and Gehling et al. (2000) each measured the diameter of hundreds of Aspidella specimens from a single bedding plane, and both found that the distributions of diameter vs. abundance are significantly right skewed (g1 = 3.84 ± 0.09, t value = 41.8, P < 0.001; reproduced here as Fig. 2A). Although Conway Morris (1989) and Seilacher (1989, 1992) stated that this distribution is atypical for metazoans, Gehling et al. (2000, after Levinton and Bambach, 1970, and Parker, 1975) ascribed this distribution to typical metazoan benthic communities with high juvenile mortality. Nonetheless, a key difference between the distributions of Levinton and Bambach (1970) and Gehling et al. (2000) is that Levinton and Bambach explicitly stated that none of their distributions are the result of "instant" mass mortality due to, for example, sudden burial and suffocation by sediment. This is decidedly unlike the Aspidella beds in Newfoundland, where populations are repeatedly buried over time. Hence the distributional data from Gehling et al. (2000) and Conway Morris (1989) reflect a census population which was alive at the time of burial.
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To test whether or not the Fermeuse Aspidella beds are unusual in that they represent high juvenile mortality rates, we measured the diameter of over 200 fossils referable to Aspidella (i.e., Cyclomedusa, Ediacaria, Paliella, and Tirasiana; see Gehling et al., 2000
for synonymy) from Member 1 of the Winter Coast of the White Sea of northern Russia. Although this does not represent a census population, the specimens all come from a narrow stratigraphic interval (1–2 m) with no detectable change in the paleoenvironment with time. The frequency distribution is shown in Figure 2B. As is the case for the Newfoundland specimens, this distribution is also significantly right skewed (g1 = 1.20 ± 0.16, t value = 7.44, P = 0.001) suggesting that the unusual distribution of Gehling et al. (2000), rather than reflecting high juvenile mortality, may reflect indeterminate and linear growth rates, assuming that single Aspidella specimens are individuals rather than colonial metazoans (contra Dewel et al., 2000).
Most metazoans have determinate growth: growth either ceases at sexual maturity or dramatically slows with respect to the exponential growth phase of the curve. Even in metazoans whose growth is theoretically indeterminate, such as sea anemones, individuals above a certain size usually cease to get larger, whether because they undergo fission, because environmental conditions restrict growth, or because a larger size is energetically inefficient (Ottaway, 1980; Sebens, 1980, 1981). Thus, a plot of size vs. age in a metazoan population typically has a logarithmic or sigmoidal shape (Sussman, 1964; Levinton and Bambach, 1970). What is important is that even if there is high juvenile mortality, the endpoints of the size distribution will not change significantly; only the mode will be shifted leftward. Fungal mycelia grow indeterminately at a constant rate throughout life, aside from a very brief period in the earliest stages in which growth is exponential (Klein, 1996; Carlile et al., 2001), so the relationship between mass and age is linear. Because fungal growth does not cease at "sexual maturity," and because the energetics of feeding in most fungi are quite different from those of metazoan bodies, there is no limit to the right endpoint. Consistent with this fact and our hypothesis, we observed Aspidella specimens that are 150 mm in diameter in the Fermeuse and Mistaken Point Formations; these sizes are twenty-five times larger than the mode found by Gehling et al. (2000). Hence, we predict that even larger specimens of Aspidella can and will be found (e.g., from the Cariboo Mountains of Canada, where exceptionally large Aspidella forms have been illustrated in reconnaissance mapping reports; Ferguson and Simony, 1991). In contrast, we predict that true Ediacaran metazoans will show determinate growth; for example, we predict no specimens of the putative metazoan Kimberella will be found that are significantly larger than their currently known maximum size of 130 mm, and a distribution of size vs. frequency will be either distributed normally or will be left skewed.
A more conclusive way to test for indeterminate growth would be to show that the growth rates of all Aspidella specimens on a single well-preserved bedding plane are the same, regardless of the individuals' size. To measure growth, one would need to measure the increase in diameter of a population of specimens as they grow upwards within laminated sediment. By serially sectioning a single slab of specimens perpendicular to the bedding plane (see Fig. 10 from Gehling et al., 2000), one could use laminations as time intervals, and compare fossil diameter to number of laminations. By correlating laminations between specimens, and by using specimens from the same slab, variations in depositional rates of individual laminations would be constant between specimens. If our model is correct, plots of diameter versus lamination number (hence, growth rate) should exhibit a linear shape. However, if larger specimens consistently grew very slowly as compared with smaller specimens, then this would refute a fungal model of growth for Aspidella.
A second interesting aspect of Aspidella growth is shown in Figure 3A. Many specimens which have no apparent aperture or open cavity (i.e., they are not Ernietta-type fossils) contain sand in the middle of the specimen, sediment which is coarser-grained than the shale surrounding the specimen. Conway Morris (1989) also noted this sedimentologic conundrum and suggested it pointed to an inorganic origin for Aspidella. We propose instead that the reason there is sand in the middle of Aspidella specimens is that this area is analogous to the aged zone of a modern fungal mycelium: sediment is being deposited here because of the absence of living tissue. A typical fungal mycelium that has a clearly defined margin and that is growing with a linear increase in the radius will show spatial differentiation from the margin to the center. From the outside inward, the mycelium has three or four zones: the extending zone, the productive zone or zone of proliferation, sometimes a specialized fruiting zone, and, at the center of the colony, the senescent zone, in which fungal cells are vacuolating and undergoing cell death (Klein, 1996; Carlile et al., 2001). A non-quantitative examination of bedding planes and hand samples from the Fermeuse Formation reveals that sand-filled specimens are rare among the small individuals, but are common among the larger individuals. This is consistent with the growth dynamics of modern mycelia: small mycelia would not have developed an aged zone. The alternative hypothesis, that this represents post-mortem collapse and infill, fails to explain why the sand is always found only in the very center of the specimens and why the sand infill is preserved in convex epirelief. Furthermore, we note that the diameter of the infill appears to be proportional to the diameter of the specimen, but this observation needs to be quantified.
Similar grain size variations may occur in charniids from the Ust'-Pinega Formation in the White Sea (Steiner and Reitner, 2001), and potentially in Cyclomedusa specimens from the Rawnsley Quartzite of South Australia (Fig. 3B). For example, the Cyclomedusa in Figure 3B has a stalk which was filled with sediment, and is preserved in three dimensions on at least two different layers. This mode of preservation suggests that either the center of the organism was filled with sediment prior to burial, or that sediment was injected into the organism's carcass coincident with burial. Because there is only a slight difference in grain size between the sediment filling the stalk and the surrounding sediment in this specimen, we cannot refute the latter hypothesis at this time. Nonetheless, because some charniids figured from the White Sea may also have sand in the middle, the stalk may have been filled with sediment long before burial. If true, this would indicate that the stalk is not a permanent feature of the organism, but instead may be a temporary structure akin to a "fruiting body." This hypothesis is consistent with the paucity of fronds or stalks attached to Aspidella specimens, and the complete absence of a detached fronds found among the tens of thousands of Ediacaran fossils preserved in this region, suggesting that Aspidella could have been the basal disc of an ephemeral frondlike body (Gehling et al., 2000).
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A fungal model appears to be the most applicable model for some of the Mistaken Point biota, at least from a structural and physiological standpoint. Therefore, we hypothesize that these organisms lived saprophytically upon sulfate-reducing bacteria (sensu Seilacher, 1989
), rather than feeding in the water column (contra Clapham and Narbonne, 2002). We further hypothesize that these organisms reproduced asexually by extending hypha-like structures throughout the mat-laden sediment, and that it is these hyphae which give Neoproterozoic microbial mats their rigidity. Finally, the possession of a stalk in taxa which lived in the mat (e.g., "pizza discs," Narbonne et al., 2001) is consistent with the idea that these taxa must have had some sort of extension or vane which extended into the water column for respiration, unlike those taxa which lived on the mat and had a high surface area to volume ratio (e.g., Aspidella).
Because the kingdom Fungi is the only major living taxon whose members are multicellular/multinuclear, have cell walls, are heterotrophic, do not move, and grow indeterminately, an affinity with modern fungi is not out of the question. However, these characteristics, by themselves, do not mean that the Mistaken Point organisms belong within total-group Fungi. A number of protist lineages have independently evolved fungus-like morphologies, notably the oomycetes, thraustochytrids, and various "slime molds." It is possible that the Avalon organisms belonged to one of these, or to an analogous but extinct protist lineage—a hypothesis very similar to Seilacher's original "Vendobionta" hypothesis (Seilacher, 1989, 1992). This raises the phylogenetic question: are the Avalon fossils related to modern Fungi?
In terms of relating them to modern marine fungi, comparisons are hampered because modern taxa have only been studied for about the last sixty years (Barghoorn and Linder, 1944), and are much less well known than their terrestrial relatives. In fact, compared to the 77,710 species of terrestrial fungi, only 498 marine species were recognized as of 1986 (Molitoris and Schaumann, 1986). Furthermore, many of these marine taxa have been described only from isolated spores; the morphology of the vegetative form remains unknown. Nonetheless, marine fungi are much more abundant and diverse than is commonly acknowledged, especially beyond the mid-archibenthic region (Johnson and Sparrow, 1961), and at least some taxa (i.e., so-called primary marine fungi) appear to have originated in the oceans (e.g., Kohlmeyer, 1986; Spatafora et al., 1998). Moreover, some marine fungi do produce fruiting structures, such as ascocarps, which may be thick-walled and mechanically resistant. These are much smaller than the Mistaken Point fossils (<1 mm), but because much of the diversity of extant marine fungi remains unknown, it is premature to accept this as a limitation on the size of the structures that marine fungi are capable of producing.
Because the Mistaken Point taxa share no known characters with any modern fungal lineage, inclusion with the fungal crown group is suspect. Furthermore, primary marine fungi are obligate parasites (Kohlmeyer, 1986), and as such cannot be related to nor used as an analogy for Mistaken Point taxa. There are secondary marine fungi, such as the free-living arenicolous fungi which are found among sand grains in marine environments, which may have a lifestyle closer to that which we infer for the Mistaken Point organisms (Kohlmeyer, 1984). However, secondary marine fungi are inferred to have evolved from terrestrial ancestors (Kohlmeyer, 1986) and again cannot be phylogenetically close to the fossil taxa of interest. One final consideration is that the known fruiting bodies of marine fungi are not as geometrically complex as the Mistaken Point taxa. An interesting but enigmatic aspect of the growth of Mistaken Point "spindles" and fronds is that they grow "fractally" (as defined by Seilacher, 1989; this is not always equivalent to the strict mathematical definition of the term). In other words, they maintain the same number of segments regardless of size, although the segments become increasingly subdivided (Seilacher, 1992, 1995). This could be similar to modern fungal growth patterns, such as mushroom gill development, which follow Seilacher's "fractal" pattern of adding secondary subdivisions between primary divisions (Moore, 1996). However, no known fungal form shows such a large, complex and repeatable fractal geometry as seen in the spindles or Charnia.
Nevertheless, exclusion from the crown group does not mean that the Mistaken Point taxa cannot be fungi: they very well could be stem-group taxa (it is worth remembering that Stegosaurus, although not very bird-like in appearance, is still a stem-group bird). Inclusion within total-group Fungi is not inconsistent with the known fossil record. Fungus-like microfossils have been found at several Late Proterozoic sites (e.g., Schopf and Barghoorn, 1969) including Ediacaran fossil-bearing rocks on the White Sea (Burzin, 1993). Although these microfossils are difficult to classify, and some could belong to non-fungal taxa such as the Oomycota (Sherwood-Pike, 1991), the fungal fossil record is at least loosely consistent with molecular clock dates which estimate that total-group Fungi evolved before 700 Ma ago (K.J.P., unpublished), and crown-group clades began diversifying around 550 Ma ago (Berbee and Taylor, 1993).
To test the hypothesis that the Mistaken Point organisms are members of total-group Fungi, one needs to show the possession of a fungal-specific character. One possibility would be to look for preserved hyphae in Ediacaran fossils and in associated microbial mats, specifically hyphae with perforate cell walls. Although indirect evidence suggests that some of these fossils were connected to a hypha-like network in the substrate (see above), the physical presence of hyphae cannot yet be demonstrated in these fossils (which is not surprising given that the size of typical hyphae is 3–10 µm; Carlile et al., 2001). An ideal place to look would be in phosphorites like the Neoproterozoic Zhongyicun Formation of China, where submicron-sized structures are commonly preserved, and where suspect-microbial structures have already been documented (Dornbos et al., 2001).
A second direct way to demonstrate the presence of fungi is to identify fungal-specific biomarkers. One important fungal-specific molecule is ergosterol, the major constituent of the plasma membranes of fungi (Carlile et al., 2001). Given the presence of sterols in Proterozoic and even older rocks (Brocks et al., 1999) it should be possible to detect the sedimentary molecules derived from ergosterol in well preserved bacterial mats. Although detecting these derivatives would demonstrate the existence of Fungi in these deposits, it would not prove that any one taxon in particular is a fungus, and, of course, contamination from modern fungi would have to be ruled out by careful collecting. Nonetheless, demonstrating that fungi lived within the bacterial mats would be an important step in understanding the ecology of the Late Neoproterozoic.
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Our fungal model is not appropriate for many other Ediacaran taxa, including such enigmatic Mistaken Point taxa such as the "triangles" (Clapham and Narbonne, 2002
), and the "bilaterian" forms from younger deposits such as Dickinsonia, Kimberella, Yorgia, and Parvancorina. Dickinsonia specimens do show contraction, distortion, and shrinkage that could result from muscle contraction (Seilacher, 1989; Gehling, 1991); some also show internal structures that resemble metazoan gut caeca or gonads (Gehling, 1991; Jenkins, 1996; Dzik and Ivantsov, 2002). Trace fossils, including escape structures, have also been found associated with Kimberella and Yorgia (Gehling, 1996; Seilacher, 1997; Ivantsov and Fedonkin, 2001). Finally, taxa such as Dickinsonia and Kimberella, not only grow like metazoans (Runnegar, 1982; B.W., personal observation), but are restricted to shallow-water deposits within one biotic province (Waggoner, 2003). This stands in stark contrast to the widespread ecological and geographic distribution of Avalonian taxa such as Aspidella, Charnia, and Charniodiscus—suggesting that there must be pronounced ecological and physiological differences between these Mistaken Point taxa and "bilaterian" taxa like Kimberella.
We do not automatically assume that all such "bilaterians" were necessarily metazoans, although we still feel that that is the best hypothesis for many of them. However, we would strongly caution against the tacit assumption that all Ediacaran organisms must share one Bauplan. For most of their 50 year history, the Ediacara biota has been assumed to represent one and only one kingdom-level taxon, whether Metazoa, lichenized Fungi, Protista, or an extinct kingdom. Such "shoehorning" has obscured the fact that there may have been several major functional groups of Ediacaran fossils that evolved and behaved differently. This should not be a surprise: most Konservat-Lagerstätten contain members of two or more kingdom-level taxa that happen to be preserved in a similar way. There is sound evidence for the presence of sponges and cnidarians among the Ediacara organisms (Gehling, 1988; Gehling and Rigby, 1996), along with plausible bilaterian metazoans similar to stem-group molluscs and arthropods (Fedonkin and Waggoner, 1997; Waggoner, 1999b). However, this does not and never has meant that all Ediacaran taxa must be interpreted as metazoans, any more than our work should be taken to imply that all Ediacaran taxa were giant mushrooms. In the end, a recognition of the high-level diversity within the Ediacara biota will provide a fuller context for understanding the origins of multicellularity and the ecological context of the origin of metazoans. In addition, recognition that other living systems might provide a better model to understand the biology of some Ediacaran taxa will eventually shed insight into their proper phylogenetic position(s).
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ACKNOWLEDGMENTS |
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We owe a great deal to J. G. Gehling, R. W. Dalrymple, and G. M. Narbonne, who convened a special session at the 2001 Geological Association of Canada/Mineralogical Association of Canada meeting, and led a field trip to examine the late Neoproterozoic strata of the Avalon Peninsula of Newfoundland. We also thank B. Runnegar, G. Retallack, A. Seilacher, M. Clapham, and D. Wood for fruitful and enlightening discussions, M. A. McPeek for his help with the statistical analyses, J. Gehling, S. Conway Morris, and two anonymous referees for their insightful reviews of an earlier draft of this manuscript. KJP is supported by NSF, NASA-Ames and Dartmouth College. BW thanks M. A. Fedonkin and the Paleontological Institute of the Russian Academy of Sciences for access to Russian material, and the College of Natural Science and Mathematics at the University of Central Arkansas for funding his participation in the 2001 GAC/MAC meeting. JWH is grateful to J. Kirschvink, K. Nealson, and the Caltech Division of Geological and Planetary Sciences for support of fieldwork in Newfoundland and postdoctoral salary support.
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FOOTNOTES |
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1 From the Symposium The Cambrian Explosion: Putting the Pieces Together presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 2–6 January 2002, at Anaheim, California.
2 E-mail: kevin.peterson{at}dartmouth.edu
3 E-mail: benw{at}mail.uca.edu
4 E-mail: jwhagadorn{at}amherst.edu
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