(4) Sediment Diagenesis and the Effects of Infaunal Burrowing
Sediments have distinct biogeochemical zones that develop in response to the amount of labile organic carbon buried, sedimentation rates, and the availability of different terminal electron acceptors, grain size and permeability. However, the idealised vertical zonation can be disrupted by the burrowing activity of invertebrates. This process, known as bioturbation, causes millimetre- to centimetre-scale biogeochemical heterogeneities that form as a result of particle remobilisation, redox oscillation, excretion, irrigation and grazing of indigenous microorganisms and other organic substrates. Importantly, the presence of open burrows within the sediment alters the solute and gas distribution profiles because they expose the previously insulated subsurface pore-waters to oxygenated waters. This, in turn, can influence the precipitation of various authigenic cements, including calcite, dolomite and ferric hydroxide (e.g., Konhauser and Gingras, 2007; Gingras et al., 2014). In a novel study, led by a former PhD student (Marilyn Zorn, now a geologist with Esso Canada), we examined the effects of marine invertebrate burrow architectures on dissolved oxygen diffusion rates in comparison with unburrowed sediment, and through the use of oxygen microsensors, measured O2 profiles on a micrometer-scale around the burrows of several macroinvertebrates. We showed that oxygen diffusive properties were directly related to burrow architecture, and that most burrow types actually facilitated the lateral diffusion of O2 into previously suboxic/anoxic sediments (Zorn et al., 2006). This then fosters biogeochemical reactions that might not be predicted from traditional models of ideally zoned sediment. A case in point is the type of cements formed. For instance, in a different study, we observed a clear relationship between the biogeochemical processes occurring within a burrow microenvironment and the cementation history of the trace fossil Rosselia socialis from shoreface deposits in the Upper Cretaceous Horseshoe Canyon Formation of Alberta, Canada (Zorn et al., 2007).
(Left Figure) Schematic representation of the biogeochemical landscape in burrowed sediment, showing a partial range of burrow types. (A) Initial organic input is derived from the water column. This source (pelagic in general) is the base of the food pyramid for the sediment-dwelling community. (B) Some sediment grazers (snails and urchins shown here) enrich the sediment in mucous as a result of the animal’s passage, dominantly in the oxic layers. Following decomposition, mucous may provide a secondary organic source for chemoheterotrophic microbial communities. (C) Organic-rich linings (commonly composed of fecal mud) on worm and arthropod burrows are another source of organic substrates. They help stabilise the burrows and serve as reactive surfaces for metal sorption and diagenetic mineral (cement) formation. (D) Small, shallow, unlined burrows probably have little impact on the long-term biogeochemical character of the sediment. (E) Organic substrates may be mined at depth. (F) Increased oxygenation of burrow waters, and the surrounding sediment, facilitates the subsurface oxidation of reduced solutes and mineral phases. (G) Burrowing convects reduced solutes and mineral phases to the seafloor where they are reoxidised. (H) Anoxic microniches can form in the oxic layers due to anaerobic respiration of labile organic substrates, particularly in fine-grained sediment. (Right Figure) Example of iron mineralization associated with burrow microenvironments in a modern tidal flat deposit, Willapa Bay, Washington State. Larger burrows are 4 mm in diameter and belong to nereid polychaetes. From Konhauser and Gingras (2007).
Burrows also contribute to the sequestration of metals from sediment pore-waters. Indeed, burrows are lined with organic materials, usually mucopolysaccharides and proteins, that are characterised by surface functional groups that become anionic over the pH range of marine pore-waters. This makes burrow linings and backfills highly reactive towards dissolved metal cations. In order to actually determine the surface reactivity of worm mucus, we incubated burrowing terebellid worms (a common infaunal species) for the purposes of harvesting their mucus secretions and investigating its composition and metal adsorptive properties. We showed that the natural mucus linings were very efficient sorbents for chalcophilic elements, such as Cd, on par with other sedimentary organic sources, such as microbial biomass (Lalonde et al., 2010). In a logical progression, we then specifically studied the main component of worm mucous, that being the glycoprotein mucin. However, owing to the difficulties in its isolation, my former PhD student (Daniel Petrash, now a PDF at Charles University in Prague) applied a surface complexation approach to model proton and Cd adsorption behaviour of partially purified Type III porcine gastric mucin (PGM), a commercially available analogue to natural infaunal mucus. We found that at marine pH, nearly two-thirds of the total ligands in mucin-type glycoproteins are deprotonated and thus available to participate in metal cation adsorption reactions. Importantly, the concentration of available organic ligands in mucin exceeds (by up to 5 times) that of a variety of other metal-reactive organic compounds comprising the organic fraction of marine sediments (Petrash et al., 2011b). Given that the number of burrows present in tidal flats, the inner shelf, and in many bays and estuaries may range from ∼100/m with such larger animals as shrimp and lugworms, to more than 50,000/m with such smaller animals as with threadworms or amphipods, and the large surface area of exposed burrow-lined mucus, we speculated that these organic substrates may represent the most important metal sinks in marginal marine sediment. In fact, back-of-the-envelope calculations suggest that a 1m surface area of burrowed sediment would have mucus linings beneath the sediment-water interface on the order of 5 m . With a burrow lining thickness of only 10 µm (Zorn et al., 2006), a mucus specific gravity of ∼1450 kg/m and a mucus ligand density of 11 mmol/g (Lalonde et al., 2010), those thin burrow linings could sequester up to 100 mg of trace metal, such as Cd (Konhauser and Gingras, 2011). The impact of irrigation enhances the ability of burrow linings to sequester metals from seawater because some animals have the capacity to cycle a water column 1–10 meters deep through their burrows each day. This ability to pump large volumes of water through their narrow burrows means that there exists a significant exchange of solutes between the overlying seawater and the sediment.
Freshwater sediments are also subject to bioturbation processes that affect the transfer of solutes and gases through the sediment-water interface. Analyses of sediment core from Cooking Lake, Alberta, revealed that H2S fluctuates from depths of several millimetres during the summer, when cyanobacteria generated sufficient O2 to drive the oxic-anoxic chemocline into the sediment, but in the winter, the H2S front extended upwards into the water column due to the cessation of cyanobacterial activity. However, burrowing behaviour was not linked to seasonal changes in the sediment chemistry, which we suggest is due to the ability of Chironomid larvae to exploit oxygen oases in the sediment: in the winter, the larvae harvest their oxygen from the uppermost photosynthetic layer in an otherwise O2 impoverished sediment. So the burrows are, in part, an oxygen-mining structure (Gingras et al., 2007). Crucially, this behaviour may have influenced the evolution of metazoans in the Neoproterozoic. In a recent paper, we suggested that perhaps some ancient ichnofossils can be interpreted as oxygen-mining structures, which then could imply that the bottom marine waters in Earth's past need not have been oxygenated, and the deep ocean waters may have remained anoxic until the latest Neoproterozoic (Gingras et al., 2011).
Drs. Murray Gingras and George Pemberton (University of Alberta), along with myself, have also recently initiated a research programme aimed at improving conceptual models for burrow-associated diagenesis. The research will address two important diagenetic manifestations: dolomitisation and patchy silica cementation in clastic sediments. The former is seen to be a direct manifestation of the presence of discrete biogenic sedimentary structures, and the latter is more commonly associated with cryptic bioturbation. The research is novel as it considers both the biogeochemical and mechanical aspects of strongly heterogeneous fabrics. New diagenetic perspectives will be coupled to petrological data with the intention of addressing the following simple objectives: (1) determine the predictability of burrow-influenced cementation and identify the key factors that influence that predictability; (2) present models for upscaling core-scale permeability fabrics to the bed-set scale; and (3) use the detailed data gathered to model bulk flow and capillary behaviour for idealised burrow facies (see Gingras et al., 2012). To date, research on this front has been led by two UofA students. The first is a former MSc student (John Gordon, now a geologist with Petro-Canada) who conducted detailed petrography of several core samples from the Cretaceous-aged Bluesky Formation in Alberta, a major gas-bearing reservoir in Alberta (Gordon et al., 2010). The unit represents a high-energy, upper shoreface succession with burrow-associated permeability enhancement. The purpose of this study was to evaluate the role that bioturbation of the originally unconsolidated sediment had on its reservoir properties. Petrographic analysis showed that the ancient burrows are generally lined with dark-coloured, iron-rich (mainly chert, shale clasts, and organic grains) fragments, whereas the burrow fill contained mainly quartz and light-coloured chert fragments. This grain segregation has improved the reservoir quality by effectively re-sorting compaction- and cement-resistant chert and quartz into the burrow fill. The second study was led by a former PhD student (Greg Baniak, now a geologist with BP Canada) who analysed the highly bioturbated dolomudstone and dolowackestones of the Mississippian Debolt Formation, the primary reservoir lithologies in the Dunvegan gas field of northwestern Alberta. Sedimentological and ichnological analyses suggest deposition in a carbonate ramp setting that includes sub-environments, such as sabkhas, hypersaline lagoons, restricted subtidal lagoons, intertidal mud flats, and peloidal shoals (Baniak et al., 2014). A low-diversity ichnological assemblage of Chondrites and Planolites commonly characterises the bioturbated reservoir intervals. Dolomitisation occurs primarily within oxidised muds and highly bioturbated sediments. In this context, dolomitisation within the burrows also appears to be mediated by sulphate-reducing bacteria within the restricted lagoonal to intertidal settings of the carbonate ramp. Organic carbon, an essential component for bacterial sulphate reduction, may have been derived, in part, from the decomposition of animals and their by-products (e.g., faecal pellets, mucous linings) associated with the burrows.
The goals for the future are to assess how bioturbation affects metal sequestration, mineral authigenesis and sediment porosity/permeability in marginal marine environments. Major questions being sought are:
What are the mineralogical, geochemical and isotopic variations within bioturbated freshwater and marine sediments?
How does bioturbation affect mineral authigenesis and sediment porosity/permeability?
What are the major metal sinks in marine sediments – POC, microbes, mucus, minerals?
Why are some burrow linings preferentially dolomitised?