PALAIOS, 2014, v. 29, 145–153
Research Article
DOI: http://dx.doi.org/10.2110/palo.2013.075
SEDIMENT EFFECTS ON THE PRESERVATION OF BURGESS SHALE–TYPE COMPRESSION FOSSILS
LUCY A. WILSON
AND
NICHOLAS J. BUTTERFIELD
Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EQ, U.K.
e-mail: [email protected]
ABSTRACT: Experimental burial of polychaete (Nereis) and crustacean (Crangon) carcasses in kaolinite, calcite, quartz, and
montmorillonite demonstrates a marked effect of sediment mineralogy on the stabilization of nonbiomineralized integuments,
the first step in producing carbonaceous compression fossils and Burgess Shale–type (BST) preservation. The greatest positive
effect was with Nereis buried in kaolinite, and the greatest negative effect was with Nereis buried in montmorillonite, a
morphological trend paralleled by levels of preserved protein. Similar but more attenuated effects were observed with Crangon.
The complex interplay of original histology and sediment mineralogy controls system pH, oxygen content, and major ion
concentrations, all of which are likely to feed back on the preservation potential of particular substrates in particular
environments. The particular susceptibility of Nereis to both diagenetically enhanced preservation and diagenetically enhanced
decomposition most likely derives from the relative lability of its collagenous cuticle vs. the inherently more recalcitrant cuticle
of Crangon. We propose a mechanism of secondary, sediment-induced taphonomic tanning to account for instances of enhanced
preservation. In light of the marked effects of sediment mineralogy on fossilization, the Cambrian to Early Ordovician
taphonomic window for BST preservation is potentially related to a coincident interval of glauconite-prone seas.
INTRODUCTION
Carbonaceous compression fossils are a major source of paleobiological data, in particular as it relates to capturing the early Paleozoic record
of ‘‘exceptional’’ Burgess Shale–type (BST) macrofossils (Butterfield
1990, 1995; Gaines et al. 2008; Page et al. 2008; Orr et al. 2009) and their
microscopic counterparts (Butterfield and Harvey 2012). Even so, the
circumstances and processes leading to the preservation of such fossils—
and thereby their paleobiological implications—have yet to be fully
resolved. The Phanerozoic record of BST-type preservation, for example,
appears to be limited to an early (but not earliest) Cambrian to Early
Ordovician taphonomic window (Butterfield 1995; Van Roy et al. 2010),
obscuring its contribution to both the Cambrian and Ordovician
radiations. Localized dysoxia–anoxia is certainly a prerequisite for
preserving nonbiomineralizing fossils, but this falls well short of a full
explanatory account. Even in the absence of oxygen, simple hydrolysis,
autolysis, and the activities of anaerobic microbes continue to degrade
carbonaceous substrates, rapidly obliterating original morphology.
Sedimentary matrix is fundamental to the fossilization process, not
only as basic packing material but also based on its potential to alter the
chemistry of early diagenesis. Despite reports of accelerated carcass decay
associated with some sediments (e.g., Plotnick 1986; Allison 1988; Briggs
and Kear 1993), most models for BST preservation invoke mineralspecific diagenesis as an essential factor, either by suppressing normal
enzyme–microbial-based decay processes (e.g., Butterfield 1990, 1995;
Gaines et al. 2005, 2012) or secondarily by enhancing the recalcitrance of
relatively labile substrates (e.g., Orr et al. 1998; Petrovich 2001).
Surprisingly, there has been little attempt to test these various models,
though Martin et al. (2004) have shown that sedimentary particles will
adhere to lobster eggs in the presence of bacteria, and Naimark et al.
(2013) have documented substantially enhanced preservation of Artemia
when they are buried in kaolinite. In this study we adapt the seminal,
sediment-free decay experiments of Briggs and Kear (1993, 1994a) to
investigate the effect of sediment mineralogy on the decay and early
diagenesis of two ‘‘model’’ nonbiomineralizing marine invertebrates:
Nereis virens (polychaete annelids with collagenous cuticle, sclerotized
collagenous jaws, and sclerotized chitinous chaetae) and Crangon crangon
(crustacean arthropods with variably sclerotized chitinous cuticle).
MATERIALS AND METHODS
In order to test the effects of sediment mineralogy on preservation
potential, we buried freshly killed Nereis and Crangon in four different
seawater-saturated sediments: kaolinite, quartz, calcite, and Ca-montmorillonite. After 4 months the carcasses were exhumed for qualitative
morphological assessment and semiquantitative chemical analysis
(structural protein, chitin, water-soluble protein, carbohydrate, and
phospholipid).
All of the sediments used in the experiments were mineralogically pure
and texturally homogeneous, though the particle size (measured using a
Micromeritics SediGraph, model 5100) differed among the four materials:
(1) kaolinite, a 1:1 layer clay, supplied by ECC International (St. Austell,
UK); particle size 0.5 to 5 mm; (2) marble-derived calcite, supplied by
English China Clay International (St. Austell, UK); milled particle size
0.5 to 10 mm; (3) quartz, supplied by Hanson PLC (Maidenhead, UK);
milled particle size 10 to 30 mm; and (4) Ca-montmorillonite, a 2:1 layer
clay, supplied by Rockwood Additives Ltd. (Widnes, UK); particle size
,0.5 mm.
All of the experiments were conducted using artificial seawater (ASW)
prepared from Instant OceanH sea salts and deionized water (mixed to a
salinity of 1.022–1.024 and with a pH of 8.4). The ASW was inoculated
with bacteria by introducing a population of 11 live mussels (Mytilus
edulis) to the aerated reservoir 2 weeks prior to use.
Published Online: June 2014
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L.A. WILSON AND N.J. BUTTERFIELD
All of the experimental subjects were alive and in good condition at the
start of the experiments. Crangon specimens (body length 50–70 mm,
supplied by Millport Marine Station, western Scotland) were killed by
subaerial exposure ca. 2 hours prior to burial. For Nereis (body length
125–250 mm, supplied by Seabait Ltd., Northumberland, UK), one series
of specimens was killed by immersion in freshwater (with a potential for
associated osmotic cell rupture) and a second by exposing their heads to a
stream of hot water (see Briggs and Kear [1993]).
For each of the taxon–sediment combinations, three to four freshly
killed specimens were buried horizontally within 4 cm of ASW-saturated
sediment and flooded with an overlying layer of ASW (Supplementary
Material, Fig. S1); individual plastic containers were closed with rubbersealed lids for the duration of the experiments, substantially restricting
oxygen availability. A sediment-free control for each taxon was also run.
Where possible, the pH, oxygen concentration, and major ion concentrations of both the ASW and sediment were measured at the beginning
and end of the experiments (Cranwell CR-95 digital pH meter, Jenway
model 970 digital DO2 meter, Varian Vista Axial Inductively Coupled
Plasma–Optical Emission Spectrophotometer).
After 4 months (17 weeks) the containers were opened (Supplementary
Material, Figs. S2, S3), the overlying ASW was siphoned off, and the
sediments were dried by continuous airflow in a laboratory fume
cupboard. The carcasses were then exposed by scraping away the
overlying sediments. Following qualitative assessment of the remains
(Supplementary Material, Table S1), the carbonaceous residues were
carefully collected and cleaned of adhering sediment via a sequence of
rinsing (on a 63-mm sieve with distilled water), ultrasonication (30 seconds
in distilled water), and rotary tumbling (24 hours in distilled water +
Calgon defloculant). This procedure also served as a general measure of
cuticle integrity. Where morphologically intact structures remained at the
end of this process (i.e., Nereis in kaolinite), these were further prepared
for scanning electron microscopy (SEM) and histological sectioning.
The cleaned organic residues were dried, powdered, and chemically
analyzed for (1) non–water-soluble protein, (2) chitin, (3) water-soluble
protein, (4) carbohydrate, and (5) phospholipid, using the various
hydrolysis and colorimetric techniques employed by Briggs and Kear
(1993). As a result of the obscuring effects of the sediment it was not
possible to document absolute amounts, so these data have been recorded
as percentages. For Nereis the chemical analyses were based on a 15segment section of the trunk under the assumption that this would be
broadly representative of the whole organism; whereas the accumulated
residue of an entire carcass was used for more anatomically differentiated
Crangon. Multiple specimens were amalgamated for the two sedimentfree controls. Where possible, duplicate chemical analyses were carried
out and the results averaged.
Chitin and sclerotized (nonsoluble) protein were measured following
the method of Hunt and Nixon (1981) as adapted by Briggs and Kear
(1993). Residual weights following alkali hydrolysis (5% KOH) to remove
protein, and acid hydrolysis (6 N HCl) to remove chitin, provide a useful
measure of the amount of protein and chitin originally present. Sample
sizes were typically in the range of 0.2 to 33 mg.
Water-soluble protein was measured using the Bradford (1976)
method, a colorimetric technique using Coomassie Brilliant Blue G-250
as a dye reagent, with an accuracy of 5 mg protein/ml of final assay
volume. Between 100 and 180 mg of each sample was dissolved in 1 ml
buffer solution (Tris) and 0.25 ml of 1 M NaOH, along with 5 ml of the
protein reagent. Absorbance was measured at 595 nm (Unicam 989 Solar
Mark 2 spectrophotometer). Blanks and a set of standards of varying
protein amounts (from 5 to 200 mg) were included for calibration.
Carbohydrate content was analyzed using the colorimetric method of
DuBois et al. (1956). Thirty to 50 mg of sample suspended in 0.5 ml of
water was mixed with 0.5 ml of 5% phenol in 0.1 M HCl and 2.5 ml of
concentrated sulfuric acid. Absorbance was measured at 490 nm (Unicam
989 Solar Mark 2 spectrophotometer). Blanks and a set of standards of
varying carbohydrate amounts (from 5 to 50 mg) were included for
spectrophotometer calibration.
Phospholipid analysis was adapted from Petersen et al. (1991). By
releasing lipid-bound phosphate using dichloromethane-methanol extraction, the quantity of phosphate can be measured colorimetrically using
malachite green as the reagent (absorbance measured at 610 nm; Unicam
989 Solar Mark 2 spectrophotometer). Blanks and a set of standards of
varying phosphate amounts (from 0.25 to 4 mg) were included for
spectrophotometer calibration.
RESULTS
Sediment mineralogy had a pronounced effect on the preservation of
primary anatomical features in both Nereis and Crangon, but with marked
taxonomic differences. In Nereis (Figs. 1, 2), both the sediment-free control
and the montmorillonite treatment yielded only chaetae and jaws (Stage 5;
Supplementary Material, Table S1), whereas the calcite-hosted and quartzhosted specimens also preserved thinly coherent remains of the original
integument (Stages 4 and 4/3, respectively). By far the most substantial
effect, however, was with the kaolinite-hosted worms, where flattened but
otherwise complete integuments were recovered, including well-preserved
segmentation, parapodia, palps, tentacular cirri, and, in one instance, the
gut (Stage 2). These kaolinite-hosted remains were sufficiently robust to
allow the extraction of entire worm cuticles, and for dissected portions to
withstand both extended tumbling and preparation for stained sections and
SEM (Figs. 1A9, 2). In carbonate- and montmorillonite-hosted Nereis
there was a conspicuous development of carcass-associated carbonate
mineralization which was not observed in kaolinite or quartz. Montmorillonite-hosted specimens typically failed to collapse in concert with the
decay of soft tissues, resulting in a three-dimensional void.
For Crangon (Fig. 3), none of the sediment types substantially enhanced
anatomical preservation relative to the ASW control, although it is notable
that the control itself preserved a significant degree of articulated cuticle
(Stage 3, Supplementary Material, Table S1). As with Nereis, it was the
kaolinite system that preserved the greatest level of anatomical detail (Stage
3), whereas calcite and quartz appear to have accelerated decay (Stage 4).
In montmorillonite, Crangon typically occurred as thin cuticular films
adhering to uncollapsed sedimentary matrix, along with significant
accumulations of a pinkish-white mineral within the body cavity—
probably calcium phosphate (cf. Briggs and Kear 1994a). Although
equivalent to Stage 3 or better in some respects (e.g., the robustly preserved
tail fan), the overall quality of Crangon preservation in montmorillonite
was substantially lower than its counterparts in kaolinite, calcite, and
ASW. Crangon in quartz also resulted in a three-dimensional void, but this
was not accompanied by the pronounced mineralization associated with
montmorillonite. None of the Crangon treatments yielded coherent cuticle
following the cleaning/tumbling procedure.
The distinctive morphological expression of the variously treated
carcasses was reflected in their residual chemical composition (Fig. 4). In
both taxa, for example, it was the kaolinite system that preserved the
highest percentage of protein—though once again there was no
measurable difference between Crangon in kaolinite and its ASW control.
Indeed, the protein:chitin:carbohydrate ratios of Crangon were not
substantially altered in any of the sediment treatments, apart from
modest increases in the chitin content (at the expense of protein) in
quartz, montmorillonite, and calcite.
By contrast, sediment mineralogy had a profound effect on the
chemical composition of the Nereis residues (Fig. 4). In kaolinite the
percentage of preserved protein was twice that of the ASW control
(including a significant occurrence of otherwise-unpreserved water-soluble
protein) whereas in quartz and montmorillonite it was less than half. The
balance was met almost exclusively by chitin, with kaolinite-hosted
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FIG. 1.—Exhumed Nereis remains after 17 weeks in A) kaolinite, B) calcite, C) quartz, and D) montmorillonite. A9–D9 are the corresponding isolated remains
following a screen rinse, ultrasonic bath, and 24 hours of aqueous tumbling. Scale bar in D equals 5 mm for A–C, 3 mm for D, and 15 mm for A9–D9.
specimens represented by ,12% chitin, compared to ,75% for those in
quartz and montmorillonite. The Nereis-quartz and Crangon-kaolinite
experiments also preserved a small amount of phospholipid.
The differing treatments also had idiosyncratic effects on whole-system
chemistry (Tables 1, 2). Most conspicuously, the addition of kaolinite
induced a significant drop in pH relative to all other treatments, though
only in Nereis was this maintained to the end of the 4-month experiment.
As expected, the oxygen content of the sediments and overlying ASW
declined in all of the decay experiments; however, the residual oxygen
levels were substantially lower in quartz and montmorillonite than in
kaolinite or carbonate. Oxygen drawdown in kaolinite- and carbonatehosted Crangon was less than half of that in corresponding treatments of
Nereis (possibly a function of differing carcass:sediment ratios, which
were not quantitatively monitored), but within the Nereis experiments the
least drawdown occurred in kaolinite.
In terms of major ion chemistry (of the overlying ASW), there was little
systematic change in the concentrations of Cl, Na, Mg, or K over the
course of the experiments, apart from marked loss of Mg in the two
carbonate treatments (Table 2). By contrast, Ca concentrations declined
significantly in sediment-free and carbonate-hosted Nereis, while increasing
for the equivalent conditions with Crangon—and increasing regardless of
carcass identity in kaolinite. Sulfur concentrations declined substantially in
the carbonate and quartz treatments of both taxa but rose in the two
kaolinite experiments. Results for montmorillonite were not available
because of its complete absorption of the overlying ASW during the course
of the experiments (see Supplementary Material, Fig. S3).
Despite the localized species effects, the different sediments exhibited
broadly characteristic responses to carcass degradation. In quartz, for
example, both Nereis and Crangon produced a permeating black exudate
that gradually dissipated over the course of the experiment (Supplementary Material, Figs. S2–S4), whereas localized ‘‘black stains’’ developed in
the vicinity of montmorillonite-hosted carcasses (more conspicuously in
Nereis than in Crangon; Supplementary Material, Fig. S3). In calcite, all
of the associated sediments turned pale gray within the first few weeks
(more conspicuously in Nereis than in Crangon), but eventually returned
to their original white color (by week 13 for Nereis and by week 17 for
Crangon). Neither of the kaolinite treatments exhibited any color
changes, though both developed thick floating fungal colonies by the
end of the experiment (Supplementary Material, Fig. S3). Nonfungal
biofilms formed in both of the quartz treatments and the ASW controls
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FIG. 2.—Exhumed Crangon remains after 17 weeks in A) kaolinite, B) calcite, C) quartz, and D) montmorillonite. A9–D9 are the corresponding isolated remains
following a screen rinse, ultrasonic bath, and 24 hours of aqueous tumbling. Scale bar in A equals 5 mm for A–D and 8 mm for A9–D9.
(more conspicuously in Nereis than in Crangon); there was no obvious
microbial growth in the montmorillonite or calcite treatments (Supplementary Material, Fig. S3).
DISCUSSION
The incorporation of sediment into laboratory decay experiments sheds
fundamental new light onto taphonomic pathways, if only because all
fossils form within some sort of sedimentary matrix. At the same time,
however, this actualistic approach adds significant new levels of
diagenetic and logistic complexity, not least of which involves the
challenge of recovering quantitative data from sediment-bound residues
while also monitoring the qualitative effects of sediment on carcass
morphology (cf. Plotnick 1986; Allison 1988; Martin et al. 2004; Darroch
et al. 2012). The compounding diagenetic feedbacks between carcasses
and sedimentary matrix also make it difficult to resolve underlying
mechanisms, though our experimental results introduce some intriguing
possibilities.
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FIG. 3.—Nereis remains after 17 weeks in
kaolinite. A) Whole specimen showing details of
segmentation, parapodia, palps, and tentacular
cirri; B) stained sectioned cuticle wall showing
preservation of three distinct integumentary
layers and preferential loss of (nonstructural)
internal organs; C) SEM of parapodia with
associated chaetae. Scale bar in C equals 2 mm
for A, 35 mm for B, and 0.5 mm for C.
Sediment Effects on the Preservation of Carbonaceous Fossils
These experiments demonstrate that sediment mineralogy can have
profound effects—both positive and negative—on the morphological
preservation of interred carcasses. Such taphonomic realignment is hardly
surprising given the well-documented influence of mineralogy on the
preservation of sedimentary organic carbon in general (Theng 1979;
Ransom et al. 1998; Lützow et al. 2006; Ziervogel et al. 2007; Wu et al.
2012) and, indeed, the preferential occurrence of carbonaceous compression fossils and microfossils in siliciclastic (vs. carbonate-rich) mudstones.
Curiously, however, it was the kaolinite system that induced the most
pronounced positive effects on carcass preservation, despite the modest
physicochemical properties of this 1:1 layer clay. By contrast, montmorillonite—an expanding 2:1 layer clay with exceptionally high surface area,
cation exchange capacity, and potential to suppress enzymatic activity
(Theng 1979; Butterfield 1990, 1995)—conspicuously accelerated decay.
In addition to sediment mineralogy, it is clear that the chemistry and
histology of the interred carcasses also influence taphonomic trajectories.
In the present experiments, for example, the most pronounced effects of
sediment on preservation potential (both positive and negative) were
associated with relatively labile collagen-based polychaete cuticle,
whereas the more recalcitrant chitin-based arthropod cuticle exhibited
only modest differences relative to the sediment-free control. Such
behavior is broadly analogous to the enhanced susceptibility of
exceptionally labile (i.e., chemically reactive) tissues to early diagenetic
mineralization (Butterfield 2002, 2003). Insofar as Nereis cuticle in
kaolinite ended up more robustly preserved than Crangon cuticle under
any of the experimental conditions, its recalcitrance was clearly acquired
secondarily, a product of early diagenetic interaction with its sedimentary
matrix.
Sediment-induced changes in morphological preservation potential also
correlate with the chemistry of fossil residues, though not necessarily in a
straightforward fashion. For Nereis in kaolinite and montmorillonite, the
quality of cuticle preservation varied directly with the percentage of
preserved protein, suggesting a novel possibility for the formation of
carbonaceous compression fossils: rather than structural polysaccharides
such as chitin and cellulose, the key ingredients might well be
proteinaceous. Even so, Nereis cuticle was also relatively well preserved
in quartz, which exhibited the lowest overall levels of protein and the
highest levels of chitin.
Taphonomic Pathways
At a minimum, the extended preservation of carbonaceous substrates
requires the suppression of aerobic heterotrophs, typically through the
removal or exclusion of free oxygen. The marked drawdown of oxygen in
all of the experiments (Table 1) can be ascribed to the early aerobic decay
of the carcasses and is presumably a primer for subsequent carbonaceous
preservation. Even so, the substantially lower levels of oxygen in the
montmorillonite and quartz treatments demonstrate that morphological
preservation is not solely a function of limited oxygen. Indeed, the degree
of oxygen drawdown—along with the production of significant black
exudates (Supplementary Material, Figs. S2–S4)—may simply reflect the
extent of initial carcass decay. For Nereis in kaolinite and Crangon in
both kaolinite and calcite, the relatively high concentrations of residual
oxygen (at or above the 18% level at which decomposition begins to be
oxygen-limited; see Briggs and Kear [1993]) point to preservational
mechanisms other than anoxia—possibly even a requirement for
molecular oxygen (see below).
The lack of correspondence between grain size and morphological
preservation suggests that sediment permeability was not a primary factor
in the preservation of carbonaceous films. Whereas the demonstrably
permeable quartz and calcite systems (evinced by uniform changes in
sediment color) yielded significant organic residues, the much finergrained, relatively impermeable montmorillonite treatments (with localized black stains; Supplementary Material, Fig. S3) exhibited the poorest
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FIG. 4.—Chemical composition of Nereis and Crangon remains after 4 months
of burial in differing sediment mineralogies and the control. ASW 5 artificial
seawater; Kao 5 kaolinite; Calc 5 calcite; Qtz 5 quartz; and Mont
5 montmorillonite.
overall quality of preserved cuticle. These closed conditions, however,
corresponded conspicuously with mineral precipitation, especially within
the body cavity of Crangon (Fig. 2D), suggesting that sediment sealing
may be essential for fossilization via early diagenetic mineralization (cf.
Briggs and Kear 1994a; Gaines et al. 2012).
Given the marked effect of sediment mineralogy on carbonaceous
preservation, there is a case to be made for differential adsorption of
degradative enzymes on mineral surfaces (Butterfield 1990, 1995). As
originally formulated, this enzyme suppression model focused on the high
specific surface areas and high cation exchange capacity of expanding
clays such as montmorillonite. These properties clearly failed to enhance
preservation in the current experiments, in which the greatest (positive)
response was associated with the relatively low surface area and cation
exchange capacity of kaolinite. It is possible, however, that enzyme
adsorption on montmorillonite accounts for at least some of the observed
pattern, acting not so much to suppress the activity of degradative
exoenzymes as to stabilize them, thereby extending their effective
lifespans (Ziervogel et al. 2007). Such preservational effects conceivably
account for the accelerated decay of sediment-associated carcasses
documented by Plotnick (1986); Allison (1988); and Briggs and Kear
(1993).
The particular mechanisms by which sediments enhance the preservation of labile organic compounds remain poorly understood, but
substrate protection/stabilization—as opposed to enzyme suppression—
appears to be the primary control in both soils (Lützow et al. 2006;
Mikutta et al. 2006) and marine sediments (Ransom et al. 1998;
Satterberg et al. 2003; Arnarson and Keil 2005; Ziervogel et al. 2007).
Sediment mineralogy is recognized as a key factor in such stabilization,
but so too is the chemical structure of the substrate, pH, the isoelectric
points of the sediment and substrate, availability of floc-inducing
multivalent cations, and organic loading. Aluminum and iron oxides
have a particularly high capacity for preserving organic carbon, as do
allophane-rich volcanic soils. At least some kaolinitic soils have greater
capacity for stabilizing organic matter than do montmorillonite soils,
possibly as a result of enhanced ligand adsorption on the broken edge
surfaces of kaolinite at low pH (Bruun et al. 2010).
One of the problems in adapting models of organic preservation from
soil science and organic geochemistry to paleontology is that they do not
obviously address the issue of morphological preservation; i.e., stabilization of carbonaceous substrates at a sufficiently early stage to capture
anatomical form. Especially for macroscopic compression fossils, the
processes responsible for preserving morphological organic carbon are
unlikely to be the same as those acting on total organic carbon (TOC). In
the present experiments, for example, there is no particular reason to
assume that the montmorillonite treatments preserved less TOC than did
kaolinite—only that macromolecular structures were more readily broken
down into smaller migration-prone compounds (with a corresponding
loss of morphology but enhanced likelihood of mineral adsorption and
amorphous recondensation [Lützow et al. 2006; Wu et al. 2012]). The lack
TABLE 1.—pH and oxygen concentration of the sediment and overlying artificial seawater (ASW) at the end of the taphonomic experiments (initial values
in parentheses). Note the low pH values associated with kaolinite (*) and Nereis (**). No final values are available for montmorillonite as a result of its
complete absorption of the ASW.
N-ASW
N-Kao
N-Calc
N-Qtz
N-Mont
C-ASW
C-Kao
C-Calc
C-Qtz
C-Mont
pH–Sediment
pH–ASW
O2%–Sediment
O2%–ASW
NA
4.77** (4.71*)
7.31 (7.48)
7.80 (7.06)
6.24 (8.92)
NA
7.34 (3.78*)
7.31 (7.48)
8.17 (6.95)
6.22 (8.44)
8.6 (8.4)
5.1** (8.4)
7.2 (8.4)
7.8 (8.4)
NA (8.4)
6.7 (8.4)
7.2 (8.4)
7.3 (8.4)
8.3 (8.4)
NA (8.4)
NA
17 (47)
10 (53)
4 (39)
8 (65)
NA
29 (48)
30 (53)
11 (36)
7 (42)
41 (75)
28 (75)
28 (75)
10 (75)
NA (75)
48 (75)
22 (75)
54 (75)
53 (75)
NA (75)
N 5 Nereis; C 5 Crangon; Kao 5 kaolinite; Calc 5 calcite; Qtz 5 quartz; Mont 5 montmorillonite; NA 5 not available.
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TABLE 2.—Major ion concentration (in ppm) of the overlying artificial seawater (ASW) at the beginning and end of the taphonomic experiments. Note the
contrasting effects of carcass type on Ca (in ASW [*] and calcite [**]) and the generally elevated S in kaolinite [***]. No final values are available for
montmorillonite as a result of its complete absorption of the ASW.
Initial ASW
N-ASW
N-Kao
N-Calc
N-Qtz
N-Mont
C-ASW
C-Kao
C-Calc
C-Qtz
C-Mont
Cl
Na
Mg
K
Ca
S
14,137
14,949
13,066
15,758
14,275
NA
11,924
12,765
12,767
15,106
NA
8769
8020
8294
8425
7821
NA
8313
8437
8636
8112
NA
1053
927
977
484
861
NA
999
894
616
840
NA
329
362
384
410
353
NA
335
341
355
349
NA
296
51*
394
76**
153
NA
415*
548
1113**
176
NA
242
234
291***
98
52
NA
234
290***
150
145
NA
N 5 Nereis; C 5 Crangon; Kao 5 kaolinite; Calc 5 calcite; Qtz 5 quartz; Mont 5 montmorillonite; NA 5 not available.
of color change in the kaolinite systems suggests that significantly less
structural material was degraded and dispersed at the outset.
The circumstances leading to the exceptional preservation of Nereis in
kaolinite (Figs. 1, 2) clearly interfered with normal decay processes at a
very early stage, but the phenomenon cannot be explained simply in terms
of reduced rates or temporary suspension. Despite the morphological
fidelity, the exhumed remains are constitutionally and chemically distinct
from the original carcasses; only cuticular structures remain, and these
exhibit none of their original susceptibility to decomposition in water
(Fig. 1A9). Partial decay will, of course, change the chemistry of any
substrate, and Gupta et al. (2009) have demonstrated that lipids can
contribute to the polymerization of decaying tissues within weeks of
death. Such alteration, however, rarely leads to the morphological
preservation of carbonaceous substrates, at least in the absence of an
external fixing agent.
Taphonomic Tanning—A Hypothesis
One of the most common means of enhancing the recalcitrance of
organic substrates is through tanning, a process involving the secondary
cross-linking of structural biomolecules. Tanning occurs biologically,
where it determines the primary recalcitrance of particular substrates such
as polychaete chaetae, arthropod cuticle, and hard keratin in vertebrates,
but it can also be induced abiologically via external tanning agents. In the
leather industry, collagen-based hides are tanned using mineral salts (e.g.,
chromium sulfate, aluminum sulfate) or polyphenolic vegetable tannins,
though there is a range of alternative tanning agents, including
multivalent Fe, Zr, Ti, and Si, polyphosphates, and various aluminosilicate minerals (Kanagy and Kronstadt 1943; Covington 1997; Hueffer
et al. 2010); in at least one patented process, the agent is derived from
kaolinite (Plapper et al. 1981). Under particular circumstances, postmortem tanning can also take place naturally. In the case of recent tanned
cadavers, for example, the exceptional preservation of external morphology appears to be related to salty, marine-influenced groundwater and
conspicuously sticky soil (Ruwanpura and Warushahennadi 2009). By
contrast, the tanning agent responsible for the selective preservation of
skin and keratin in medieval peat bogs has been identified as a carbonylrich polysaccharide (sphagnan), facilitated by a suppression of exoenzymes at moderately low pH (Painter 1991).
Reduced pH also appears to have been a significant factor in the
postmortem stabilization of Nereis cuticle in kaolinite (Table 1), likely
induced by the high proportion of reactive crystal edges and low cation
exchange capacity of the clay component (Tombácz and Szekeres 2006),
but also by the effects of incorporated organic acids and CO2 (e.g.,
Hutcheon et al. 1993). It is possible that the preservation effects were due
entirely to such pickling, though this fails to explain the histological
selectivity, focused exclusively on structural cuticle (cf. Painter 1991).
Moreover, the 4.7 to 5.1 pH of the Nereis-kaolinite system is well above
levels that interfere with anaerobic fermentation or bacterial sulfate
reduction (Painter 1991; Fauville et al. 2004). The preferential and
exceptional preservation of collagenous cuticle in kaolinite suggests a
significant level of secondary, diagenetically induced tanning (alongside
the biologically tanned chaetae and jaws).
In industrial tanning, an initial pickling phase is necessary to reduce the
rate of collagen cross-linking and to enhance the penetration of tanning
agent, while background ionic concentrations (salts) limit osmotic
swelling and deformation; controlling the balance between substrate
reactivity, penetrability, and (morphological) integrity is key to the
tanner’s art (Covington 1997). The same situation is likely to hold for
taphonomic tanning, in which the interplay of degrading carcasses and
sedimentary matrix determines the progress of secondary cross-linking
and, ultimately, the quality of a potential carbonaceous compression
fossil. In the case of the Nereis-kaolinite experiment, we suggest that the
enhanced preservation was controlled by the presence of a sedimentderived (presumably Al-based) tanning agent combined with a particularly favorable compliment of ion concentrations and pH trajectory (cf.
Naimark et al. 2013). The proclivity of organic material to concentrate
environmental Al under acidic conditions (Mulholland et al. 1987) may
have been a significant factor in this process.
Kaolinite-based tanning clearly cannot account for all instances of
enhanced preservation, since Nereis carcasses in both quartz and
carbonate also survived substantially better than does the sediment-free
control. Nor is tanning necessarily the only contributing process: given
the relatively elevated S and O2 concentrations associated with the
kaolinite experiments (Tables 1, 2), it is possible that disulfide bonding
(via the oxidation of sulfhydryl groups) might also have contributed to
the stabilization of morphology-defining proteins (cf. Visschers and de
Jongh 2005). If so, then localized availability of free oxygen might be a
critical factor in fossil preservation, just as it is for the (primary) crosslinking of hard keratins (Greenberg and Fudge 2013).
Implications for BST Preservation
Burgess Shale–type preservation is a loosely defined taphonomic mode
characterized by the exceptional preservation of carbonaceous compression fossils in marine shales (Butterfield 1995; Gaines et al. 2008). Much
of the BST fossil record derives from biologically tanned structures such
as arthropod cuticle and polychaete chaetae, which tend to be sharply, if
not always robustly, preserved. Not surprisingly, the situation with
biologically untanned integument is much more variable. Polychaete
152
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L.A. WILSON AND N.J. BUTTERFIELD
cuticle in the Burgess Shale, for example, sometimes exhibits exquisite
levels of anatomical detail but is usually less precisely preserved (Conway
Morris 1979), typically appearing more like Nereis in quartz (Fig. 1C)
than like Nereis in kaolinite (Fig. 1A); in many Burgess Shale specimens
segmentation is only recognizable through the preservation of segmentally disposed chaetae. Such variability points to complex diagenetically
and phylogenetically sensitive taphonomic pathways, consistent with a
diagenetic tanning mechanism.
The potential for secondarily tanned structures to taphonomically
outperform inherently more recalcitrant structures is demonstrated in
BST biotas by the common preservation of carbonaceous gut structures
(Wilson 2006); indeed, it is the exceptionally thin (i.e., more tenuously
preserved) nature of most arthropod cuticle (Orr et al. 2009) that reveals
this internal anatomy. By contrast, secondarily tanned structures tend to
be much more uniformly expressed and can be exceptionally thick and/or
reflective, as in the case of Eldonia guts (Butterfield 1996). A similar,
highly reflective style of carbonaceous preservation occurs in the stemgroup chordate Pikaia (Butterfield 1990, 2003; Briggs and Kear 1994b;
Conway Morris and Caron 2012), which might also be ascribed to the
taphonomic tanning of a collagen-based integument.
The recognition of secondary, diagenetically induced shifts in
preservation potential also has important implications for interpreting
the histological and phylogenetic affiliations of problematic BST fossils
(Butterfield 2003). By selectively enhancing the preservation potential of
more labile substrates, early diagenetic tanning—like early diagenetic
mineralization—undermines assumptions of tapho-anatonomic ordering
based on sediment-free degradation experiments (e.g., Allison 1988;
Briggs and Kear 1993, 1994a; Sansom et al. 2010). At the other end of
the scale, sediment mineralogy has the potential to accelerate the
degradation of inherently more recalcitrant substrates; e.g., Crangon in
montmorillonite, but also notable in soils, where lignin commonly
degrades more rapidly than sediment-stabilized polysaccharides and
proteins (Lützow et al. 2006; Mikutta et al. 2006; Schmidt et al. 2011).
Unfortunately, the complex interplay of original histology and early
diagenesis precludes most broad-scale generalizations.
Despite the idiosyncratic nature of exceptional preservation, the
distinctive expression of BST biotas and corresponding small carbonaceous fossils through the Cambrian and Early Ordovician suggests a
broadly comparable diagenetic context (Butterfield 1995, 2003; Van Roy
et al. 2010; Butterfield and Harvey 2012). In light of the present
experiments, secular changes in the average clay mineralogy and ocean
chemistry are likely to have been significant factors in the opening and
closing of this taphonomic window. Intriguingly, oceanic pH is estimated
to have been at its Phanerozoic minimum during the early Paleozoic
(Arvidson et al. 2013), coincident with the interval of enhanced BST
preservation. Elevated kaolinite input may well have played a role but is
difficult to demonstrate in particular BST settings because of instances
due to secondary alteration of original clay minerals (cf. Powell 2003;
Forchielli et al. 2013).
At a broader scale, there is a conspicuous correlation between BST
preservation and a Cambro–Ordovician spike in the occurrence of
anomalously shallow-water glauconite (see Brasier 1980; Chafetz and
Reid 2000; Nielsen and Schovsbo 2011; Peters and Gaines 2012). As a
class, glauconite–Fe-illite–Fe-smectite represents a broad continuum of
iron-rich, redox-sensitive clay minerals that form during marine
diagenesis (Meunier and El Albani 2007). Iron-rich clays have previously
been invoked to explain BST preservation through the adsorption and
deactivation of degradative enzymes (Butterfield 1995) but might
alternatively be viewed as evidence of enhanced marine Fe2+ availability,
leading to the secondary stabilization of otherwise-labile substrates (cf.
Petrovitch 2001). This latter process might reasonably be described as
iron-based tanning (cf. Kanagy and Kronstadt 1943).
As a product of early diagenesis, glauconite does not represent the
original mineralogy of incoming aluminosilicates and may not itself be
the cause of early Paleozoic shifts in preservation potential. Many
Cretaceous greensands, for example, appear to be derived from volcanic
sources (Jeans et al. 1982), and it is clear that glauconite forms from a
wide range of precursor minerals, including kaolinite (Meunier and El
Albani 2007). Evidence of intense, large-scale continental weathering
through the Cambro–Ordovician interval (Avigad et al. 2005; Peters and
Gaines 2012) implies significant inputs of Al-rich clays to the global
oceans at this time, potentially contributing to both the spike in both
shallow-water glauconite and BST preservation.
CONCLUSION
Entry into the body fossil record requires that carcasses, or components
of carcasses, survive their individual taphonomic thresholds. For Nereistype polychaete cuticle this means disrupting the normal course of
decomposition within the first 2 to 4 weeks, and for Crangon-type
arthropod cuticle, it means disrupting the course within 25+ weeks
(Allison 1988; Briggs and Kear 1993, 1994a). Our experimental results
indicate that this can be readily achieved with burial in sediments of
particular mineralogies—provided the accompanying histologies and
pore-water chemistries are all suitably aligned. The sensitivity of such
systems to local circumstance suggests that exceptional BST preservation
is likely to be the exception, even where conditions are generally favorable
(such as in the low-pH, glauconite-prone oceans of the early Paleozoic)—
hence, the vast volumes of unoxidized marine mudstones lacking any hint
of BST fossils. Conversely, the identification of first-order effects of
sediment mineralogy on the preservation potential of carbonaceous
substrates offers an explanatory mechanism for fossilization, even under
seemingly suboptimal conditions, such as the surprisingly common
occurrence of well-defined leaf compression–impression fossils in
coarse-grained sandstones (see Krishtofovich [1944]).
The other critical factor is the carcasses themselves. Some tissues are
inherently more recalcitrant than others, but their potential for
fossilization depends on the interplay of particular organic substrates
and their early diagenetic conditions. Despite the conventional focus on
biologically tanned chitinous cuticle, exceptional BST preservation may
owe more to the secondary tanability of more labile substrates,
particularly proteins. Given the marked sensitivity of this phenomenon
to local circumstance, perhaps the most remarkable aspect of BST
preservation is its capacity to capture such a range of histological and
phylogenetic diversity in localized Lagerstatten.
ACKNOWLEDGMENTS
We thank Gillian Forman for her enormous assistance with the laboratory
work. LAW was supported by a NERC (Natural Environment Research
Council, UK) PhD studentship.
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SUPPLEMENTARY MATERIAL
Supplemental material is available from the PALAIOS data archive:
http://palaios.ku.edu/data.html.