Ichnotaxonomy of Microbial Trace Fossils in Volcanic Glass
McLoughlin, N., Furnes, H., Banerjee, N. R., Muehlenbachs, K., Staudigel, H., Journal of the Geological Society
Ancient microbial activity in volcanic glass creates micron-sized cavities that can be regarded as trace fossils. These are common in glassy rims of oceanic pillow lavas and volcanic breccias. Morphologically comparable mineralized traces are also found in (meta)-volcanic glasses from ophiolites and Precambrian greenstone belts. Multiple lines of evidence indicate microbial formation of these borings, although the affinity of the trace maker(s) is poorly constrained. Two broad morphological types have been previously recognized and termed 'granular' and 'tubular' bioalteration textures. Here optical microscopy and SEM observations are used to erect two new ichnogenera: Granulohyalichnus igen. nov. and Tubulohyalichnus igen, nov. Five ichnospecies are also defined: Granulohyalichnus vulgaris isp. nov., a granular species; Tubulohyalichnus simplus isp. nov., an unornamented tubular species; Tubulohyalichnus annularis isp. nov., an annulated tubular species; Tubulohyalichnus spiralis isp. nov., a helicoidal tubular species; Tubulohyalichnus stipes isp. nov., a branched tubular species. This systematic taxonomy is advanced to allow reliable comparisons to be made between new and existing reports of these microbial borings. Moreover, the adoption of a taxonomic framework will aid the development of these ichnofossils as palaeoenvironmental indicators and tracers of microbial evolution.
A trace fossil is defined as 'a morphologically recurrent structure resulting from the life activity of an individual organism (or homotypic organisms) modifying the substrate' (Bertling et al. 2006). This definition encompasses both macroscopic and microscopic traces that are found in substrates such as rock, unlithified sediment, shell, bones and wood. Familiar examples include burrows, tracks and trails in soft sediments, and, our focus here, borings in marine substrates (Bromley 2004). Less well-known than microborings in marine carbonate substrates are borings found in the volcanic glass of pillow lava rims and volcanic breccias. These micro-textures have now been recognized for over 20 years (Ross & Fisher 1986), during which time multiple lines of evidence have come together to support their biogenicity, and these are briefly reviewed below (see also Staudigel et al. 2006; Furnes et al. 2008). We formally propose herein that these textures should be considered as trace fossils. Microborings are widespread in marine pillow lavas and have been described from all of the major oceanic basins back to the oldest (c. 170 Ma) in situ oceanic crust (e.g. Fisk et al. 1998). Comparable mineralized micro-textures have also been reported from ancient fragments of oceanic crust preserved in Phanerozoic ophiolites and Precambrian greenstone belts, to as early perhaps as the Early Archaean (Furnes et al. 2004; Banerjee et al. 2006, 2007; Fumes et al. 2007). The idea that these micro-textures are trace fossils has been implicit in many earlier reports and explicit in some recent studies that used the term ichnofossil (e.g. Walton 2005; Banerjee et al. 2007; Cockell & Herrera 2008; Staudigel et al. 2008); however, to date only a preliminary ichnological description using open nomenclature has been attempted (McLoughlin et al. 2008).
Here the first systematic description of microbial ichnofossils from volcanic glass is presented, and the novel ichnogenera Granulohyalichnus igen. nov. and Tubulohyalichnus igen. nov. are defined. Their occurrence in volcanic glass substrates is the principal criterion or ichnotaxobase that underpins the establishment of these novel ichnogenera, and to emphasize this hyalo from the Greek hyaleos for glassy is incorporated into their name. These new ichnotaxa show some morphological similarities to trace fossils previously described from carbonate substrates and further details are given below. We argue that they deserve to be treated as separate ichnotaxa however, because their occurrence in volcanic glass requires markedly different bioerosion mechanisms and opens up a novel, globally extensive ichnofossil habitat. (A parallel situation exists for borings in lithic and woody substrates that exhibit similar morphologies but form two exclusive ichnofossil groups with separate ichnotaxonomies; Bertling et al. 2006.) In this study we focus on examples obtained from the in situ oceanic crust and Phanerozoic ophiolites that are relatively well preserved and exhibit intricate morphological details that allow the establishment of five new ichnotaxa.
The principal motivation for erecting these trace fossils and providing distinguishing features for the different taxa is to allow reliable comparisons to be made between new and existing reports from in situ oceanic crust, ophiolites and greenstone belts. The second reason is that trace fossils can be used as palaeoenvironmental indicators, and systematic taxonomy will aid the development of trace fossils in volcanic glass as indicators of, for instance, palaeo-redox conditions, fluid flow and microbial evolution (e.g. Fumes & Staudigel 1999). Third, trace fossils often provide information concerning the behaviour of the constructing organism, and we here draw attention to some of the key morphological and textural relationships observed in volcanic glass that may encode behavioural information (see also Walton 2008). Hence, the overall aim of this paper is to provide an ichnological framework that will facilitate the future study of microbial trace fossils in volcanic glass. In comparison with the study of trace fossils in sedimentary and biological substrates this is a fledgling branch of ichnology. Below we briefly review what is currently known about the micro-organisms thought to be responsible, the distribution of these trace fossils in the oceanic crust and their fossil record (see Furnes et al. 2008, for a detailed review). Table 1 of Staudigel et al. (2008) gives the most up-todate summary of (meta)-volcanic glass sample sites investigated for ichnofossils by the authors of this paper.
Review of work to date
Microbial bioerosion of volcanic glass was first recognized by Ross & Fisher (1986), who reported grooves on the surface of glass shards from a Miocene tephra that they likened to fungal borings found in carbonate grains. Some years later, the investigation of sub-glacial volcanic breccias from Iceland led Thorseth et al. (1992) to propose a mechanism for the microbial dissolution of volcanic glass leading to the creation of etch pits. Since that early work, it has been argued in global surveys of volcanic glass from the oceanic crust that microbial bioerosion is a widespread phenomenon that produces conspicuous granular and tubular cavities (e.g. Fisk et al. 1998; Furnes et al. 2001c). Moreover, these microbial bioerosion traces or ichnofossils can be distinguished from abiotic processes of glass alteration that produce a smooth interface between the fresh glass and altered products (e.g. Furnes et al. 2007, fig. 13). This altered material is termed palagonite and is a fine-grained and often banded mixture of clays, iron-oxyhydroxides and zeolites (Stroncik & Schmincke 2001). In contrast, the granular and tubular textures produced by microbial alteration form a much more irregular and ramified interface between the fresh glass and alteration products. The complex morphology of the tubular textures, in particular their often curved, twisted and sometimes branched paths, which are described in detail below, led to their investigation as biogenic structures.
Trace fossils in volcanic glass substrates have been documented in the rims of pillow lavas and hyaloclastites from submarine environments (e.g. Furnes et al. 2001c), with the majority of known examples occurring in basaltic glasses. Subterranean microbial activity in continental flood basalts has also been reported (e.g. Stevens & McKinley 1995) but no trace fossils have yet been described from these environments. There are four main lines of evidence that support a biological origin for tubular and granular microborings found in pillow lavas. (1) The application of biological stains has shown that DNA is concentrated at the interface between fresh and altered glass, especially on the margins of granular and tubular structures (e.g. Giovannoni et al. 1996; Torsvik et al. 1998, fig. 2; Banerjee & Muehlenbachs 2003, fig. 14; Walton & Schiffman 2003, fig. 8.). (2) Thin linings less than 1 µp? wide of carbon, nitrogen and phosphorus have been detected by electron probe mapping of modern and ancient bioalteration textures (e.g. Giovannoni et al. 1996; Torsvik et al. 1998; Furnes & Muehlenbachs 2003). These linings are independent of the distribution of calcium, thereby confirming that the carbon occurs in an organic phase that is interpreted to be decayed cellular material (e.g. Torsvik et al. 1998; Banerjee & Muehlenbachs 2003). (3) Carbon isotope values measured upon volcanic glasses from pillow lava rims that contain candidate ichnofossils show a marked shift relative to the pillow cores that lack ichnofossils, and this shift is consistent with biological activity (further explanation has been given by Furnes et al. 2001b). (4) Partially fossilized, mineral encrusted microbial cells have been observed in or near etch pits on altered glass surfaces and, crucially, these pits show forms and sizes that resemble the microbes, suggesting that they are responsible for pit formation (e.g. Thorseth et al. 1992, 2001, 2003). Taken together, this morphological and chemical mapping, combined with the carbon isotopic shifts in the host glass, strongly points towards a microbial origin for these ichnofossils.
A consortium of endolithic (i.e. rock dwelling) micro-organisms including heterotrophs and chemolithoautotrophs is involved in the bioalteration of volcanic glass. Culture-independent molecular profiling studies have found that basaltic glass is colonized by micro-organisms that are distinct from those found in both seawater and sea-floor sediments (Mason et al. 2007, and references therein). For example, one study found that indigenous microbial sequences obtained from the Arctic sea floor were affiliated to eight main phylogenetic groups of bacteria and a single marine Crenarchaeota group (Lysnes et al. 2004). In contrast, another study found a predominance of archeal over bacterial nucleic acid sequences in submarine oceanic island hyaloclastites from Hawaii (Fisk et al. 2003). It is envisaged that these micro-organisms include heterotrophs, which use organic carbon from circulating seawater as a carbon source (Staudigel et al. 2008). The microbial consortia also likely include chemolithoautotrophs that use oxidized compounds such as Fe^sup 3+^, Mn^sup 4+^, SO^sub 4^^sup 2-^ and CO2 in the glass and/or circulating seawater as electron acceptors coupled to electron donors such as reduced Fe and Mn in the glass (e.g. Bach & Edwards 2003; Templeton et al. 2005). The suggestion that iron oxidation is employed by microbes that bioerode volcanic glass is consistent with the resemblance of bacterial moulds found on glass to the branched and twisted filaments of iron-oxidizing bacteria such as Gallionella and Mariprofundus ferrooxydans (e.g. Thorseth et al. 2001; Emerson et al. 2007). Volcanic glass substrates may also provide a source of key nutrients, especially phosphorus, which is otherwise scarce in oligotrophic sub-sea-floor environments, and it has been confirmed experimentally that micro-organisms preferentially colonize both phosphorus- and iron-bearing silicate glass (Roberts-Rogers & Bennett 2004). In the oceanic crust prokaryotic micro-organisms occur as a dispersed biomass and apparently have long generation times that may explain why it has not yet been possible to cultivate any of these micro-organisms in the laboratory (Einen et al. 2006). There are even reports of eukaryotes from within the oceanic crust, with putative marine fungi described from carbonate-filled vesicles in Eocene sea-floor basalts (Schumann et al. 2004). These findings may be significant, because fungi produce hyphae that are known to produce tubular cavities in silicate minerals (see Smits 2006).
Controlled laboratory experiments in which seawater microbial populations are cultivated on volcanic glass have produced etch pits and alteration rinds on glass fragments (e.g. Thorseth et al. 1995a). Moreover, it has been shown that micro-organisms enhance the production of authigenic mineral phases relative to purely abiotic experiments and, in particular, cause marked Sr exchange between seawater and volcanic glass (Staudigel et al. 1998). These types of laboratory experiments have failed to produce extended micro-tubular cavities, however, and it has been speculated that this again may be due to the long microbial generation times involved. None the less, it has been demonstrated that micro-organisms contribute to enhanced, localized dissolution of volcanic glass, and thus a conceptual model of how they create granular and tubular bioerosion traces has been advanced and refined in a series of papers (e.g. Thorseth et al. 1992, 1995a; Staudigel et al. 1995, 1998, 2008; Furnes et al. 2008). This process begins when circulating fluids introduce micro-organisms into pore spaces in the rock such as fractures or vesicles and along the rims of glass fragments. These microbes progressively etch the fresh glass, creating the trace fossil cavities, which radiate away from the surface of initiation and form a ramified interface comprising tubes and coalesced granular cavities, thereby increasing the surface area of fresh glass available for dissolution (Staudigel et al. 2004). Dissolution may also be accompanied by precipitation of fine-grained authigenic minerals such as clays, iron-oxyhydroxides and zeolites within the ichnofossils and fractures. These may entomb decayed organic remains, creating the localized enrichment in carbon, nitrogen and phosphorus along the margins of the bioalteration textures. The exact biochemical mechanisms of dissolution of the glass by micro-organisms are only partially understood and might conceivably include the secretion of organic acids, or the production of siderophores and complexing agents (Staudigel et al. 2008).
Systematic ichnology and methods
In this paper we erect two novel ichnogenera Granulohyalichnus igen. nov. and Tubulohyalichnus igen, nov., which correspond to the previously recognized granular and tubular bioalteration textures found in volcanic glass. We provide below a systematic description of the morphological features that characterize both ichnogenera. We then further subdivide these into five ichnospecies on the basis of morphological variations in their form: Granulohyalichnus vulgaris isp. nov., a granular form; Tubulohyalichnus simplus isp. nov., an unornamented tubular form; Tubulohyalichnus annularis isp. nov., an annulated tubular form; Tubulohyalichnus spiralis isp. nov., a helicoidal tubular form; Tubulohyalichnus stipes isp. nov., a branched tubular form. All of these ichnotaxa are summarized in the line drawing Figure 1, and optical and scanning electron microscopy images are shown in Figures 2-6. The helicoidal and branched morphologies, in particular, have not previously been illustrated in such detail and these images provide new constraints, discussed below, on the microbial origins of these structures. A previous study by Fisk et al. (1998) stated that 'putative microbial weathering, produces at least eight styles of pits, channels tunnels and voids'. A survey of the material available to us and examination of previous illustrations (detailed synonym lists are given below) provided us with ichnotaxobases for proposing five ichnospecies at present. We hope and intend that this ichnotaxonomy will be adopted by future studies of microboring in volcanic glass and will be extended and refined to include new morphologies that may come to light.
The trace makers responsible for each of these ichnotalxa have not yet been positively identified, and we suspect that homomorphic production of these traces (i.e. different organisms creating the same traces), especially in case of the more simple granular forms, is highly likely. Conversely, it is also probable that the same micro-organisms may produce different ichnofossil morphologies in volcanic glass with different substrate geochemistries and environmental conditions. It is therefore unlikely that there is a one-to-one relationship between ichnofossil morphology and the constructing micro-organisms.
The optical images shown here were obtained using a Nikon LV100Pol Polarizing microscope at the Centre for Geobiology in Bergen, and the images denoted edf are extended depth of focus images. These are composite images created by stacking an aligned series of images collected in the z-direction. This allows 3D structures such as microborings that curve in and out of the plane of the section to be shown entirely in focus at high magnification. The three slides containing type material (collection numbers: TS-3419, TS-3420, TS-3421) are lodged with the Natural History Museum in Bergen, Norway.
Ichnogenus Granulohyalichnus igen. nov. McLoughlin & Furnes 2008
Type ichnospecies. Granulohyalichnus vulgaris isp. nov.
Diagnosis. Spherical structures found along fractures, on vesicle walls and around the margins of volcanic glass fragments. Occur as isolated granules, or irregular clusters of granules that can coalesce to form bands of granular textures.
Differential diagnosis. Isolated granules that may coalesce to form larger, irregular clusters and or bands. The granules are equidimensional and can be distinguished from Tubulohyalichnus igen. nov., which shows much greater length-to-width ratios. Granulohyalichnus igen. nov. is comparable with the ichnotaxon Planobola isp. (Schmidt 1992) found in carbonate substrates, which is thought to include the initial microborings of various trace makers, especially cyanobacteria and green algae, as well as the mature traces of unicellular or globular-multicellular cyanobacteria such as Cyanosaccus piriformis (Lukas & Golubic 1981). However, Planobola isp. traces are significantly larger in diameter than Granulohyalichnus igen. nov., typically 10-30 µm, and are sometimes connected to the surface by a single, thick stalk that is not seen in the Granulohyalichnus igen. nov.
Etymology. Granulum (Latin, a small particle; this follows previous terminology used to describe these structures), ichnos (Greek, trace) and hyaleos (Greek, glass), referring to the sole substrate bearing this ichnogenus and species.
Ichnospecies. Granulohyalichnus vulgaris isp. nov.
1992 'pit textures', Thorseth et al. (1992, pp. 845-849, figs 1 and 2)
19956 'etching marks', Thorseth et al. (1995e, pp. 146-152, fig. 4)
1996 'micropits . . . small to large spherical bodies (types 1, 2, 3 subdivided by size)', Furnes et al. (1996, p. 192, figs 1-3)
1998 'spherical structures', Torsvik et al. (1998, p. 167, figs 2 and 3)
1999 'spherical alteration', Furnes et al. (1999, pp. 229-230, figs 2 and 3)
1999 'isolated and/or . . . continuous zones of coalescing spherical patches', Furnes & Staudigel (1999, p. 98, fig. 1)
2000 'spherulitic bodies', Alt & Mata (2000, pp. 303-305, fig. 1)
2001c 'granular alteration', Furnes et al. (2001c, pp. 5-16, figs 3 and 7)
2001 'etch marks', Thorseth et al. (2001, pp. 33-35, fig. 1 especially le)
2001a 'spherical bodies', Furnes et al. (2001a, pp. 76-77, fig. 2)
2002a 'granular textures', Furnes et al. (2002a, pp. 408-411, figs 1,2 and 6)
2003 'granular alteration . . . individual and/or coalesced spherical bodies', Banerjee & Muehlenbachs (2003, pp. 4-5, fig. 4)
2007 'granular alteration', Furnes et al. (2007, pp. 159-160, figs 9A and 10)
2008 'granular alteration', Furnes et al. (2008, pp. 1-68, fig. 1)
2008 'granular alteration', McLoughlin et al. (2008, pp. 392393, fig. 5)
Diagnosis. Spherical structures found along fractures, on vesicle walls and around the margins of volcanic glass fragments. Occur as isolated granules, or irregular clusters of granules that can coalesce to form bands of granular textures.
Etymology. Granulum (Latin, a small particle), hyaleos (Greek, glass), ichnos (Greek, trace) and vulgaris (Latin, common), chosen because of the abundance of this ichnospecies.
Description. Individual spherical bodies may be partly hollow or filled with very fine-grained phyllosilicates, zeolites and ironoxyhydroxides and perhaps also titanite (CaTiSiO^sub 4^). The diameter of the granules, regardless of age, location and depth in the oceanic crust, varies from around 0.1 µm to rare examples that are 1.5 µm across, with the most common size around half a micron (data presented by Furnes et al. 2007, fig. 6). In the initial stages of bioerosion the granules occur as isolated spherical bodies along fresh surfaces in the glass; as the bioalteration proceeds they become more numerous and coalesce into aggregates, and then continuous bands of granular material.
Type material, locality and horizon. Sample 418A-62-4, 64-70 from Ocean Drilling Program-Deep Sea Drilling Project (ODPDSDP) hole 41 8 A on the Bermuda Rise in the Atlantic Ocean (25°02.10'N, 68°03.44'W). The oceanic crust has an age of 110 Ma at this location and the sample was collected 366.1 m into the volcanic basement (Furnes et al. 2001c). This sample also contains the type example of Tubulohyalichnus simplus isp. nov. Bergen Natural History Museum collection number TS3419.
Distribution. Granulohyalichnus vulgaris isp. nov. has been reported from numerous in situ oceanic crust sites worldwide. These include the Atlantic Ocean ODP-DSDP holes 648B, 409, 411, 559, 561, 410A, 396B, 407, 417D and 418A; and the Pacific holes 504B, 896A, 834B and 11 84 A. A map of these has been given by Fumes et al. (2008, fig. 4) and lithological logs for each site have been given by Fumes et al. (2008, fig. 5). Examples described from ophiolites include the 92 Ma Troodos ophiolite from Cyprus (Fumes et al. 2001a) and the 160 Ma Mirdita ophiolite from Albania (Fumes et al. 2007). The only putative examples documented to date from meta-volcanic glass in Precambrian greenstone belts come from the Barberton Greenstone Belt of South Africa (Banerjee et al. 2006).
Remarks. Granulohyalichnus vulgaris isp. nov. is by far the most abundant ichnofossil found in recent volcanic glass. Their relatively small size, however, means that they are highly susceptible to recrystallization of volcanic glass during metamorphism, and as a consequence their geological record is less extensive than that of Tubulohyalichnus igen. nov. As a note of caution, the relative simple morphology of Granulohyalichnus vulgaris isp. nov. demands that putative examples must be carefully distinguished from abiotic, chemical etch pits that may form in the absence of microbes. For example, geochemical support for microbial involvement, such as enrichments in carbon and nitrogen associated with Granulohyalichnus vulgaris isp. nov. and the attachment of biological stains in sub-recent material, must be sought.
Ichnogenus Tubulohyalichnus igen. nov. McLoughlin & Furnes 2008
Type ichnospecies. Tubulohyalichnus simplus isp. nov.
Diagnosis. Tubular structures that radiate away from fractures, vesicle walls and inwards from the margins of volcanic glass fragments. Tubes range in diameter between c. 0.4 µm and c. 6 µta with an average diameter of 1.4 µm and the mineralized tubes being higher in this range (data presented by Fumes et al. 2007, fig. 6). Their lengths are highly variable, from a few microns to several hundred microns, with only limited variation in diameters along their lengths. Tubes may be straight, curved, branched or helical, and may exhibit annulations along their walls. They occur as isolated tubes or dense clusters of subparallel tubes that may be hollow, partially or wholly infilled with mineral phase(s).
Differential diagnosis. Extended tubular structures that propagate away from fresh surfaces along fractures, vesicle walls and the rims of volcanic glass fragments. They can be distinguished from Granulohyalichnus igen. nov. by their much greater length-towidth ratio. Tubulohyalichnus igen. nov. is comparable with the ichnogenus Fascichnus ispp. found in carbonate substrates (Radtke & Golubic 2005), which is produced by cyanobacteria, and, in particular, ichnotaxa such as Fasciculus dactylus, first described by Radtke (1991). This trace is characterized by a carpet or radiating bundle of tubes up to 150 µm long and 3-8 µm in diameter that show only rare bifurcations (e.g. Wisshak et al. 2005, fig. 6A). These tubes are of constant diameter except sometimes for slight thickening seen towards their distal ends. This ichnotaxon is known to be produced homeomorphologically and at least three cyanobacteria species are capable of forming this trace (see Wisshak et al. 2005).
Etymology. Tubulus (Latin, a small tube; this follows previous terminology used to describe these structures), hyaleos (Greek, glass) and ichnos (Greek, trace).
Ichnospecies. Tubulohyalichnus simplus isp. nov.
1996 'micro-channels, vermicular (type 4)', Furnes et al. (1996, p. 192, figs 1-3)
1998 'tube-like structures', Torsvik et al. (1998, p. 167, figs 2 and 3)
1998 'channels ... septate channels ... bulbous channels ... irregular branching channels', Fisk et al. (1998, pp. 978-979, fig. 1)
1999 'irregular tubular features', Furnes & Staudigel (1999, p. 98, fig. 1)
1999 'irregular vermicular bodies', Furnes et al. (1999, pp. 2-4, figs 2 and 3)
2000 'irregular or vermicular tubes and channels', Alt & Mata (2000, pp. 303-305, fig. 1)
2001c 'tubular alteration', Furnes et al. (2001c, pp. 5-16, figs 4 and 7)
2001a 'tubular bodies', Furnes et al. (2001a, pp. 76-77, fig. 2)
2002a 'tubular textures', Furnes et al. (2002a, pp. 408-411, figs 3-5, 7 (fig. 3b shows projections termed buds on the sides of the tubes))
2003 'tubes', Fisk et al. (2003, pp. 3-4, figs 2 and 4)
2003 'tubules, curving and villiform', Walton & Schiffman (2003, pp. 10-1 1, figs 4, 7 and 8)
2003 'tubular to vermicular, channel-like features . . . straight and curved . . . highly convoluted . . . bifurcate, numerous branches . . . scalloped walls', Banerjee & Muehlenbachs (2003, pp. 48, fig. 4)
2004 'tubules and zones of microbial alteration', Storrie-Lombardi & Fisk (2004, p. 3, fig. 1)
2007 'tubular alteration, straight to curved . . . budding, branching', Furnes et al. (2007, pp. 159-160, figs 2-5, 9b, c and 10b)
2008 'tubular projections', Furnes et al. (2008, pp. 1-68, fig. 25g and h)
2008 'tubular alteration', McLoughlin et al. (2008, pp. 393-396, figs 6 and 7)
2008 'simple tubes', Walton (2008, pp. 351-364, figs 1-5)
Diagnosis. Simple unbranched, tubular structures that lack ornamentation on their walls and may be hollow or partially infilled with mineral phase(s). Are of near-uniform diameter, except towards their terminations, where they may taper or swell. The majority, however, simply end or pass out of the plane of section, although some show more complex terminal morphologies (Walton 2008, and below).
Differential diagnosis. Unbranched, unornamented tubes with a straight to curvilinear growth axis. These are the simplest morphological form of the genus Tubulohyalichnus igen. nov.
Etymology. Simplus (Latin, simple), emphasizing that this is the simple, unornamented species.
Description. The borings are unbranched and occur as isolated tubes or dense clusters and 'fringing' bands of subparallel tubes that propagate away from fractures, vesicle walls and the rims of glass fragments (e.g. Fig. 3). In some examples the tubes show an anastamosing path that can curve back on itself and form loose tangles towards their ends (e.g. Fig. 3b; also Walton 2008, fig. 5A). More typically, however, the tubes show a strong directionality, propagating in a linear to curvilinear path at high angles to the surface from which they originate. Some examples from the Troodos ophiolite show a very fine ornament, often discontinuous on the wall (e.g. Fig. 3c); the origin of this is uncertain but we hypothesize that the desiccation of fluids once present inside the tubes may be responsible. Microtubes described from the Hawaii Scientific Drilling Project exhibit an especially wide range of terminal morphologies including 'finials, nail heads, numerous branches . . . mushroom shapes' (Walton 2008).
Type material, locality and horizon. Sample 418A-62-4, 64-70 from ODP-DSDP hole 418A on the Bermuda Rise in the Atlantic Ocean (25°02.10'N, 68°03.44'W). The oceanic crust is 110 Ma old at this location and the sample was collected 366.1 m into the volcanic basement (Furnes et al. 2001c). This sample also contains the type example of G. vulgaris isp. nov. Bergen Natural History Museum collection number TS-3419.
Distribution. These are widely reported from in situ oceanic crust, including the North to central Atlantic Ocean, the Lau Basin in the SW Pacific and the Costa Rica Rift in the western Pacific (Furnes et al. 2008, fig. 4), the Hawaiian seamount chain (e.g. Walton & Schiffman 2003; Walton 2008) and the Ontong-Java Plateau (Banerjee & Muehlenbachs 2003). Examples described from ophiolites include the 92 Ma Troodos ophiolite from Cyprus (Furnes et al. 2001a, fig. 6F and G), the 160 Ma Mirdita ophiolite from Albania (Furnes et al. 2007, fig. 7B) and the 443 Ma Solund-Stavfjord Ophiolite in Norway (Furnes et al. 2002b). Mineralized examples described from greenstone belts include the c. 2.5 Ga Wutai Greenstone Belt of China, the c. 2.7 Ga Abitibi Greenstone Belt of Canada (Bridge et al. 2007), the c. 3.5 Ga Barberton Greenstone Belt of South Africa (Furnes et al. 2004; Banerjee et al. 2006, 2007) and the c. 3.5 Ga Pilbara Craton of Western Australia (Banerjee et al. 2007; Furnes et al. 2007).
Remarks. The simple unbranched tubular forms lacking ornamentation are the most abundant of all the tubular forms. Scanning electron microscopy investigation has found examples containing fine, sub-micron wide filaments that are suggested to be of biological origin (Banerjee & Muehlenbachs 2003, Figs 6-8).
Ichnospecies. Tubulohyalichnus annularis isp. nov.
1998 'septate channels ... string-of-bead shapes', Fisk et al. (1998, pp. 978-979, fig. If and g)
2001 'segmented tubes', Furnes et al. (2001a, pp. 76-77, fig. 2f)
2002a 'segmented tubes', Furnes et al. (2002a, pp. 408-411, fig. 4)
2003 'anastamosing channels with dark walls and segmented appearance', Banerjee & Muehlenbachs (2003, pp. 4-8, fig. 4e)
2008 'annulated tubular', McLoughlin et al. (2008, pp. 393-396, fig. 6B)
Diagnosis. Tubes with regularly or irregularly spaced annulations or constrictions along their length that confer a septate appearance.
Differential diagnosis. Only species that exhibits annulations.
Etymology. Annulatus (Latin, ringed) referring to the diagnostic morphological annulations.
Description. Most commonly, tubes are of near-uniform diameter with regularly spaced annulations (e.g. Fig. 4a and b). Less common are examples with irregularly spaced annulations and variations in tube diameter, especially towards their ends (e.g. Fig. 4c and d). These can be compared with the 'string-of-beads' form previously described by Fisk et al. (1998), which shows irregularly spaced bulbous swellings along the length of the tubes. T. annularis isp. nov. has a larger diameter than T. simplus isp. nov., being up to 15 µm across.
Type material, locality and horizon. Sample CY-1-30 from drill core CY-1 in the Akaki River section (35°02'54"N, 33°10'46"E) through the Troodos ophiolite, Cyprus (location map and lithological log of the drill core and sample heights have been given by Furnes et al. 2001a, fig. 1). This partially altered volcanic glass fragment, with an age of c. 92 Ma, is of zeolite to prenhitepumpellyite grade and also contains the type example of T. spiralis isp. nov. Bergen Natural History Museum collection number TS-3420.
Distribution. From the in situ oceanic crust, Tubulohyalichnus annularis isp. nov. is reported from the Ontong-Java Plateau (Banerjee & Muehlenbachs 2003) and in pillow lavas from the Indian Ocean (Fisk et al. 1998). The only examples described to date (four samples) from an ophiolite come from the Troodos ophiolite of Cyprus (Furnes et al. 2001a).
Remarks. The annulations are an intrinsic feature of the tube, as their orientation and spacing are independent of glass substrate; that is, they do not change when the tubes curve, as would be predicted if this reflected some structural control or imprint from the host glass. It has been suggested that the annulations are a result of stepwise or pulsed dissolution by the euendolithic micro-organisms that created the tube (Staudigel et al. 2008). Such features are well known from ichnotaxa in calcareous substrates; for instance, Podichnus centrifugalis as reported by Bromley (2005, fig. 6).
Ichnospecies. Tubulohyalichnus spiralis isp. nov.
1998 'helical channels', Fisk et al. (1998, p. 979, no illustration)
2001 'spiral structures', Furnes et al. (2001a, pp. 76-77, fig. 2c)
2002a 'spiral tubes', Furnes et al. (2002a, pp. 408-411, fig. 2b)
2008 'tubular', McLoughlin et al. (2008, pp. 393-396, fig. 6f and g)
Diagnosis. Unbranched tubes with a coiled or helical axis (Fig. 5), with up to 12 whorls (i.e. complete rotations), but they normally show fewer than this and may be either sinistrally or dextrally coiled. Tubulohyalichnus spiralis isp. nov. may show a linear or curved growth axis with the spacing and diameter of the whorls changing along its length.
Differential diagnosis. The only tubular ichnotaxa in volcanic glass that has a helical axis.
Etymology. Spiralis (Latin, a coil) referring to the diagnostic helical form.
Description. These are coiled or helical-shaped tubes that penetrate into the glass away from the margins of glass fragments, analogous to the cavity made by a corkscrew driven into the cork of a wine bottle. The tubular helix may change along its length, most typically with the diameter decreasing towards the termination of the tube and the whorls becoming more closely spaced. Occasionally, T. spiralis isp. nov. is seen to wrap around a single-stranded tube of T. simplus isp. nov. (e.g. Fig. 5a-e).
Type material, locality and horizon. Sample CY- 1-30 from drill core CY-1 in the Akaki River section (35°02'54"N, 33°10'46"E) of the Troodos ophiolite of Cyprus (location map and lithological log of the drill core and sample heights have been given by Fumes et al. (2001a, fig. 1). This partially altered volcanic glass fragment, with an age of c. 92 Ma, is of zeolite to prenhitepumpellyite grade and also contains the type example of T. annularis isp. nov. Bergen Natural History Museum collection number TS-3420.
Distribution. All examples known to date (four samples) come from the Troodos ophiolite of Cyprus (Fumes et al. 2001a).
Remarks. This sophisticated helical morphology strongly supports a biogenic origin for these structures. The functional significance of the helical shape is uncertain but might reflect a growth and/or feeding strategy developed by a hypha-like process within the tube. The documentation of Tubulohyalichnus spiralis isp. nov. wrapping around a simple Tubulohyalichnus simplus isp. nov. is also suggestive of biological behaviour.
Ichnospecies. Tubulohyalichnus stipes isp. nov.
1998 'radiating, irregular branching channels', Fisk et al. (1998, pp. 978-979, fig. 1e)
2002a 'curved tubes sometimes branching', Fumes et al. (2002a, pp. 410-411, fig. 3b)
2008 'branched tubes', McLoughlin et al. (2008, pp. 393-396, fig. 6d and e)
2008 'fine branching channels', Cockell & Herrera (2008, p. 105, fig. 1 (M. Fisk, unpublished material from the Mid-Atlantic Ridge; the tubes and branching are more widely separated in comparison with the example shown here)
2008 'branching microtubules', Walton (2008, pp. 351-364, fig. 3a and c)
Diagnosis. Dichotomously branching tubes in which the diameters of the daughter branches are equal to those of the parent branches.
Differential diagnosis. The only tubular ichnotaxa in volcanic glass that exhibits branching.
Etymology. Stipe (Latin, branch), referring to the diagnostic branching of this ichnospecies.
Description. Dense intergrowths of branching tubes that may occur in hemispherical-shaped clusters or more irregular bands that radiate away from fractures in the glass, vesicle walls and the rims of glass fragments. The tubes are of similar diameter to T. simplus isp. nov., being typically less than 3 µm across.
Type material, locality and horizon. Sample 396B-20R-3, 108112 from ODP hole 396B located 150 km east of the MidAtlantic Ridge (22°59.14' N, 43°30.90'W). The oceanic crust has an age of 10Ma at this location and the sample was collected 140.1 m into the volcanic basement (Fumes et al. 2001c). Bergen Natural History Museum collection number TS-3421.
Distribution. Only a small number of Tubulohyalichnus stipes isp. nov. have been described to date compared with the abundance and widespread distribution of Tubulohyalichnus simplus isp. nov. The sample locations include a Pacific seamount (sample CD- 1-6, Fisk et al. 1998), DSDP site 504B on the Costa Rica Rift (Fumes et al. 2002a), ODP site 396B in the mid-Atlantic (McLoughlin et al. 2008) and the Mid-Atlantic (M. Fisk, impubi, data, illustrated by Cockell & Herrera (2008)).
Remarks. Short projections on the margins of tubular textures have previously been illustrated and termed buds (e.g. Fumes et al. 2002a, fig. 3b). It is suggested that these may represent incipient branching. We suspect that as new material comes to light additional branching morphologies may be found in microborings within volcanic glass.
This paper systematically describes the range of morphological features known to date from microbial ichnofossils in volcanic glass and uses these to erect the ichnotaxa illustrated in Figure 1. This has highlighted key morphological attributes that further strengthen the case for a biogenic origin of these micro-textures and that also encode behavioural information. First, the complex helicoidal morphology of Tubulohyalichnus spiralis isp. nov. is very suggestive of a biological origin, especially examples in which the spacing and diameter of the helix changes along the length of the tube. These features cannot be explained by the migration of mineral inclusions through the glass under elevated fluid pressures, a phenomenon known as ambient inclusion trails that has previously been highlighted by some workers as capable of generating hollow tubular structures in chert substrates (Barghoom & Tyler 1965; Brasier et al. 2006). Rather, we tentatively compare Tubulohyalichnus spiralis isp. nov. to helical fungal hyphae, like those exhibited by some laboratory cultures of dermatophytes (e.g. Trichophyton mentagrophytes van Mentagrophytes; Ellis & Hermanis 2006). This is a tentative comparison, as morphological similarities alone cannot be used to demonstrate a fungal origin. Second, a putative biological growth relationship is recorded by the intertwining of Tubulohyalichnus spiralis isp. nov. and Tubulohyalichnus simplus isp. nov. in which the spiralled tube wraps around a central linear tube and is comparable in shape and size with the coiling of parasitic fungal hyphae around the hyphae of a host fungus (e.g. Nordbring-Hertz 2004, fig. 8). Third, it is conspicuous that the tubular borings do not intersect; rather, subparallel Tubulohyalichnus simplus isp. nov. are sometimes seen to abruptly change growth direction by up to 180° when they meet another tube or fracture (as previously recognized by Fumes et al. 2007, fig. 4C; Walton 2008, fig. 5A). This is argued to reflect adjacent micro-organisms sharing the substrate (i.e. 'not invading one another's patch'), whereas abiotic tubular structures might be expected to intersect. This sharing of the substrate may also explain why in areas with a high density of microborings the tubes are subparallel to avoid intersecting, whereas in areas of lower density microboring the tubes show more anastamosing paths. Lastly, it has been argued that microborings show evidence of mining behaviour in volcanic glass, with their sometimes anastamosing paths being designed to systematically exploit the substrate and extract useful material (Walton 2008). Moreover, tubular microborings sometimes appear to seek olivine phenocrysts, which are a rich source of iron in the glass, and to avoid plagioclase (Walton 2008). Microborings in volcanic glass are thus more than dwelling traces and represent feeding traces, created by microbes harvesting chemical energy in the glass. This is a strong argument for establishing microborings in volcanic glass as a separate taxonomic group from borings in marine carbonates that may show some morphological similarities but are largely dwelling traces.
There have only been a small number of systematic studies to date that have investigated the controls on the distribution of ichnofossils in volcanic glass. Preliminary studies have been undertaken to estimate the per cent abundance of microbial ichnofossils in volcanic glass with depth, temperature, permeability and porosity in the oceanic crust (e.g. Furnes et al. 2001c, and references therein). These studies have found that Granulohyalichnus igen. nov. is by far the most abundant trace fossil and can be found at all depths into the oceanic crust where fresh glass is preserved down to c. 550 m. In the upper c. 350 m of the oceanic crust Granulohyalichnus igen. nov. is the most abundant trace fossil, decreasing steadily to become scarce at temperatures of c. 115 °C near the currently known upper limits of hyperthermophilic life. In contrast, the ichnogenera Tubulohyalichnus igen, nov. constitute only a minor fraction of the total microbial alteration, at most c. 20%, and show an abundance maxima at c. 120-130m depth. In the whole oceanic volcanic pile, the total percentage of microbial alteration increases with permeability and also with the presence of celadonite, which is suggestive of oxygenated waters (e.g. Furnes & Staudigel 1999; Furnes et al. 2001c). With respect to the timing of microboring in the oceanic crust it is noteworthy that both the 5.9 Ma Costa Rica Rift and the HOMa western Atlantic oceanic sections show a similar maxima in the amount of microbial alteration as a percentage of the total alteration, despite their very different ages (Furnes et al. 2001c, fig. 11). This suggests that a substantial portion of the microboring occurs early in crustal history, but it is thought to persist within the crust as long as hydrothermal fluid circulation continues (Staudigel et al. 2008). It should also be borne in mind that taphonomic variables such as changes in fluid flow and authigenic mineral precipitation will modify the preservation potential of the microbial trace fossils in different parts of the oceanic volcanic pile. In summary, the development of an ichnofabric index for volcanic glass substrates, or in other words, a semi-quantitative measure of the textural products of microbial activity in volcanic glass, could help to further elucidate the controls on the distribution of microbial activity in the oceanic crust. This ichnofabric approach is well established for sedimentary substrates (see Droser & Bottjer 1993) and initial attempts have been made to apply and adapt this to volcanic glass substrates (e.g. Montague et al. 2007).
Microbial borings in volcanic glass are ubiquitous in the modern oceanic crust. They represent a valuable potential archive of information concerning the activities of euendolithic microorganisms in the sub-sea-floor, given that as much as 10-20% of the upper oceanic crust may comprise volcanic glass (Staudigel & Hart 1983). Continuing work suggests that microbial activity is also recognizable in meta-volcanic glasses, with a fossil record that is extensive and may include some of the earliest forms on life on Earth (e.g. Furnes et al. 2004; Banerjee et al. 2006, 2007). We therefore formally propose herein an ichnofossil taxonomy for these conspicuous features that have previously been loosely termed tubular and granular bioalteration textures. The new ichnogenera Granulohyalichnus igen. nov. and Tubulohyalichnus igen. nov. are defined and subdivided into the ichnospecies G. vulgaris isp. nov., T. simplus isp. nov., T. annularis isp. nov., T. spiralis isp. nov. and T. stipes isp. nov. (Figs 1-6). It is hoped that this ichnotaxonomy will aid the comparison of new and existing reports of microbial bioerosion textures in volcanic glass and that this 'common language' will aid communication between geobiologists, palaeontologists and igneous petrologists investigating these features. Lastly, the acceptance of an ichnotaxonomic framework, such as that proposed here, will facilitate future efforts to develop the use of microbial borings in volcanic glass as both palaeoenvironmental indicators and recorders of microbial evolution.
We acknowledge the help of many collaborators with the work reviewed herein describing the microbial bioerosion of volcanic glass, including I. Thorseth, T. Torsvik, O. Tumyr, M. de Wit and M. Van Kranendonk. We thank M. Wisshak, in particular, for detailed advice regarding ichnofossil taxonomy, and B. Hannisdal for constructive comments. Editorial comments by D. Mcllroy and reviews by 2 anonymous reviewers helped improve this manuscript. Financial support for this research was provided by the Norwegian Research Council, the National Sciences and Engineering Research Council of Canada, the US National Science Foundation, the Agouron Institute and the National Research Foundation of South Africa. We also thank the many individuals and organizations who have assisted our field studies over the last 15 years and who are too numerous to name here.
ALT, J.C. & MATA, P. 2000. On the role of microbes in the alteration of submarine basaltic glass: a TEM study. Earth and Planetary Science Letters, 181, 301313.
BACH, W. & EDWARDS, K.J. 2003. Iron and sulphide oxidation within the basaltic ocean crust: Implications for chemolithoautotrophic microbial biomass production. Geochimica et Cosmochimica Acta, 67, 3871-3887.
BANERJEE, N.R. & MUEHLENBACHS, K. 2003. Tuff Life: bioalteration in volcaniclastic rocks from the Ontong Java Plateau. Geochemistry, Geophysics, Geosystems, 4, doi:1029/2002GC000470.
BANERJEE, N.R., FURNES, H., MUEHLENBACHS, K., STAUDIGEL, H. & de WIT, M.J. 2006. Preservation of microbial biosignatures in 3.5 Ga pillow lavas from the Barberton Greenstone Belt, South Africa. Earth and Planetary Science Letters, 241, 707-722.
BANERJEE, N.R., SIMONETTI, A., FURNES, H., STAUDIGEL, H., MUEHLENBACHS, K., HEAMAN, L. & VAN KRANENDONK, M.J. 2007. Direct dating of Archean microbial ichnofossils. Geology, 35, 487-490.
BARGHOORN, E.S. & TYLER, S.A. 1965. Microorganisms from the Gunflint Chert. Science, 147, 563-577.
BERTLING, M., BRADDY, S.J., BROMLEY, R.G., et al. 2006. Names for trace fossils: a uniform approach. Lethaia, 39, 265-286.
BRASIER, M.D., MCLOUGHLIN, N. & WACEY, D. 2006. A fresh look at the fossil evidence for early Archaean cellular life. Philosophical Transactions of the Royal Society of London, Series B, 361, 887-902.
BRIDGE, N., BANERJEE, N.R., MUELLER, W., CHACKO, T., MUEHLENBACHS, K. & Furnes, H. 2007. Traces of early life in Archean volcanic rocks from the Abitibi Greenstone Belt, Canada. Geological Society of America, Abstracts with Programs, 39, 409.
BROMLEY, R.G. 2004. A stratigraphy of marine bioerosion. In: McIlroy D. (ed.) The Applications of Ichnology to Palaeoenvironmental and Stratigraphic Analysis. Geological Society, London, Special Publications, 288, 453-477.
BROMLEY, R.G. 2005. Preliminary study of bioerosion in the deep-water coral Lophelia, Pleistocene, Rhodes, Greece. In: Freiwald, A. & Roberts, J.M. (eds) Cold-water Corals and Ecosystems. Springer, Berlin, 895-914.
COCKELL, CS. & HERRERA, A. 2008. Why are some microorganisms boring? Trends in Microbiology, 16, 101-106.
DROSER, M.L. & BOTTJER, DJ. 1993. Trends and patterns of Phanerozoic ichnofabrics. Annual Review of Earth and Planetary Sciences, 21, 205-225.
EINEN, J., KRUBER, C., øVREåS, L., THORSETH, LH. & TORSVIK, T. 2006. Microbial colonization and alteration of basaltic glass. Biogeosciences Discussions, 3, 273-307.
ELLIS, D. & HERMANIS, R. 2006. Trichophyton mentagrophytes var. mentagrophytes. Kaminski's digital image library of medical mycology, University of Adelaide. World Wide Web Address: http://www.mycology.adelaide.edu.au/ Fungal_Descriptions/Dermatophytes/Trichophyton/mentagrophytes.html.
EMERSON, D., RENTZ, J.A., LILBURN, TG. , ET AL. 2007. A novel lineage of Proteobacteria involved in formation of marine Fe-oxidizing microbial mat communities. PLoS ONE, 2, e667.
FISK, M.R., GIOVANNONI, S.J. & THORSETH, I.H. 1998. The extent of microbial life in the volcanic crust of the ocean basins. Science, 281, 978-979.
FISK, M.R., STORRIE-LOMBARDI, M.C., DOUGLAS, S., POPA, R., MCDONALD, G. & DI MEO-SAVOIE, C. 2003. Evidence of biological activity in Hawaiian subsurface basalts. Geochemistry, Geophysics, Geosystems, 4, doi:10.1029/ 2002GC000387.
FURNES, H. & MUEHLENBACHS, K. 2003. Bioalteration recorded in ophiolitic pillow lavas. In: DILEK, Y. & Robinson, P.T. (eds) Ophiolites in Earth's History. Geological Society, London, Special Publications, 218, 415-426.
FURNES, H. & STAUDIGEL, H. 1999. Biological mediation in ocean crust alteration: how deep is the deep biosphere? Earth and Planetary Science Letters, 166, 97-103.
FURNES, H.. THORSETH, I.H., TUMYR, O., TORSVIK, T. & FISK, M.R. 1996. Microbial activity in the alteration of glass from pillow lavas from Hole 896A. In: Alt, J.C., Kinoshita, H., Stokking, L.B. & Michael, PJ. (eds) Proceedings of the Ocean Drilling Program, Scientific Results, 148. Ocean Drilling Program, College Station, TX, 191-206.
FURNES, H., MUEHLENBACHS, K., TUMYR, O., TORSVIK, T. & THORSETH, I. 1999. Depth of active bioalteration in the oceanic crust: Costa Rica Rift (Hole 504?). Terra Nova, 11, 228-233.
FURNES, H., MUEHLENBACHS, K., TUMYR, O., TORSVIK, T. & XENOPHONTOS, C. 2001a. Biogenic alteration of volcanic glass from the Troodos ophiolite, Cyprus. Journal of the Geological Society, London, 158, 75-84.
FURNES, H., MUEHLENBACHS, K., TORSVIK, T., THORSETH, LH. & TUMYR, O. 2001b. Microbial fractionation of carbon isotopes in altered basaltic glass from the Atlantic Ocean, Lau Basin and Costa Rica Rift. Chemical Geology, 173,313-330.
FURNES, H., STAUDIGEL, H., THORSETH, LH., TORSVIK, T., MUEHLENBACHS, K. & TUMYR, O. 2001c. Bioalteration of basaltic glass in the oceanic crust. Geochemistry, Geophysics, Geosystems, 2, doi:10.1029/2000GC000150.
FURNES, H., THORSETH, I.H., TORSVIK, T., MUEHLENBACHS, K., STAUDIGEL, H. & TUMYR, O. 2002a. Identifying bio-interaction with basaltic glass in oceanic crust and implications for estimating the depth of the oceanic biosphere: A review. In: Smellie, J.L. & Chapman, M. G. (eds) Volcano-Ice Interaction on Earth and Mars. Geological Society, London, Special Publications, 202, 407-421.
FURNES, H., MUEHLENBACHS, K., TORSVIK, T., TUMYR, O. & Lang, S. 2002.. Biosignatures in metabasaltic glass of a Caledonian ophiolite West Norway. Geological Magazine, 139, 601-608.
FURNES, H., BANERJEE, N.R., MUEHLENBACHS, K., STAUDIGEL, H. & DE WIT, M.J. 2004. Early life recorded in Archean pillow lavas. Science, 304, 578-581.
FURNES, H., BANERJEE, N.R., STAUDIGEL, H., MUEHLENBACHS, K., DE WIT, M" MCLOUGHLIN, N. & VAN KRANENDONK, M. 2007. Bioalteration textures in recent to Mesoarchean pillow lavas: A petrographic signature of subsurface life in oceanic igneous rocks. Precambrian Research, 158, 156-176.
FURNES, H., MCLOUGHLIN, N., MUEHLENBACHS, K., ET AL. 2008. Oceanic pillow lavas and hyaloclastites as habitats for microbial life through time - a review. In: DILEK. Y., FURNES, H. & MUEHLENBACHS, K. (EDs) Links between Geological Processes, Microbial Activities, and Evolution of Life. Springer, Berlin, 1-68.
GIOVANNONI, S.J., FISK, M.R., MULLINS, T.D. & FURNES, H. 1996. Genetic evidence for endolithic microbial life colonizing basaltic glass/seawater interfaces. In: Alt, J., Kinoshita, H., Stokking, L.B. & Michael, PJ. (eds) Proceedings of the Ocean Drilling Program, Scientific Results, 148. Ocean Drilling Program, College Station, TX, 207-214.
LUKAS, K.J. & GOLUBIC, S. 1981. New endolithic cyanophytes from the North Atlantic Ocean: I. Cyanosaccus piriformis gen. et sp. nov. Journal of Phycology, 17, 224-229.
LYSNES, K, THORSETH. I.H., STEINSBU, B.O., øVREÅS, L., TORSVIK, T. & PEDERSEN, R.B. 2004. Microbial community diversity in seafloor basalts from the Arctic spreading ridges. FEMS Microbiology and Ecology, 50, 213-230.
MASON, O.U., STINGL, U., WILHELM, L.J., MOESENEDER, M.M., DI MEO-SAVOIE, CA., FISK, M.R. & GIOVANNONI, SJ. 2007. The phytogeny of endolithic microbes associated with marine basalts. Environmental Microbiology, 9, 2539-2550.
MCLOUGHLIN, N., FURNES, H" BANERJEE, N.R., STAUDIGEL, H., MUEHLENBACHS, K., DE WIT, M. & VAN KRANENDONK, M. 2008. Micro-bioerosion in volcanic glass: extending the ichnofossil record to Archean basaltic crust. In: Wisshak, M. & Tapanila, L. (eds) Current Developments in Bioerosion. Springer, Berlin, 372-396.
MONTAGUE, K.E., HASIOTIS, S.T. & WALTON, A. W. 2007. Endolithic microborings in basalt glass fragments in hyaloclastites: extending the ichnofabric index to microbioerosion. Geological Society of America, Abstracts with Programs, 39, 73.
NORDBRING-HERTZ, B. 2004. Morphogenesis in the nematode-trapping fungus Arthrobotrys oligospora - an extensive plasticity of infection structures. Mycologist, 18, 125-133.
RADTKE, G. 1991. Die mikroendolithischen Spurenfossilien im Alt-Tertiär West Europas und ihre palökologische Bedeutung. Courier Forschinstitut Senckenberg, 138, 1-185.
RADTKE, G. & GOLUBIC, S. 2005. Microborings in mollusk shells, Bay of Safaga, Egypt: morphometry and ichnology. Facies, 51, 118-134.
ROBERTS-ROGERS, J. & BENNETT, P.C. 2004. Mineral stimulation of subsurface microorganisms: release of limiting nutrients from silicates. Chemical Geology, 203, 91-108.
ROSS, K.A. & FISHER, R.V 1986. Biogenic grooving on glass shards. Geology, 14, 571-573.
SCHMIDT, H. 1992. Mikrobohrspuren ausgewählter Faziesbereiche der tethyalen und germanischen Trias (Beschreibung, Vergleich und bathymetrische Interpretation). Frankfurter Geowissenschaftliche Arbeiten A Geologie-Paläontologie, 12, 1-228.
SCHUMANN, G., MANZ, W., REITNER, J. & LUSTRINO, M. 2004. Ancient fungal life in North Pacific Eocene oceanic crust. Geomicrobiology Journal, 21, 24-246.
SMITS, M.M. 2006. Mineral tunnelling by fungi. In: Gadd, G.M. (ed.) Fungi in Biogeochemical Cycles. Cambridge, Cambridge University Press, 681-717.
STAUDIGEL, H. & HART, S.R. 1983. Alteration of basaltic glass: mechanisms and significance for the oceanic crust-seawater budget. Geochimica et Cosmochimica Acta, 47, 337-350.
STAUDIGEL, H., CHASTAIN, R.A., YAYANOS, A. & BOURCIER, R. 1995. Biologically mediated dissolution of glass. Chemical Geology, 126, 119-135.
STAUDIGEL, H., YAYANOS, A., CHASTAIN, R., ET AL. 1998. Biologically mediated dissolution of volcanic glass in seawater. Earth and Planetary Science Letters, 164, 233-244.
STAUDIGEL, H., FURNES, H., KELLEY, K., PLANK, T., MUEHLENBACHS, K., TEBO, B. & YAYANOS, A. 2004. The oceanic crust as a bioreactor. In: Wilcock, W., Kelley, D., DeLong, E.F., Kelley, D.S., Baross, J.A. & Cary, SC (eds) Deep Subsurface Biosphere at Mid-Ocean Ridges. Geophysical Monograph, America Geophysical Union, 144, 325-341.
STAUDIGEL, H., FURNES, H., BANERJEE, N.R., DILEK, Y. & MUEHLENBACHS, K. 2006. Microbes and volcanos: a tale from the oceans, ophiolites and greenstone belts. GSA Today, 16, doi:10.1130/GSAT01610A.l.
STAUDIGEL, H., FURNES, H., MCLOUGHLIN, N., BANERJEE, N.R., CONNELL, L.B. & Templeton, A. 2008. 3.5 Billion years of glass bioalteration: volcanic rock as a basis for microbial life? Earth-Science Reviews, 89, 156-176.
STEVENS, T.O. & MCKINLEY, J.R 1995. Lithoautotrophic microbial ecosystems in deep basalt aquifers. Science, 270, 450-454.
STORRIE-LOMBARDI, MC & FISK, M.R. 2004. Elemental abundance distributions in suboceanic basalt glass: Evidence of biogenic alteration. Geochemistry, Geophysics, Geosystems, 5, doi:10.1029/2004GC000755.
STRONCIK, N. & SCHMINCKE, H.U 2001. Evolution of palagonite: Crystallization, chemical changes, and element budget. Geochemistry, Geophysics, Geosystems, 2, doi:10.1029/2000GC000102.
TEMPLETON, A.S., STAUDIGEL, H. & TEBO, B.M. 2005. Diverse Mn(II)-oxidizing bacteria isolated from submarine basalts at Loihi Seamount. Journal of Geomicrobiology, 22, 127-139.
THORSETH, I.H., FURNES, H. & HELDAL, M. 1992. The importance of microbiological activity in the alteration of natural basaltic glass. Geochimica et Cosmochimica Acta, 56, 845-850.
THORSETH, LH., TORSVIK, T., FURNES, H. & MUEHLENBACHS, K. 1995a. Microbes play an important role in the alteration of oceanic crust. Chemical Geology, 126, 137-146.
THORSETH, LH., FURNES, H. & TUMYR, O. 1995ft. Textural and chemical effects of bacterial activity on basaltic glass: an experimental approach. Chemical Geology, 119, 139-160.
THORSETH, LH., TORSVIK, T., TORSVIK, V., DAAE, F.L., PEDERSEN, R.B. & KELDYSH-98 Scientific party 2001. Diversity of life in ocean floor basalts. Earth and Planetary Science Letters, 194, 31-37.
THORSETH, I.H., PEDERSEN, R.B. & CHRISTIE, DM. 2003. Microbial alteration of 0-30-Ma seafloor and sub-seafloor basaltic glasses from the Australian Antarctic Discordance. Earth and Planetary Science Letters, 215, 237-247.
TORSVIK, T., FURNES, H., MUEHLENBACHS, K., THORSETH, I. H. & TUMYR, O. 1998. Evidence for microbial activity at the glass-alteration interface in oceanic basalts. Earth and Planetary Science Letters, 162, 165-176.
WALTON, A.W. 2005. Petrography of peridophyllic endolithic microborings from hyaloclastites of Kilauea's Hilina slope: comparison with microborings in HSDP hyaloclastites. Geological Society of America, Abstracts with Programs, 37, 253.
WALTON, A.W. 2008. Microtubules in basalt glass from Hawaii Scientific Drilling Project #2 phase 1 core and Hilina slope, Hawaii: evidence of the occurrence and behaviour of endolithic microorganisms. Geobiology, 6, 351-364.
WALTON, A.W. & SCHIFFMAN, P. 2003. Alteration of hyaloclastites in the HSDP 2 Phase 1 Drill Core 1 . Description and paragenesis. Geochemistry, Geophysics, Geosystems, 4, doi:10.1029/2002GC000368.
WISSHAK, M., GEKTIDIS, M. & FREIWALD, A. 2005. Bioerosion along a bathymetric grathent in a cold temperature setting (Kosterfjord, SW Sweden): an experimental study. Facies, 51, 93-117.
Received 30 April 2008; revised typescript accepted 10 September 2008.
Scientific editing by Duncan McIlroy.
N. MCLOUGHLIN1*, H. FURNES1, N. R. BANERJEE2, K. MUEHLENBACHS3 & H. STAUDIGEL4
1 Department of Earth Science and Center for Excellence in Geobiology, University of Bergen, Allegaten 41, N-5007 Bergen, Norway
2 Department of Earth Sciences, University of Western Ontario, London, ON, N6A 5B7, Canada
3 Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB, T6G 0E2, Canada
4 Scripps institution of Oceanography, University of California, La Jolla, CA 92093-0225, USA
* Corresponding author (e-mail: Nicola.McLoughlin@geo.uib.no)…
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Publication information: Article title: Ichnotaxonomy of Microbial Trace Fossils in Volcanic Glass. Contributors: McLoughlin, N. - Author, Furnes, H. - Author, Banerjee, N. R. - Author, Muehlenbachs, K. - Author, Staudigel, H. - Author. Journal title: Journal of the Geological Society. Volume: 166. Publication date: January 2009. Page number: 159+. © Geological Society Publishing House Jan 2009. Provided by ProQuest LLC. All Rights Reserved.