sediment effects on the preservation of burgess … · the complex interplay of original histology...

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. BUTTERFIELDDepartment 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, andmontmorillonite 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 positiveeffect was with Nereis buried in kaolinite, and the greatest negative effect was with Nereis buried in montmorillonite, amorphological 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 ionconcentrations, all of which are likely to feed back on the preservation potential of particular substrates in particularenvironments. The particular susceptibility of Nereis to both diagenetically enhanced preservation and diagenetically enhanceddecomposition most likely derives from the relative lability of its collagenous cuticle vs. the inherently more recalcitrant cuticleof Crangon. We propose a mechanism of secondary, sediment-induced taphonomic tanning to account for instances of enhancedpreservation. In light of the marked effects of sediment mineralogy on fossilization, the Cambrian to Early Ordoviciantaphonomic window for BST preservation is potentially related to a coincident interval of glauconite-prone seas.

INTRODUCTION

Carbonaceous compression fossils are a major source of paleobiolog-ical data, in particular as it relates to capturing the early Paleozoic recordof ‘‘exceptional’’ Burgess Shale–type (BST) macrofossils (Butterfield1990, 1995; Gaines et al. 2008; Page et al. 2008; Orr et al. 2009) and theirmicroscopic counterparts (Butterfield and Harvey 2012). Even so, thecircumstances and processes leading to the preservation of such fossils—and thereby their paleobiological implications—have yet to be fullyresolved. The Phanerozoic record of BST-type preservation, for example,appears to be limited to an early (but not earliest) Cambrian to EarlyOrdovician taphonomic window (Butterfield 1995; Van Roy et al. 2010),obscuring its contribution to both the Cambrian and Ordovicianradiations. Localized dysoxia–anoxia is certainly a prerequisite forpreserving nonbiomineralizing fossils, but this falls well short of a fullexplanatory account. Even in the absence of oxygen, simple hydrolysis,autolysis, and the activities of anaerobic microbes continue to degradecarbonaceous substrates, rapidly obliterating original morphology.

Sedimentary matrix is fundamental to the fossilization process, notonly as basic packing material but also based on its potential to alter thechemistry of early diagenesis. Despite reports of accelerated carcass decayassociated with some sediments (e.g., Plotnick 1986; Allison 1988; Briggsand Kear 1993), most models for BST preservation invoke mineral-specific diagenesis as an essential factor, either by suppressing normalenzyme–microbial-based decay processes (e.g., Butterfield 1990, 1995;Gaines et al. 2005, 2012) or secondarily by enhancing the recalcitrance ofrelatively 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 willadhere to lobster eggs in the presence of bacteria, and Naimark et al.(2013) have documented substantially enhanced preservation of Artemiawhen they are buried in kaolinite. In this study we adapt the seminal,

sediment-free decay experiments of Briggs and Kear (1993, 1994a) toinvestigate the effect of sediment mineralogy on the decay and earlydiagenesis of two ‘‘model’’ nonbiomineralizing marine invertebrates:Nereis virens (polychaete annelids with collagenous cuticle, sclerotizedcollagenous 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 preservationpotential, we buried freshly killed Nereis and Crangon in four differentseawater-saturated sediments: kaolinite, quartz, calcite, and Ca-mont-morillonite. After 4 months the carcasses were exhumed for qualitativemorphological assessment and semiquantitative chemical analysis(structural protein, chitin, water-soluble protein, carbohydrate, andphospholipid).

All of the sediments used in the experiments were mineralogically pureand texturally homogeneous, though the particle size (measured using aMicromeritics 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 byEnglish China Clay International (St. Austell, UK); milled particle size0.5 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 layerclay, 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 asalinity of 1.022–1.024 and with a pH of 8.4). The ASW was inoculatedwith bacteria by introducing a population of 11 live mussels (Mytilusedulis) to the aerated reservoir 2 weeks prior to use.

Published Online: June 2014

Copyright E 2014, SEPM (Society for Sedimentary Geology) 0883-1351/14/029-145/$03.00

All of the experimental subjects were alive and in good condition at thestart of the experiments. Crangon specimens (body length 50–70 mm,supplied by Millport Marine Station, western Scotland) were killed bysubaerial exposure ca. 2 hours prior to burial. For Nereis (body length125–250 mm, supplied by Seabait Ltd., Northumberland, UK), one seriesof specimens was killed by immersion in freshwater (with a potential forassociated osmotic cell rupture) and a second by exposing their heads to astream of hot water (see Briggs and Kear [1993]).

For each of the taxon–sediment combinations, three to four freshlykilled specimens were buried horizontally within 4 cm of ASW-saturatedsediment and flooded with an overlying layer of ASW (SupplementaryMaterial, Fig. S1); individual plastic containers were closed with rubber-sealed lids for the duration of the experiments, substantially restrictingoxygen availability. A sediment-free control for each taxon was also run.Where possible, the pH, oxygen concentration, and major ion concen-trations of both the ASW and sediment were measured at the beginningand end of the experiments (Cranwell CR-95 digital pH meter, Jenwaymodel 970 digital DO2 meter, Varian Vista Axial Inductively CoupledPlasma–Optical Emission Spectrophotometer).

After 4 months (17 weeks) the containers were opened (SupplementaryMaterial, Figs. S2, S3), the overlying ASW was siphoned off, and thesediments were dried by continuous airflow in a laboratory fumecupboard. The carcasses were then exposed by scraping away theoverlying sediments. Following qualitative assessment of the remains(Supplementary Material, Table S1), the carbonaceous residues werecarefully collected and cleaned of adhering sediment via a sequence ofrinsing (on a 63-mm sieve with distilled water), ultrasonication (30 secondsin distilled water), and rotary tumbling (24 hours in distilled water +Calgon defloculant). This procedure also served as a general measure ofcuticle integrity. Where morphologically intact structures remained at theend of this process (i.e., Nereis in kaolinite), these were further preparedfor scanning electron microscopy (SEM) and histological sectioning.

The cleaned organic residues were dried, powdered, and chemicallyanalyzed for (1) non–water-soluble protein, (2) chitin, (3) water-solubleprotein, (4) carbohydrate, and (5) phospholipid, using the varioushydrolysis and colorimetric techniques employed by Briggs and Kear(1993). As a result of the obscuring effects of the sediment it was notpossible to document absolute amounts, so these data have been recordedas percentages. For Nereis the chemical analyses were based on a 15-segment section of the trunk under the assumption that this would bebroadly representative of the whole organism; whereas the accumulatedresidue of an entire carcass was used for more anatomically differentiatedCrangon. Multiple specimens were amalgamated for the two sediment-free controls. Where possible, duplicate chemical analyses were carriedout and the results averaged.

Chitin and sclerotized (nonsoluble) protein were measured followingthe method of Hunt and Nixon (1981) as adapted by Briggs and Kear(1993). Residual weights following alkali hydrolysis (5% KOH) to removeprotein, and acid hydrolysis (6 N HCl) to remove chitin, provide a usefulmeasure of the amount of protein and chitin originally present. Samplesizes 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-250as a dye reagent, with an accuracy of 5 mg protein/ml of final assayvolume. Between 100 and 180 mg of each sample was dissolved in 1 mlbuffer solution (Tris) and 0.25 ml of 1 M NaOH, along with 5 ml of theprotein reagent. Absorbance was measured at 595 nm (Unicam 989 SolarMark 2 spectrophotometer). Blanks and a set of standards of varyingprotein amounts (from 5 to 200 mg) were included for calibration.

Carbohydrate content was analyzed using the colorimetric method ofDuBois et al. (1956). Thirty to 50 mg of sample suspended in 0.5 ml ofwater was mixed with 0.5 ml of 5% phenol in 0.1 M HCl and 2.5 ml ofconcentrated sulfuric acid. Absorbance was measured at 490 nm (Unicam

989 Solar Mark 2 spectrophotometer). Blanks and a set of standards ofvarying carbohydrate amounts (from 5 to 50 mg) were included forspectrophotometer calibration.

Phospholipid analysis was adapted from Petersen et al. (1991). Byreleasing lipid-bound phosphate using dichloromethane-methanol extrac-tion, the quantity of phosphate can be measured colorimetrically usingmalachite green as the reagent (absorbance measured at 610 nm; Unicam989 Solar Mark 2 spectrophotometer). Blanks and a set of standards ofvarying phosphate amounts (from 0.25 to 4 mg) were included forspectrophotometer calibration.

RESULTS

Sediment mineralogy had a pronounced effect on the preservation ofprimary anatomical features in both Nereis and Crangon, but with markedtaxonomic differences. In Nereis (Figs. 1, 2), both the sediment-free controland the montmorillonite treatment yielded only chaetae and jaws (Stage 5;Supplementary Material, Table S1), whereas the calcite-hosted and quartz-hosted specimens also preserved thinly coherent remains of the originalintegument (Stages 4 and 4/3, respectively). By far the most substantialeffect, however, was with the kaolinite-hosted worms, where flattened butotherwise complete integuments were recovered, including well-preservedsegmentation, parapodia, palps, tentacular cirri, and, in one instance, thegut (Stage 2). These kaolinite-hosted remains were sufficiently robust toallow the extraction of entire worm cuticles, and for dissected portions towithstand both extended tumbling and preparation for stained sections andSEM (Figs. 1A9, 2). In carbonate- and montmorillonite-hosted Nereisthere was a conspicuous development of carcass-associated carbonatemineralization which was not observed in kaolinite or quartz. Montmo-rillonite-hosted specimens typically failed to collapse in concert with thedecay of soft tissues, resulting in a three-dimensional void.

For Crangon (Fig. 3), none of the sediment types substantially enhancedanatomical preservation relative to the ASW control, although it is notablethat the control itself preserved a significant degree of articulated cuticle(Stage 3, Supplementary Material, Table S1). As with Nereis, it was thekaolinite system that preserved the greatest level of anatomical detail (Stage3), whereas calcite and quartz appear to have accelerated decay (Stage 4).In montmorillonite, Crangon typically occurred as thin cuticular filmsadhering to uncollapsed sedimentary matrix, along with significantaccumulations of a pinkish-white mineral within the body cavity—probably calcium phosphate (cf. Briggs and Kear 1994a). Althoughequivalent to Stage 3 or better in some respects (e.g., the robustly preservedtail fan), the overall quality of Crangon preservation in montmorillonitewas substantially lower than its counterparts in kaolinite, calcite, andASW. Crangon in quartz also resulted in a three-dimensional void, but thiswas not accompanied by the pronounced mineralization associated withmontmorillonite. None of the Crangon treatments yielded coherent cuticlefollowing the cleaning/tumbling procedure.

The distinctive morphological expression of the variously treatedcarcasses was reflected in their residual chemical composition (Fig. 4). Inboth taxa, for example, it was the kaolinite system that preserved thehighest percentage of protein—though once again there was nomeasurable difference between Crangon in kaolinite and its ASW control.Indeed, the protein:chitin:carbohydrate ratios of Crangon were notsubstantially altered in any of the sediment treatments, apart frommodest increases in the chitin content (at the expense of protein) inquartz, montmorillonite, and calcite.

By contrast, sediment mineralogy had a profound effect on thechemical composition of the Nereis residues (Fig. 4). In kaolinite thepercentage of preserved protein was twice that of the ASW control(including a significant occurrence of otherwise-unpreserved water-solubleprotein) whereas in quartz and montmorillonite it was less than half. Thebalance was met almost exclusively by chitin, with kaolinite-hosted

146 L.A. WILSON AND N.J. BUTTERFIELD P A L A I O S

specimens represented by ,12% chitin, compared to ,75% for those inquartz and montmorillonite. The Nereis-quartz and Crangon-kaoliniteexperiments also preserved a small amount of phospholipid.

The differing treatments also had idiosyncratic effects on whole-systemchemistry (Tables 1, 2). Most conspicuously, the addition of kaoliniteinduced a significant drop in pH relative to all other treatments, thoughonly in Nereis was this maintained to the end of the 4-month experiment.As expected, the oxygen content of the sediments and overlying ASWdeclined in all of the decay experiments; however, the residual oxygenlevels were substantially lower in quartz and montmorillonite than inkaolinite or carbonate. Oxygen drawdown in kaolinite- and carbonate-hosted Crangon was less than half of that in corresponding treatments ofNereis (possibly a function of differing carcass:sediment ratios, whichwere not quantitatively monitored), but within the Nereis experiments theleast drawdown occurred in kaolinite.

In terms of major ion chemistry (of the overlying ASW), there was littlesystematic change in the concentrations of Cl, Na, Mg, or K over thecourse of the experiments, apart from marked loss of Mg in the twocarbonate treatments (Table 2). By contrast, Ca concentrations declinedsignificantly in sediment-free and carbonate-hosted Nereis, while increasing

for the equivalent conditions with Crangon—and increasing regardless ofcarcass identity in kaolinite. Sulfur concentrations declined substantially inthe carbonate and quartz treatments of both taxa but rose in the twokaolinite experiments. Results for montmorillonite were not availablebecause of its complete absorption of the overlying ASW during the courseof the experiments (see Supplementary Material, Fig. S3).

Despite the localized species effects, the different sediments exhibitedbroadly characteristic responses to carcass degradation. In quartz, forexample, both Nereis and Crangon produced a permeating black exudatethat gradually dissipated over the course of the experiment (Supplemen-tary Material, Figs. S2–S4), whereas localized ‘‘black stains’’ developed inthe vicinity of montmorillonite-hosted carcasses (more conspicuously inNereis than in Crangon; Supplementary Material, Fig. S3). In calcite, allof the associated sediments turned pale gray within the first few weeks(more conspicuously in Nereis than in Crangon), but eventually returnedto their original white color (by week 13 for Nereis and by week 17 forCrangon). Neither of the kaolinite treatments exhibited any colorchanges, though both developed thick floating fungal colonies by theend of the experiment (Supplementary Material, Fig. S3). Nonfungalbiofilms formed in both of the quartz treatments and the ASW controls

FIG. 1.—Exhumed Nereis remains after 17 weeks in A) kaolinite, B) calcite, C) quartz, and D) montmorillonite. A9–D9 are the corresponding isolated remainsfollowing 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.

SEDIMENT EFFECTS ON BURGESS SHALE–TYPE PRESERVATION 147P A L A I O S

(more conspicuously in Nereis than in Crangon); there was no obviousmicrobial growth in the montmorillonite or calcite treatments (Supple-mentary Material, Fig. S3).

DISCUSSION

The incorporation of sediment into laboratory decay experiments shedsfundamental new light onto taphonomic pathways, if only because allfossils form within some sort of sedimentary matrix. At the same time,

however, this actualistic approach adds significant new levels ofdiagenetic and logistic complexity, not least of which involves thechallenge of recovering quantitative data from sediment-bound residueswhile also monitoring the qualitative effects of sediment on carcassmorphology (cf. Plotnick 1986; Allison 1988; Martin et al. 2004; Darrochet al. 2012). The compounding diagenetic feedbacks between carcassesand sedimentary matrix also make it difficult to resolve underlyingmechanisms, though our experimental results introduce some intriguingpossibilities.

FIG. 2.—Exhumed Crangon remains after 17 weeks in A) kaolinite, B) calcite, C) quartz, and D) montmorillonite. A9–D9 are the corresponding isolated remainsfollowing 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.


Sediment Effects on the Preservation of Carbonaceous Fossils

These experiments demonstrate that sediment mineralogy can haveprofound effects—both positive and negative—on the morphologicalpreservation of interred carcasses. Such taphonomic realignment is hardlysurprising given the well-documented influence of mineralogy on thepreservation of sedimentary organic carbon in general (Theng 1979;Ransom et al. 1998; Lutzow et al. 2006; Ziervogel et al. 2007; Wu et al.2012) and, indeed, the preferential occurrence of carbonaceous compres-sion fossils and microfossils in siliciclastic (vs. carbonate-rich) mudstones.Curiously, however, it was the kaolinite system that induced the mostpronounced positive effects on carcass preservation, despite the modestphysicochemical properties of this 1:1 layer clay. By contrast, montmoril-lonite—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 andhistology of the interred carcasses also influence taphonomic trajectories.In the present experiments, for example, the most pronounced effects ofsediment on preservation potential (both positive and negative) wereassociated with relatively labile collagen-based polychaete cuticle,whereas the more recalcitrant chitin-based arthropod cuticle exhibitedonly modest differences relative to the sediment-free control. Suchbehavior is broadly analogous to the enhanced susceptibility ofexceptionally labile (i.e., chemically reactive) tissues to early diageneticmineralization (Butterfield 2002, 2003). Insofar as Nereis cuticle inkaolinite ended up more robustly preserved than Crangon cuticle underany of the experimental conditions, its recalcitrance was clearly acquiredsecondarily, a product of early diagenetic interaction with its sedimentarymatrix.

Sediment-induced changes in morphological preservation potential alsocorrelate with the chemistry of fossil residues, though not necessarily in astraightforward fashion. For Nereis in kaolinite and montmorillonite, the

quality of cuticle preservation varied directly with the percentage ofpreserved protein, suggesting a novel possibility for the formation ofcarbonaceous compression fossils: rather than structural polysaccharidessuch as chitin and cellulose, the key ingredients might well beproteinaceous. Even so, Nereis cuticle was also relatively well preservedin quartz, which exhibited the lowest overall levels of protein and thehighest levels of chitin.

Taphonomic Pathways

At a minimum, the extended preservation of carbonaceous substratesrequires the suppression of aerobic heterotrophs, typically through theremoval or exclusion of free oxygen. The marked drawdown of oxygen inall of the experiments (Table 1) can be ascribed to the early aerobic decayof the carcasses and is presumably a primer for subsequent carbonaceouspreservation. Even so, the substantially lower levels of oxygen in themontmorillonite and quartz treatments demonstrate that morphologicalpreservation is not solely a function of limited oxygen. Indeed, the degreeof oxygen drawdown—along with the production of significant blackexudates (Supplementary Material, Figs. S2–S4)—may simply reflect theextent of initial carcass decay. For Nereis in kaolinite and Crangon inboth kaolinite and calcite, the relatively high concentrations of residualoxygen (at or above the 18% level at which decomposition begins to beoxygen-limited; see Briggs and Kear [1993]) point to preservationalmechanisms other than anoxia—possibly even a requirement formolecular oxygen (see below).

The lack of correspondence between grain size and morphologicalpreservation suggests that sediment permeability was not a primary factorin the preservation of carbonaceous films. Whereas the demonstrablypermeable quartz and calcite systems (evinced by uniform changes insediment color) yielded significant organic residues, the much finer-grained, relatively impermeable montmorillonite treatments (with local-ized black stains; Supplementary Material, Fig. S3) exhibited the poorest

FIG. 3.—Nereis remains after 17 weeks inkaolinite. A) Whole specimen showing details ofsegmentation, parapodia, palps, and tentacularcirri; B) stained sectioned cuticle wall showingpreservation of three distinct integumentarylayers and preferential loss of (nonstructural)internal organs; C) SEM of parapodia withassociated chaetae. Scale bar in C equals 2 mmfor A, 35 mm for B, and 0.5 mm for C.


overall quality of preserved cuticle. These closed conditions, however,corresponded conspicuously with mineral precipitation, especially withinthe body cavity of Crangon (Fig. 2D), suggesting that sediment sealingmay 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 carbonaceouspreservation, there is a case to be made for differential adsorption ofdegradative enzymes on mineral surfaces (Butterfield 1990, 1995). Asoriginally formulated, this enzyme suppression model focused on the highspecific surface areas and high cation exchange capacity of expandingclays such as montmorillonite. These properties clearly failed to enhancepreservation in the current experiments, in which the greatest (positive)response was associated with the relatively low surface area and cationexchange capacity of kaolinite. It is possible, however, that enzymeadsorption on montmorillonite accounts for at least some of the observedpattern, acting not so much to suppress the activity of degradativeexoenzymes as to stabilize them, thereby extending their effectivelifespans (Ziervogel et al. 2007). Such preservational effects conceivablyaccount for the accelerated decay of sediment-associated carcassesdocumented by Plotnick (1986); Allison (1988); and Briggs and Kear(1993).

The particular mechanisms by which sediments enhance the preserva-tion of labile organic compounds remain poorly understood, butsubstrate protection/stabilization—as opposed to enzyme suppression—appears to be the primary control in both soils (Lutzow 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 isoelectricpoints of the sediment and substrate, availability of floc-inducingmultivalent cations, and organic loading. Aluminum and iron oxideshave a particularly high capacity for preserving organic carbon, as doallophane-rich volcanic soils. At least some kaolinitic soils have greatercapacity for stabilizing organic matter than do montmorillonite soils,possibly as a result of enhanced ligand adsorption on the broken edgesurfaces of kaolinite at low pH (Bruun et al. 2010).

One of the problems in adapting models of organic preservation fromsoil science and organic geochemistry to paleontology is that they do notobviously address the issue of morphological preservation; i.e., stabiliza-tion of carbonaceous substrates at a sufficiently early stage to captureanatomical form. Especially for macroscopic compression fossils, theprocesses responsible for preserving morphological organic carbon areunlikely to be the same as those acting on total organic carbon (TOC). Inthe present experiments, for example, there is no particular reason toassume that the montmorillonite treatments preserved less TOC than didkaolinite—only that macromolecular structures were more readily brokendown into smaller migration-prone compounds (with a correspondingloss of morphology but enhanced likelihood of mineral adsorption andamorphous recondensation [Lutzow et al. 2006; Wu et al. 2012]). The lack

FIG. 4.—Chemical composition of Nereis and Crangon remains after 4 monthsof burial in differing sediment mineralogies and the control. ASW 5 artificialseawater; Kao 5 kaolinite; Calc 5 calcite; Qtz 5 quartz; and Mont5 montmorillonite.

TABLE 1.—pH and oxygen concentration of the sediment and overlying artificial seawater (ASW) at the end of the taphonomic experiments (initial valuesin 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.

pH–Sediment pH–ASW O2%–Sediment O2%–ASW

N-ASW NA 8.6 (8.4) NA 41 (75)N-Kao 4.77** (4.71*) 5.1** (8.4) 17 (47) 28 (75)N-Calc 7.31 (7.48) 7.2 (8.4) 10 (53) 28 (75)N-Qtz 7.80 (7.06) 7.8 (8.4) 4 (39) 10 (75)N-Mont 6.24 (8.92) NA (8.4) 8 (65) NA (75)C-ASW NA 6.7 (8.4) NA 48 (75)C-Kao 7.34 (3.78*) 7.2 (8.4) 29 (48) 22 (75)C-Calc 7.31 (7.48) 7.3 (8.4) 30 (53) 54 (75)C-Qtz 8.17 (6.95) 8.3 (8.4) 11 (36) 53 (75)C-Mont 6.22 (8.44) NA (8.4) 7 (42) NA (75)

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 lessstructural material was degraded and dispersed at the outset.

The circumstances leading to the exceptional preservation of Nereis inkaolinite (Figs. 1, 2) clearly interfered with normal decay processes at avery early stage, but the phenomenon cannot be explained simply in termsof reduced rates or temporary suspension. Despite the morphologicalfidelity, the exhumed remains are constitutionally and chemically distinctfrom the original carcasses; only cuticular structures remain, and theseexhibit none of their original susceptibility to decomposition in water(Fig. 1A9). Partial decay will, of course, change the chemistry of anysubstrate, and Gupta et al. (2009) have demonstrated that lipids cancontribute to the polymerization of decaying tissues within weeks ofdeath. Such alteration, however, rarely leads to the morphologicalpreservation of carbonaceous substrates, at least in the absence of anexternal fixing agent.

Taphonomic Tanning—A Hypothesis

One of the most common means of enhancing the recalcitrance oforganic substrates is through tanning, a process involving the secondarycross-linking of structural biomolecules. Tanning occurs biologically,where it determines the primary recalcitrance of particular substrates suchas polychaete chaetae, arthropod cuticle, and hard keratin in vertebrates,but it can also be induced abiologically via external tanning agents. In theleather 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, includingmultivalent Fe, Zr, Ti, and Si, polyphosphates, and various aluminosil-icate minerals (Kanagy and Kronstadt 1943; Covington 1997; Huefferet al. 2010); in at least one patented process, the agent is derived fromkaolinite (Plapper et al. 1981). Under particular circumstances, postmor-tem tanning can also take place naturally. In the case of recent tannedcadavers, for example, the exceptional preservation of external morphol-ogy appears to be related to salty, marine-influenced groundwater andconspicuously sticky soil (Ruwanpura and Warushahennadi 2009). Bycontrast, the tanning agent responsible for the selective preservation ofskin and keratin in medieval peat bogs has been identified as a carbonyl-rich polysaccharide (sphagnan), facilitated by a suppression of exoen-zymes at moderately low pH (Painter 1991).

Reduced pH also appears to have been a significant factor in thepostmortem stabilization of Nereis cuticle in kaolinite (Table 1), likelyinduced by the high proportion of reactive crystal edges and low cationexchange capacity of the clay component (Tombacz 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 histologicalselectivity, focused exclusively on structural cuticle (cf. Painter 1991).Moreover, the 4.7 to 5.1 pH of the Nereis-kaolinite system is well abovelevels that interfere with anaerobic fermentation or bacterial sulfatereduction (Painter 1991; Fauville et al. 2004). The preferential andexceptional preservation of collagenous cuticle in kaolinite suggests asignificant level of secondary, diagenetically induced tanning (alongsidethe biologically tanned chaetae and jaws).

In industrial tanning, an initial pickling phase is necessary to reduce therate of collagen cross-linking and to enhance the penetration of tanningagent, while background ionic concentrations (salts) limit osmoticswelling and deformation; controlling the balance between substratereactivity, penetrability, and (morphological) integrity is key to thetanner’s art (Covington 1997). The same situation is likely to hold fortaphonomic tanning, in which the interplay of degrading carcasses andsedimentary matrix determines the progress of secondary cross-linkingand, ultimately, the quality of a potential carbonaceous compressionfossil. In the case of the Nereis-kaolinite experiment, we suggest that theenhanced preservation was controlled by the presence of a sediment-derived (presumably Al-based) tanning agent combined with a particu-larly favorable compliment of ion concentrations and pH trajectory (cf.Naimark et al. 2013). The proclivity of organic material to concentrateenvironmental Al under acidic conditions (Mulholland et al. 1987) mayhave been a significant factor in this process.

Kaolinite-based tanning clearly cannot account for all instances ofenhanced preservation, since Nereis carcasses in both quartz andcarbonate also survived substantially better than does the sediment-freecontrol. Nor is tanning necessarily the only contributing process: giventhe relatively elevated S and O2 concentrations associated with thekaolinite experiments (Tables 1, 2), it is possible that disulfide bonding(via the oxidation of sulfhydryl groups) might also have contributed tothe stabilization of morphology-defining proteins (cf. Visschers and deJongh 2005). If so, then localized availability of free oxygen might be acritical factor in fossil preservation, just as it is for the (primary) cross-linking of hard keratins (Greenberg and Fudge 2013).

Implications for BST Preservation

Burgess Shale–type preservation is a loosely defined taphonomic modecharacterized by the exceptional preservation of carbonaceous compres-sion fossils in marine shales (Butterfield 1995; Gaines et al. 2008). Muchof the BST fossil record derives from biologically tanned structures suchas arthropod cuticle and polychaete chaetae, which tend to be sharply, ifnot always robustly, preserved. Not surprisingly, the situation withbiologically untanned integument is much more variable. Polychaete

TABLE 2.—Major ion concentration (in ppm) of the overlying artificial seawater (ASW) at the beginning and end of the taphonomic experiments. Note thecontrasting 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.

Cl Na Mg K Ca S

Initial ASW 14,137 8769 1053 329 296 242N-ASW 14,949 8020 927 362 51* 234N-Kao 13,066 8294 977 384 394 291***N-Calc 15,758 8425 484 410 76** 98N-Qtz 14,275 7821 861 353 153 52N-Mont NA NA NA NA NA NAC-ASW 11,924 8313 999 335 415* 234C-Kao 12,765 8437 894 341 548 290***C-Calc 12,767 8636 616 355 1113** 150C-Qtz 15,106 8112 840 349 176 145C-Mont NA NA NA NA NA NA

N 5 Nereis; C 5 Crangon; Kao 5 kaolinite; Calc 5 calcite; Qtz 5 quartz; Mont 5 montmorillonite; NA 5 not available.


cuticle in the Burgess Shale, for example, sometimes exhibits exquisitelevels of anatomical detail but is usually less precisely preserved (ConwayMorris 1979), typically appearing more like Nereis in quartz (Fig. 1C)than like Nereis in kaolinite (Fig. 1A); in many Burgess Shale specimenssegmentation is only recognizable through the preservation of segmen-tally disposed chaetae. Such variability points to complex diageneticallyand phylogenetically sensitive taphonomic pathways, consistent with adiagenetic tanning mechanism.

The potential for secondarily tanned structures to taphonomicallyoutperform inherently more recalcitrant structures is demonstrated inBST biotas by the common preservation of carbonaceous gut structures(Wilson 2006); indeed, it is the exceptionally thin (i.e., more tenuouslypreserved) nature of most arthropod cuticle (Orr et al. 2009) that revealsthis internal anatomy. By contrast, secondarily tanned structures tend tobe much more uniformly expressed and can be exceptionally thick and/orreflective, as in the case of Eldonia guts (Butterfield 1996). A similar,highly reflective style of carbonaceous preservation occurs in the stem-group chordate Pikaia (Butterfield 1990, 2003; Briggs and Kear 1994b;Conway Morris and Caron 2012), which might also be ascribed to thetaphonomic tanning of a collagen-based integument.

The recognition of secondary, diagenetically induced shifts inpreservation potential also has important implications for interpretingthe histological and phylogenetic affiliations of problematic BST fossils(Butterfield 2003). By selectively enhancing the preservation potential ofmore labile substrates, early diagenetic tanning—like early diageneticmineralization—undermines assumptions of tapho-anatonomic orderingbased on sediment-free degradation experiments (e.g., Allison 1988;Briggs and Kear 1993, 1994a; Sansom et al. 2010). At the other end ofthe scale, sediment mineralogy has the potential to accelerate thedegradation of inherently more recalcitrant substrates; e.g., Crangon inmontmorillonite, but also notable in soils, where lignin commonlydegrades more rapidly than sediment-stabilized polysaccharides andproteins (Lutzow et al. 2006; Mikutta et al. 2006; Schmidt et al. 2011).Unfortunately, the complex interplay of original histology and earlydiagenesis precludes most broad-scale generalizations.

Despite the idiosyncratic nature of exceptional preservation, thedistinctive expression of BST biotas and corresponding small carbona-ceous fossils through the Cambrian and Early Ordovician suggests abroadly comparable diagenetic context (Butterfield 1995, 2003; Van Royet al. 2010; Butterfield and Harvey 2012). In light of the presentexperiments, secular changes in the average clay mineralogy and oceanchemistry are likely to have been significant factors in the opening andclosing of this taphonomic window. Intriguingly, oceanic pH is estimatedto have been at its Phanerozoic minimum during the early Paleozoic(Arvidson et al. 2013), coincident with the interval of enhanced BSTpreservation. Elevated kaolinite input may well have played a role but isdifficult to demonstrate in particular BST settings because of instancesdue to secondary alteration of original clay minerals (cf. Powell 2003;Forchielli et al. 2013).

At a broader scale, there is a conspicuous correlation between BSTpreservation and a Cambro–Ordovician spike in the occurrence ofanomalously shallow-water glauconite (see Brasier 1980; Chafetz andReid 2000; Nielsen and Schovsbo 2011; Peters and Gaines 2012). As aclass, glauconite–Fe-illite–Fe-smectite represents a broad continuum ofiron-rich, redox-sensitive clay minerals that form during marinediagenesis (Meunier and El Albani 2007). Iron-rich clays have previouslybeen invoked to explain BST preservation through the adsorption anddeactivation of degradative enzymes (Butterfield 1995) but mightalternatively 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 asiron-based tanning (cf. Kanagy and Kronstadt 1943).

As a product of early diagenesis, glauconite does not represent theoriginal mineralogy of incoming aluminosilicates and may not itself bethe cause of early Paleozoic shifts in preservation potential. ManyCretaceous greensands, for example, appear to be derived from volcanicsources (Jeans et al. 1982), and it is clear that glauconite forms from awide range of precursor minerals, including kaolinite (Meunier and ElAlbani 2007). Evidence of intense, large-scale continental weatheringthrough the Cambro–Ordovician interval (Avigad et al. 2005; Peters andGaines 2012) implies significant inputs of Al-rich clays to the globaloceans at this time, potentially contributing to both the spike in bothshallow-water glauconite and BST preservation.

CONCLUSION

Entry into the body fossil record requires that carcasses, or componentsof carcasses, survive their individual taphonomic thresholds. For Nereis-type polychaete cuticle this means disrupting the normal course ofdecomposition within the first 2 to 4 weeks, and for Crangon-typearthropod cuticle, it means disrupting the course within 25+ weeks(Allison 1988; Briggs and Kear 1993, 1994a). Our experimental resultsindicate that this can be readily achieved with burial in sediments ofparticular mineralogies—provided the accompanying histologies andpore-water chemistries are all suitably aligned. The sensitivity of suchsystems to local circumstance suggests that exceptional BST preservationis 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 hintof BST fossils. Conversely, the identification of first-order effects ofsediment mineralogy on the preservation potential of carbonaceoussubstrates offers an explanatory mechanism for fossilization, even underseemingly suboptimal conditions, such as the surprisingly commonoccurrence of well-defined leaf compression–impression fossils incoarse-grained sandstones (see Krishtofovich [1944]).

The other critical factor is the carcasses themselves. Some tissues areinherently more recalcitrant than others, but their potential forfossilization depends on the interplay of particular organic substratesand their early diagenetic conditions. Despite the conventional focus onbiologically tanned chitinous cuticle, exceptional BST preservation mayowe more to the secondary tanability of more labile substrates,particularly proteins. Given the marked sensitivity of this phenomenonto local circumstance, perhaps the most remarkable aspect of BSTpreservation is its capacity to capture such a range of histological andphylogenetic diversity in localized Lagerstatten.

ACKNOWLEDGMENTS

We thank Gillian Forman for her enormous assistance with the laboratorywork. LAW was supported by a NERC (Natural Environment ResearchCouncil, UK) PhD studentship.

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Received 25 July 2013; accepted 3 November 2013.

SUPPLEMENTARY MATERIAL

Supplemental material is available from the PALAIOS data archive:http://palaios.ku.edu/data.html.


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