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Biogenicity of terrestrial oncoids formed in soil pockets, Cayman Brac, British West Indies
Sedimentary Geology 236 (2011) 95–108
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Sedimentary Geology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / s e d g e o
Biogenicity of terrestrial oncoids formed in soil pockets, Cayman Brac, British West Indies Brian Jones Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta, Canada, T6G 2E3
a r t i c l e
i n f o
Article history: Received 21 September 2010 Received in revised form 29 November 2010 Accepted 23 December 2010 Available online 7 January 2011 Editor: M.R. Bennett Keywords: Terrestrial oncoids Microbes Micrite Coated grains Reticulate filaments
a b s t r a c t Terrestrial oncoids, up to 85 mm long, are common in some of the soil-filled pockets found in the finely crystalline dolostones of the Cayman Formation on Cayman Brac. Each of these coated grains has a nucleus formed of a white, finely crystalline dolostone lithoclast (derived from the Cayman Formation) that is encased by a light brown to tan cortex that is formed largely of micrite and minimicrite, is vaguely laminated, and lacks obvious biogenic structures. The cortex, typically b 10 mm thick, is variable in thickness around individual grains and from grain to grain. On the surfaces of the oncoids there is a diverse microbiota that includes various reticulate filaments that are typically b 1 μm in diameter, cocci, some large-diameter collapsed and calcified filaments, sporangia-like structures, and locally, exopolysaccharides (EPS). In the subsurface parts of the cortices, however, filaments are very rare and there are only scattered cocci. Evidence derived from the surface microbes indicates that they played an active role in the growth of the cortical laminae by binding material to their surfaces, calcification of the microbes, providing substrates on which calcite was precipitated, and forming cavities in which calcite cement was later precipitated. In stark contrast, it is difficult to ascribe a biotic influence to the formation of the subsurface laminae because of the paucity of preserved microbes. The lack of microbes, however, probably reflects the fact that the formative microbes were destroyed during diagenesis. This example clearly demonstrates that the lack of preserved microbes cannot be taken as an indication that the grains formed as a result of abiogenic processes. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Microbes are mystical organisms that seem to have an influence on carbonate precipitation and accretion that is out of all proportion to their size. Nowhere is this more apparent than in the terrestrial realm where coated grains that form in many different settings, have been ascribed to various abiogenic and/or biogenic processes (Calvet, 1982; Calvet and Julia, 1983; Wright, 1989; Jones, 1991). Although microbes have clearly influenced the growth and development of some of these grains, others have cortices that appear structureless and devoid of any organic components. The biogenicity of coated grains is a critical issue because it has commonly been used as a basis for classification. Peryt (1983a, his Table 2), for example, used biogenicity as one of the main criteria for classifying coated grains and the names of different types of coated grains commonly reflect the principle microbe involved in their formation (e.g., Riding, 1983). It is commonly difficult, however, to locate microbes in the very fine-grained calcitic cortices of terrestrial/ pedogenic coated grains, especially if they are only assessed through low-magnification microscopy (Wright, 1989; Jones, 1991). Thus, such grains are commonly considered abiogenic — a decision that automatically influences their classification and notions regarding their origin.
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This paper focuses on coated grains, up to 85 mm long, that are found in soil pockets in the finely crystalline dolostones (Cayman Formation) that form the land surface on the eastern part of Cayman Brac (Figs. 1 and 2). Although their nuclei and cortices are obvious (Fig. 2C), their cortices appear structureless and devoid of microbes when viewed at low-magnification (Fig. 2C and D). At high magnification, however, it becomes readily apparent that microbes are common on the oncoids surfaces and played a formative role in the growth and development of the cortical laminae. In contrast, the cortical laminae beneath the surface of the coated grains contain very few microbes and hence appear to be abiogenic in origin — a conclusion that is diametrically opposite to that derived from examination of the surface microbial mats. Such a contrast is of critical importance given that the issue of biogenicity is central to most classification systems (e.g., Peryt, 1983b) of coated grains. Accordingly, this study focuses on the Cayman coated grains with the view of explaining the dichotomy in the distribution of the microbes and the impact that that may have on the classification and interpretation of coated grains. 2. Terminology Many different names have been assigned to coated grains that have formed in terrestrial/pedogenic settings, including vadoids
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Fig. 1. Location maps. (A) Location of Cayman Brac (CB) in Caribbean Sea. (B) Geological map of Cayman Brac (Jones, 1994, his Fig. 2.3D) showing location where samples were collected (NRC) on Ann Tatum Road.
(Peryt, 1983c), pedogenic coated grains (Wright, 1989), terrestrial oncoids (Wright, 1989; Jones, 1991), and pisoids/ooids (Wright, 2008; Zhou and Chafetz, 2009). Selecting the most appropriate term for the Cayman coated grains is fraught with problems because many of these terms have inherent generic connotations or have been used without definition and therefore simply reflect the bias of the individual researcher. Herein the term “terrestrial oncoids” is applied to the Cayman coated grains because they conform to Wright's (1989) original definition of “…laminated, microbially formed structures that occur in vadose settings, either forming at the atmosphere-soil or sediment or rock interface, or within soil profiles”. As such they are a type of pedogenic coated grain, commonly found in calcrete soils, that are characterized by multiple coats of micrite (Wright, 1989). The microbes found in the Cayman terrestrial oncoids are herein described as filaments and cocci (spherical forms) with no implied taxonomic or genetic implications. The term “micrite” has been applied to carbonate crystals 1–4 μm long and “minimicrite” to carbonate grains b1 μm long (Folk, 1974; Reid and MacIntyre, 1998). Riding (1979), however, applied the term “minimicrite” to grains 0.2–1.0 μm long, Flügel (1982) used the term for grains b2 μm long, and Guo and Riding (1994) reserved it for grains b0.1 μm long. In this study, the terms “micrite” (1–4 μm) and “minimicrite” (b1 μm) are used as first defined by Folk (1974). 3. Geological setting Cayman Brac, the smallest of the Cayman Islands, has a core formed of Tertiary carbonates with an upper surface that slopes from a maximum elevation of ~40 m at its east end to sea level at its west end (Fig. 1). Limestones of the Ironshore Formation (Pleistocene), which onlap an erosional bench cut into the Tertiary carbonates, forms a flat apron along the south, west, and north coasts of the island. The Tertiary carbonates, which dip to the west at ~ 0.5° (Jones, 1994), belong to the Bluff Group that is formed of the Brac Formation (Lower Oligocene), the Cayman Formation (Upper Miocene), and the Pedro Castle Formation (Lower Pliocene). The coated grains, which are the focus of this study, came from an outcrop on Ann Tatum Road, which is located on the northeast side of Cayman Brac (Fig. 1B).
Construction of the road in 2008 provided clean, fresh sections through the white, finely crystalline dolostones of the Cayman Formation that forms the land surface in that area at an elevation of ~30 above sea level (Fig. 2A). Before construction of the road, the area was covered with a dense natural vegetation of tropical trees, bushes, and ground creepers that were rooted in potholes and root cavities that are filled with soil (Fig. 2A). The densely packed coated grains, of variable size and shape, were found in the soil pockets that are up to 0.5 m in diameter and up to 3 m deep and contain numerous roots (Fig. 2A and B). It should be noted, however, that the soil pockets (1) are highly variable in diameter and depth, (2) commonly merge or bifurcate below ground, and (3) have highly irregular walls. The poorly lithified soil is formed of red to dark brown clays that are mixed with biofragments (largely derived from land snails), and irregular fragments of dolostone that came from the surrounding bedrock. Given that the coated grains were collected only a few months after the rock, terra rossa, and coated grains had been exposed, there had had been little time for tropical weathering to modify them. 4. Methodology Large (7.5 × 5.0 cm) thin sections were made from three of the terrestrial oncoids so that their internal structures could be determined. Scanning electron microscope (SEM) analyses were conducted on a JOEL Field Emission SEM (JOEL 6301FE). An accelerating voltage of 5 kV was used for imaging because this is the optimal setting for high-resolution images. SEM samples were carefully extracted from the terrestrial oncoids with note being made of their location and orientation in the cortices. The samples were mounted on SEM stubs using double-sided tape and/or silver conductive glue. Samples were sputter coated with a very thin layer of gold or chrome prior to being examined on the SEM. This study is based largely on 845 SEM photomicrographs that were obtained from the terrestrial oncoids. Energy-dispersive X-ray (EDX) analyses were done using the Princeton Gamm-Tech X-ray analysis system that is attached to the SEM. These analyses were conducted with an accelerating voltage of 20 kV using the minimum beam diameter possible. Some analytical
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Fig. 2. Photographs of coated grains. (A) Outcrop showing white dolostones of upper part of Cayman Formation with pockets of soil in which trees and bushes (removed during road construction) were rooted. White letter B indicates position of Fig. 2B. (B) Terrestrial oncoids held in loose matrix amid root system. (C) Polished cross-sections through terrestrial oncoid showing nuclei formed of white fossilifereous dolostone derived from the Cayman Formation coated with light to dark orange cortex. (D, E) Thin section photomicrographs showing cortical laminae formed of micrite and scattered detrital grains of dolomite (white). Note vaguely defined laminae and Mn precipitates (arrows). Blue area is epoxy covering outside of grain. (F, G) Laminae in interior of cortices formed of small coated grains, micrite, and patches of calcite cement. Some coated grains have distinct nuclei formed of detrital dolomite/calcite (white) grains whereas others appear to be formed entirely of micrite.
problems were encountered because the volume of material analyzed (~1 μm3) is commonly larger than the diameter of the microbes being analyzed. Thus, the beam may penetrate through the microbes and detect elements that are located in the background or to one side of the object being analyzed. These problems were overcome by analyzing clusters of microbes rather than single filaments or cocci,
and/or obtaining separate analyses of microbes and their underlying substrate so that the exact location of the elements detected by EDX analysis could be determined. Any questionable analyses were disregarded. Adobe Photoshop CS © was used to adjust the brightness and contrast of the digital field, thin section, and SEM images.
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5. Terrestrial oncoids — morphology The terrestrial oncoids, which have a dull, light to medium brown surface color (Fig. 2B), are 7 to 85 mm long, 7 to 82 mm wide, and 5 to 44 mm high (Fig. 3). The small (b1 cm) coated grains are typically spherical whereas the larger grains range from elongate cylinders to large, flat, plate-like forms. The cortices are thin (typically b20%, rarely to 40%, of grain radius) and irregularly developed around the grain with one side commonly being two to three times the thickness on the other side (Fig. 2C). As such they are equivalent to the “superficial pisoids” of Zhou and Chafetz (2009). Many of the larger, highly irregular oncoids formed through the amalgamation of numerous smaller grains. They are akin to the “compound pisoids of Zhou and Chafetz (2009). 5.1. Nucleus Cross-sections through the terrestrial oncoids shows that each has a large nucleus that is encased by a thin, vaguely laminated cortex (Fig. 2C). The irregular-shaped nuclei are formed of white, finely crystalline fossilifereous dolostone that came from the Cayman Formation (Fig. 2A) of the surrounding bedrock (Fig. 2C). 5.2. Cortex The cream to light orange colored cortex contrasts sharply with the white dolostone nuclei (Fig. 2C). Vaguely defined laminae are highlighted by slight variations in color and/or disseminated black, Mn-rich precipitates. The cortices are formed largely of very finely crystalline calcite (minimicrite/micrite) along with minor amounts of clay, dolomite, and Mn oxides (Fig. 2C and D). Thin section analysis shows that the cortices are characterized by (1) dense, dark-colored
micrite with vaguely defined laminae that are evident because of slight color variations and/or minor concentrations of small detrital grains (Fig. 2D), (2) small (b0.1 mm long) detrital dolomite and/or calcite crystals concentrated in some laminae (Fig. 2E), (3) small (b0.5 mm long) biofragments, derived from gastropod shells, and (4) small, round to ovate coated grains that are ~0.1 mm diameter (Fig. 2F and G). Each of the micro-coated-grains has a well-defined nucleus that is encased by a cortex formed of micrite (Fig. 2F and G). Some nuclei are formed of detrital calcite or dolomite grains whereas others are formed of micrite that is slightly different in color from the surrounding cortex (Fig. 2F and G). In effect, these grains are miniature versions of the large coated grains. 5.3. Surface topography The surfaces of the terrestrial oncoids are irregular with elevated mounds and ridges separated by valleys (Figs. 2B and 4A and B). There is no pattern to the size, shape, or distribution of these features and there are no indications that one side developed in preference to another. The summits of the elevated areas are typically smooth and disrupted by desiccation cracks (Fig. 4C). Thin (b1 μm thick) mats, which appear to be calcified exopolysacchrides (EPS) films, overlie detrital calcite and dolomite grains, micrite, calcified filaments, and cocci that are commonly infused with EPS (Fig. 4D). Textural relationships indicate that the mats bound loose sediment to the surface of the coated grain. The valleys between the topographic highs are characterized by small (b0.1 mm diameter), loosely packed coated grains (Fig. 4B, E andF), micrite (Fig. 4G), filamentous microbes (Fig. 4E and H), detrital calcite and dolomite grains that are commonly encased with micrite (Fig. 4I and J), cocci, and sporangia. Patches of EPS are found throughout these areas and locally, there are secondary Mn-oxide precipitates (Figs. 2E and F and 4K). In many areas, filamentous microbes lie under and on top of these Mn precipitates (Fig. 4K). There is no pattern to the distribution of these components. 6. Terrestrial oncoids — biota
Fig. 3. Bivariant graphs for terrestrial oncoids showing relationship between (A) length and width, and (B) length and height. Dashed line indicates 1:1 ratio.
The surfaces of the terrestrial oncoids are populated by a diverse array of microbes (Figs. 5–10) that are highly variable in terms of their preservation. Some are completely collapsed with no evidence of any mineralization whereas others have been fully calcified. Determining if a microbe has been calcified posed significant problems because they are commonly b1 μm in diameter, and detection of light elements, including C, on the SEM system used is difficult. With these caveats in mind, however, determination of microbe mineralization was based on (1) whether or not the microbe was collapsed, (2) detection of elements in the microbe by EDX analysis, with such analyses being preferentially located in areas where there were intertwined filaments or clusters of cocci provide larger target areas for analysis, (3) the presence of C peaks on the EDX diffractograms, where evident, (4) the presence/absence of crystals, and/or (5) how the microbes react when the electron beam is placed on their surfaces — non-mineralization forms will commonly expand and burst open as the electron beam is placed on their surfaces (Melim et al., 2009; Jones, 2010a). Collectively, these features provide a very good indication of the preservation state of the microbes. Partly desiccated threads of EPS can produce structures that mimic filamentous microbes. Herein, tube-like structures were deemed to be filamentous microbes if (1) their diameter was relatively constant along their length and from specimen to specimen, (2) there was no evidence of distortion due to desiccation, and (3) they had the appearance of filaments as opposed to dried and curled EPS. Conversely, “filaments” were considered to be desiccated EPS if (1) curled edges were readily apparent, (2) there was radical changes in diameters along their length, and/or (3) their morphology was
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Fig. 4. SEM photomicrographs showing main features on exterior of terrestrial oncoids. (A) General view showing elevated smooth area, covered with EPS, surrounded by lower areas covered with porous, granular material. (B) Low-lying area covered with loosely bound grains of various sizes and shaped and filamentous microbes. (C) Smooth, desiccated EPS on surface of elevated area (from Fig. 4A). (D) Micrite and minimicrite that lies just beneath the EPS layer shown in Fig. 4C. (E) Loose grain on surface of coated grain (from area like that shown in Fig. 4B) coated with micrite, EPS, and filamentous microbes. Box labeled F indicates position of Fig. 4F. (F) Enlarged view from Fig. 4E showing EPS covering surface of grain. (G) Micrite and minimicrite coating surface of loose grain. (H) Filamentous microbes and micrite on surface of loose grain. (I, J) Small grains (boundaries indicated by arrows) partly coated with micrite and microbes (see Fig. 2F, G). (K) Mn-oxide precipitate (arrows) coating substrate. Note associated filamentous microbes and cocci.
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Fig. 5. SEM photomicrographs of reticulate filaments RF-C to J (see Table 1 for descriptions). Repeated EDX analyses of many different specimens indicate that these filaments are calcified.
inconsistent along their length or between specimens that were located close to each other. The microbial biota found on the surfaces of the terrestrial oncoids is divided into the (1) reticulate filaments, b1 μm in diameter, with walls characterized by a meshwork structure (Figs. 5–7), (2) large-diameter calcified filaments, up to 10 μm in diameter (Fig. 8A–F), (3) largediameter (3.5–4.0 μm wide, in flattened form), septate collapsed filaments that are partly calcified (Fig. 8G–I), (4) filamentous microbes formed of linked beads, up to 15 μm external diameter, with calcified walls (Fig. 8J–L), and (5) spherical to ovate cocci (Fig. 9), some of which are held in sporangia-like structures (Fig. 10).
6.1. Reticulate filaments These non-branching and possible septate filaments, typically b1 μm in diameter and commonly N500 μm long (Figs. 5–7), have walls formed of an open meshwork (Melim et al., 2008; Jones, 2009a). EDX analyses consistently showed that they are formed of Ca that is presumed to be in the form of calcite. The appearance of the filaments, their 3-dimensional form, and the paucity of collapsed forms support this suggestion (Figs. 5–7). The reticulate filaments are divided into nine different types based on their external diameter, surface ornamentation, and morphology of the meshwork (shape and size
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Table 1 Summary descriptions of reticulate filaments found in terrestrial oncoids from Cayman Brac with comparisons to previously described reticulate filaments. Mesh opening (nm)
Mesh wall thickness (nm)
Chamber shape and arrangement
500–700 350–450
60–70 40–50
60–70 40–60
RF-E 5 C
500–600
40–50
40–50
Diamond, spiral along length Rounded diamond, spiral along length Square, parallel to length
RF-F 5D
550–650
RF-G 5E,F
400–450
RF-H 5 G,H
750–850
RF-I 5I,J
Morphotype/figure
External diameter (nm)
RF-C 5A RF-D 5B
Wall thickness (nm)
Chambers hidden by surface ornamentation ~ 30
20–25
Square
200
50–60
45–55
Diamond, irregular
750–850
140–150
~ 20
15–25
Square to round, parallel to length
RF-J 5 K,L
500–550
200
RF-K 6A-C
500–750
150–200
Previous descriptions Group 1 Group 2 RF-A RF-B
of reticulate filaments 300–1000 300–1000 400–700 150–175 700–950
40–100 40–100 75–100
30–40 30–40 35–50
150–300
50–110
Distinctive feature
This paper This paper Mesh wall parallel to length forms discontinuous elevated ridge; not universally present Surface covered by ridges, 60–70 nm wide, discontinuous, slightly sinuous, spiral along length Continuous elevated ridge, 55–65 nm wide, spiral along length Surface ornamentation of straight to slightly curved, isolated spines up to 150 nm long Surface almost completely covered with short (~75 nm) blunt spines that are commonly linked to neighboring spine. Mesh only evident on interior wall of filament (Fig. 4J). Smooth outer surface with scattered pores (10–20 nm) that may be part of meshwork. Central mesh tube, encircled by regularly spaced discs (100 nm thick), small pillars (~25 nm diameter) between discs.
Hexagonal, parallel to length Diamond, spiral along length Hexagonal, spiral along length Rectangular to hexagonal, parallel to length
of open mesh, mesh pattern, thickness of mesh walls) that forms the filament walls (Table 1, Figs. 5 and 6). The morphological attributes of these filaments are considered to be taxa-specific because the different morphotypes, where intertwined with each other, each maintain their own characteristic features (Fig. 7). This would not be expected if the ornamentation reflected calcification patterns. Given that Jones (2009a) referred to two different forms as morphotypes RF-A and RF-B, the morphotypes from the Cayman terrestrial oncoids are herein labeled as RF-C to RF-K (Table 1, Figs. 5 and 6). 6.2. Large-diameter calcified filaments Calcified branching filaments, commonly N200 μm long, with an external diameter of up to 12 μm and an internal diameter of up to 10 μm, are common on some surfaces (Fig. 8A–F) but absent from most. The filament walls are formed of slightly elongate anhedral calcite crystals, up to 1 μm long, that generally have their long axis radiating outwards (Fig. 8C). The surfaces of the filaments are commonly coated with EPS, collapsed filamentous microbes, various types of reticulate filaments, various types of cocci, and detrital calcite, dolomite, and clay grains (Fig. 8A–F). The interior walls are smooth. 6.3. Large-diameter collapsed filaments These septate, non-branching filaments, 3.5 to 4 μm wide, commonly form bundles (Fig. 8G–I) that are very common on some growth surfaces in the terrestrial oncoids. Reticulate filaments, preserved in their 3-dimensional form are commonly found on the surfaces of these collapsed filaments. The filaments are covered, to varying degrees, by minimicrite and micrite that is formed of anhedral crystals (Fig. 8H and I). The calcite, which seems to have formed after collapse of the filaments, is highly variable in its distribution. Thus,
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Melim et al. (2008) Melim et al. (2008) Jones (2009a) Jones (2009a)
some parts of the filaments are devoid of calcite, other parts may only have a few scattered grains on their surface (Fig. 8H), and other filaments are almost completely encased with calcite (Fig. 8I). 6.4. Beaded filaments This filamentous microbe is the dominant microbe in some parts of the coated grains. At least 1 mm long, it is formed of linked “beads” that each have an external diameter of ~15 μm (Fig. 8J–L). Their calcified walls, at least 2 μm thick, seem to merge imperceptibly with the calcite of the surrounding groundmass (Fig. 8K). Individual “beads” are linked by a canal, ~1 μm in diameter, that is also encased by a calcitic wall (Fig. 8K). The “beads” are either hollow (Fig. 8J and K) or partly filled with small euhedral calcite crystals (Fig. 8L). 6.5. Cocci Numerous ovate to (sub)spherical cocci, 1–2 μm in diameter, are common throughout the cortices of the coated grains (Fig. 9). At least 20 different morphotypes (designated as C–A to C–T with prefix C indicating that they are coccus) are recognized based on their size, shape, surface ornamentation, and pores (Fig. 9). Some are spinose (Fig. 9B–E), some have smooth surfaces (Fig. 9F–H), whereas others are characterized by 30–50 nm diameter pores (Fig. 9J) that, in some morphotypes, are surrounded by a low rim (Fig. 9M and N) and/or spines (Fig. 9O). Repeated EDX analyses of numerous cocci indicate that they are calcified. That notion is supported by the three-dimensional form of the cocci with preservation of their delicate ornamentation (Fig. 9) and broken sections through them shows that they are formed of closely packed anhedral grains that are b50 nm long. Although the cocci are similar to spores in terms of their size and shape, they are unusual because (1) none are attached to filaments
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6.6. Sporangia-like structures Blister-like structures, up to 50 μm in diameter and 30 μm high, are commonly rooted on the surface or on growth surfaces in the coated grains (Fig. 10). Although the outer envelope is not always evident, the dense concentration of cocci in these small masses indicates that they may be sporangia. They typically contain one type of coccus (Fig. 10A–C), but some contain two or three different types of cocci and scattered filaments (Fig. 10D and E). Some of these microbes, however, may have been introduced after the sporangia-like structure had broken open. Many of the sporangia-like structures are characterized by (1) calcification of cocci (Fig. 10C and G), (2) precipitation of calcite between some of the cocci (Fig. 10B), and/or (3) calcite cements that partly to totally fill some of the cocci. The concentration of filamentous microbes around these sporangia-like structures suggests that the filamentous microbes may have used them as a food source.
6.7. Affinity of microbes
Fig. 6. SEM photomicrographs of reticulate filament RF-K (see Table 1 for descriptions). Repeated EDX analyses of many different specimens indicate that these filaments are calcified.
even though they are commonly found among the reticulate filaments and commonly have a main opening that could be interpreted as an attachment collar (Fig. 9B), (2) many of the cocci are rooted to the substrate by small strands (Fig. 9I, L, O and Q), and (3) the main opening is typically on top of the cocci and hence pointing away from the substrate (Fig. 9F–I and K). These cocci may be the basal spore of “spore chains” that once extended from the substrates; the implication being that all other “spores” in the original chain have broken away and dispersed. From the perspective of size, morphology, and ornamentation, it could be suggested that many of the cocci are related to the reticulate filaments that commonly occur around them. It is, however, impossible to verify this suggestion because none of them are connected to any of the filaments and there are no definitive morphological attributes that unequivocally allow attribution of the cocci to any of the filaments.
The reticulate filaments, by virtue of their perforate walls, are the most distinctive microbes associated with the Cayman terrestrial oncoids. RF-C, RF-D, and RF-G are akin to the “perforate filaments” and “spiral filament” described by Jones (1991, his Table 2 and Figs. 9E, 6B, 9F respectively). They are also comparable to reticulate filaments that Melim et al. (2008) described from speleothems found in many different caves throughout the world. Melim et al. (2008) divided these filaments into two morphotypes based largely on the filament diameter and the shape, size, and disposition of the openings in the meshwork structure. Jones (2009a) described two morphotypes (RF-A, RF-B) of reticulate filaments found in cave pearls from Old Man Village Cave on Grand Cayman. The nine morphotypes found in the terrestrial oncoids from Cayman Brac (Table 1) are different from those described by Melim et al. (2008) and Jones (2009a) with the possible exception of RF-C (Fig. 4A), which may be akin to RF-A of Jones (2009a). They are also similar to reticulate filaments found in stalactites and stalagmites that have grown in the wave-cut notch on Cayman Brac that is ~6 m above sea level and formed ~125,000 years ago (Jones, 2010b, his Fig. 11A–D). Clearly, the diversity of the reticulate filaments is far greater than that originally documented by Melim et al. (2008). Despite their distinctive morphology, the taxonomic affinity of these microbes remains open to debate. Melim et al. (2008) concluded that they probably belonged to an unknown group of microorganisms that prefer moist cave environments. Although the morphotypes documented herein do not provide any resolution to the issue of their taxonomic affinity, it does show that they are not restricted to caves.
Fig. 7. SEM photomicrographs showing different types of reticulate filaments intertwined with each other, indicating that their morphology and ornamentation are taxa-specific and not related to diagenetic overprinting.
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Fig. 8. SEM photomicrographs of large-diameter filamentous microbes associated with terrestrial oncoids. (A–F) Large-diameter bifurcating (arrow) calcified filament on surface of terrestrial oncoid (A, B). Walls formed of single layer (C) of radiating anhedral to subhedral calcite crystals (D), collapsed filamentous microbes (E), and detrital grains (F). (G–I) Collapsed large-diameter, non-branching, septate (arrows – H) filaments that are partly covered with micrite and minimicrite (H, I). (J–K) Large-diameter filament formed of connected “beads”. Fig. 8K shows connection between “beads” (arrows) and calcified walls. Hollow “beads” commonly partly filled with calcite cement (L).
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Fig. 9. SEM photomicrographs of cocci found on surface of terrestrial oncoids. Twenty different morphotypes (C–A to C–T) are defined by size, shape, ornamentation, and pores. Note that some cocci are “rooted” to the substrate with opening pointing away from substrate (e.g., Fig. 9I, O, Q). EDX analyses indicate that all cocci have been calcified.
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Fig. 10. SEM photomicrographs of sporangia-like structures found in terrestrial oncoids. (A) Ovate to round mass of cocci surrounded by micrite. W = gap once occupied by wall of sporangia-like structure. Box labeled B indicates position of Fig. 10B. (B) Group of calcified cocci from interior of structure shown in Fig. 10A. (C) Enlarged view of calcified coccus from sporangia-like structure. (D) Ovate mass of cocci (sporangia ?) in micrite groundmass. W = gap once occupied by wall of sporangia(?). (E) Calcified cocci from sporangia (?) shown in Fig. 10D. (F) Sporangia (?) holding group of smooth cocci. Box labeled G indicates position of Fig. 10G. (G) Broken coccus (see Fig. 10F), showing thin calcified wall and hollow interior. (H) Calcified cocci held in calcite cement that has filled a sporangia-like structure. Box labeled I indicates position of Fig. 10I. (I) Spar calcite cement encasing calcified coccus, from Fig. 10H.
Cocci are a common component of the Cayman terrestrial oncoids (Fig. 9). C–B (Fig. 9B) is morphologically akin to the “smooth spore with radiating spines” illustrated by Jones (1991, his Table 2 and Fig. 9E) whereas C–M (Fig. 9M) is similar to the “smooth spores with pores” illustrated by Jones (1991). Similarly, some of the cocci found in the terrestrial oncoids are morphologically akin to forms found in the notch speleothems on Cayman Brac (e.g., compare Fig. 9B and M of this paper with Jones, 2010b, his Figs, 11G, H, respectively) and cave speleothems from Old Man Village Cave on Grand Cayman (e.g., compare Fig. 9 of this paper with Jones, 2009b, his Fig. 8). Although it is not clear if these cocci are related to the reticular filaments it is interesting to note that this diverse arrays of cocci, with each morphotype characterized by distinctive ornamentation and/or pores, are invariably associated with the reticulate filaments found in cave pearls (Jones, 2009a), in notch speleothems (Jones, 2010c), and
in cave speleothems (Jones, 2010c). Many of the cocci are morphologically similar to the actinomycetid spores that are illustrated and described in the Digital Atlas of Actinomycetes (Miyadoh et al., 1997) and shown in SEM photomicrographs presented in other studies of these organisms (e.g., Tresner et al., 1961; Dietz and Mathews, 1969, 1971). 7. Interior cortical laminae The cortex interiors are formed largely of densely packed micrite and minimicrite that appears vaguely laminated when seen in thin section (Fig. 2D–G) but largely featureless when viewed on the SEM (Fig. 11). The micrite and minimicrite is formed of tightly interlocking anhedral calcite crystals that may, in part, be the result of recrystallization. Porosity is low, being restricted to submicron
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intercrystalline pores and scattered ovate to spherical pores that are similar in size and shape to many of the cocci found on the exterior of the coated grains (Fig. 11F). In some parts of the cortices there are spherical bodies, typically b1 μm in diameter, which may represent cocci (Fig. 11B–F). In rare examples, the presence of pores or other structures on the surfaces of these spherical bodies supports this notion (Fig. 11C). In most cases, however, the spherical grains are probably the internal moulds of cocci. Despite extensive searching, little or no trace of filamentous microbes were found in the interior parts of the cortices. The number of microbes evident in the cortex decreases with increasing distance from the surface of the coated grain. Examination of numerous cortices shows that the microbial layer that is rich in filaments and cocci is largely superficial. In most of the coated grains, preserved microbes (mainly cocci) are scattered throughout the outermost parts of the cortices (typically ~100 μm). Evidence of filamentous microbes in this zone is scant. Although impossible to determine with accuracy, the number of microbes evident in this outer zone is probably b5% of those found on the outer surfaces of the coated grains. In the innermost parts of the cortices, even fewer microbes are evident with widely scattered, poorly preserved cocci being present with no evidence of filaments. 8. Discussion Each of the terrestrial oncoids from Cayman Brac has a distinct nucleus encased by a finely crystalline calcite cortex that is formed largely of minimicrite and micrite, is only vaguely laminated, and lacks obvious biogenic features (Fig. 2C). High resolution, highmagnification SEM imaging, however, reveals a diverse microbiota (Figs. 5–9) dominated by cocci and filamentous microbes that are b1 μm in diameter (Figs. 5–9). Large-diameter calcified and collapsed
filaments (Fig. 8A–I), found only in a few laminae, form a minor part of the total biota. This biota is readily apparent on the outer surface of the terrestrial oncoids but hard to detect in the cortical lamina beneath the grain surfaces. The filamentous microbes, cocci, and their associated EPS contributed to the formation of these coated grains by binding material to the surfaces (Fig. 4), calcification of the microbes (Figs. 5, 6, 8A–F, 9 and 10), providing substrates on which calcite was later precipitated (Fig. 8G–I), and forming cavities in which calcite cement was precipitated (Fig. 8L). In addition, some of the particulate calcite in the cortices may have been derived from the breakdown of the calcified filaments and cocci. The terrestrial oncoids grew among plant roots in soil pockets that are housed in the finely crystalline dolostones of the Cayman Formation (Fig. 2A and B). Any model invoked to explain their genesis must acknowledge that (1) growth took place in the dark environments of the subsurface soil, (2) the zones between the terrestrial oncoids are filled with soil (Fig. 2B), (3) there was little free-flowing water (Fig. 2A and B), and (4) the oncoids seem to be stationary, being held in place by neighbouring oncoids, the soil matrix, and the plant roots (Fig. 2A and B). The fact that many of the larger terrestrial oncoids formed through the merger of smaller oncoids also indicates that they underwent little rotation or movement. Nevertheless, it is possible that growth of the plant roots, burrowing organisms (if present), and periods of exceptional high water flow after severe storms (e.g., hurricanes) may have caused some movement of individual oncoids. Irrespective of these nuances, the issue of growth space is important because the cavities between the coated grains are filled with soil, roots, and other debris (Fig. 2B). Thus, growth of the terrestrial oncoids could only be achieved if expansion caused displacement of matrix away from the growth surfaces, and/or the matrix material was assimilated into the cortical lamina. Although there is no direct evidence for displacement
Fig. 11. SEM photomicrographs showing fabrics in inner part of cortex of terrestrial oncoids. (A) Homogeneous cortex (C) with sharp boundary with dolomite (D) nucleus. Outer surface at top of image. (B) Dense, low porosity micrite in inner part of cortex with single possible coccus (arrow) evident. (C–E) Micrite with scattered spherical bodies that may be cocci (arrows). (F) Dense micrite with scattered pores that may be inherited from cocci.
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of the matrix during growth, the presence of small shell fragments, detrital dolomite grains, and coated micrograins (Fig. 2D–G) indicates that some of the matrix material was assimilated into the oncoids as they grew. Coated grains with cortices formed largely of micrite have been described from many successions, including those in Barbados (James, 1972; Harrison, 1977), Spain (Nagtegaal, 1969; Calvet and Julia, 1983), North Kentucky (Walls et al., 1975), South Africa (Siesser, 1973), and Florida (Coniglio and Harrison, 1983). In most cases, abiotic processes were deemed responsible for cortex formation. Calvet (1982), Calvet and Julia (1983), Wright (1989), and Jones (1991), however, argued that micritic cortical laminae commonly form through various biogenic processes. Each noted that the formative microbes, evidence of microbial calcification, and associated needle-fiber calcite crystals are most apparent in the outermost (i.e., youngest) layers. The inference is that direct evidence of the microbes is progressively lost as time passes and new cortical layers encase the grains. This is also apparent in the terrestrial oncoids from Cayman Brac with evidence of microbial activity being readily apparent on the outer surface, rarer in the outermost lamina (Figs. 5–10), and very scarce in the innermost lamina (Fig. 11). Such observations suggest that evidence of biogenicity may be progressively lost during early diagenesis due to (1) decay of the soft tissues of the microbes and/or EPS, (2) degradation and break up of calcified microbes, and/or (3) precipitation of calcite that gradually disguises and/or buries the microbes, even if calcified. In this context, scale is critically important because most of the microbes are b1 μm in diameter and hence become easily lost amid the surrounding micrite (1–4 μm) and minimicrite (b1 μm). Coated grains, irrespective of their place of origin, are morphologically unified by their simple internal structure wherein a nucleus is encased by a cortex. These grains grow in many disparate environments and it is becoming increasingly evident that a wide array of biogenic and abiogenic processes governs their genesis. This is especially true for coated grains that develop in terrestrial environments. The terrestrial oncoids from Cayman Brac are, for example, are superficially similar to cave pearls (up to 8 cm long) found in Old Man Village Cave on Grand Cayman (Fig. 1C). The cave pearls, described by Jones and MacDonald (1989) and Jones (2009a), have laminated cortices that are formed of prismatic calcite crystals that are up to 1 mm long, clusters of outward radiating columnar trigonal calcite crystals, crystal bushes, particulate calcite grains (detrital grains, fiber calcite crystals, calcified filaments, calcified cocci) up to 150 μm long (Jones, 2009a, his Figs. 3–5). The microbiota found in these cave pearls included four filamentous microbe morphotypes (including two reticulate filaments designated as morphotypes RF-A, RF-B), seven “spores” (morphotypes S1 to S7), and copious amounts of EPS (Jones, 2009a, his Figs. 6, 7). Although the fabrics and crystalline components of the terrestrial oncoids and the cave pearls are quite different, the microbiota are, in many respects, similar. Reticulate filaments are present in both and many of the cocci are morphologically identical. The terrestrial oncoids share some similarities with other types of speleothems found on Cayman Brac and Grand Cayman. Stalagmites and stalactites that adorn the wave-cut notch on Cayman Brac (Jones, 2010b), for example, are formed largely of micrite and minimicrite and contain a diverse microbiota that includes a diverse array of filamentous microbes, “spores”, and EPS (Jones, 2010b). Some of the reticulate filaments and spores in these notch speleothems are the same as those found in the terrestrial oncoids. Likewise, some of the “spores” found in stalactites in Old man Village Cave on Grand Cayman (Jones, 2009b) are morphologically similar to cocci found in the terrestrial oncoids. Comparison of the biotas found in the terrestrial oncoids with those found in cave pearls, notch speleothems, and cave speleothems shows that they share many elements in common, especially with respect to the reticulate filaments and the cocci. The widespread occurrences of these microbes may reflect microbes that (1) inhabit a wide range of habitats, or (2) live in one particular environment but
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are subsequently transported elsewhere by running water, wind, or animals. The latter possibility is certainly viable given that many of these microbes are b1 μm in diameter and hence easy to transport and move through even the smallest pore systems. Features that argue against significant transportation, however, include (1) long, delicate reticulate filaments that show little or no evidence of breakage or abrasion (Fig. 5), (2) filaments that are intricately entwined with each other and various components of their host substrate (Fig. 7), (3) cocci that are extremely well preserved with little or no evidence of abrasion or breakage (Fig. 9), and (4) copious amounts of EPS that coat the host substrates and are intimately associated with the filaments and/or cocci (Fig. 4A, C and F). The fact that many of these microbes are found in the terrestrial oncoids, the notch speleothems, and the cave speleothems suggests that they are capable of living in many different environments. It must be stressed, however, that this does not preclude the possibility that some transportation has taken place, as examples of broken filaments and cocci are present in some of the oncoids and speleothems. 9. Conclusions A detailed analysis of large terrestrial oncoids that have grown among plant roots in some of the soil-filled pockets found on Cayman Brac leads to the following important conclusions. • Each coated grain has a distinct nucleus that is enveloped by a vaguely laminated, thin cortex that is formed largely of micrite and minimicrite. • The surfaces of the coated grains are covered with a diverse array of reticulate filaments and cocci that are typically b1 μm in diameter, some large-diameter collapsed and calcified filaments, sporangialike structures, and in some areas, thin coatings of EPS. • The microbes on the surface of the coated grains promoted growth by binding grains to their surfaces, calcification of the microbes, providing substrates on which calcite was precipitated, and forming cavities in which calcite cement was later precipitated. • Many microbes found in the terrestrial oncoids are morphologically similar to microbes found in other terrestrial carbonates, including notch speleothems, cave stalactites and stalagmites, and cave pearls found elsewhere on Grand Cayman and Cayman Brac. • The subsurface cortical laminae appear to be abiogenic in origin because they contain only scattered cocci and virtually no evidence of filamentous microbes. It appears, however, that most of the formative microbes were destroyed during diagenesis. • The terrestrial oncoids provide yet another example of the complex and multifaceted processes that microbes mediate in the development of coated grains. • Evidence for the biogenicity of coated grains can commonly be difficult to detect, especially if early diagenesis disguises their presence or destroys them. Acknowledgements I am grateful to the Natural Sciences and Engineering Research Council of Canada, which funded this study (grant A6090), Hendrik van Genderen of the Water Authority of the Cayman Islands who helped me in the field, and George Braybrook (University of Alberta), who took the SEM photomicrographs used in this study. I am also indebted to Drs. Ana Alonso-Zarza and Michal Gradzinski who provided critical and thought provoking reviews of an earlier version of this manuscript. References Calvet, F., 1982. Constructive micrite envelope developed in vadose continental environment in Pleistocene eolianites of Mallorca (Spain). Acta Geologica Hispánica 17, 169–178.
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Calvet, F., Julia, R., 1983. Pisoids in the caliche profiles of Tarragona, north east Spain. In: Peryt, T.M. (Ed.), Coated Grains. Springer-Verlag, Berlin, pp. 456–473. Coniglio, M., Harrison, R.S., 1983. Facies and diagenesis of Late Pleistocene carbonates from Big Pine Key, Florida. Bulletin of Canadian Petroleum Geology 31, 135–147. Dietz, A., Mathews, J., 1969. Scanning electron microscopy of selected members of the Streptomyces hygroscopicus group. Applied Microbiology 18, 694–696. Dietz, A., Mathews, J., 1971. Classification of Strepomyces spore surfaces into five groups. Applied Microbiology 21, 527–533. Flügel, E., 1982. Microfacies Analysis of Limestones. Springer-Verlag, Berlin. 633 pp. Folk, R.L., 1974. The natural history of crystalline calcium carbonate: effect of magnesium content and salinity. Journal of Sedimentary Petrology 44, 40–53. Guo, L., Riding, R., 1994. Origin and diagenesis of Quaternary travertine shrub fabrics, Rapolano Terme, central Italy. Sedimentology 41, 499–520. Harrison, R.S., 1977. Caliche profiles: indicators of near-surface subaerial diagenesis, Barbados, West Indies. Bulletin of Canadian Petroleum Geology 25, 123–173. James, N.P., 1972. Holocene and Pleistocene calcareous crust (caliche) profiles: criteria for subaerial exposure. Journal of Sedimentary Petrology 42, 817–836. Jones, B., 1991. Genesis of terrestrial oncoids, Cayman Islands, British West Indies. Canadian Journal of Earth Sciences 28, 382–397. Jones, B., 1994. Geology of the Cayman Islands. In: Brunt, M.A., Davies, J.E. (Eds.), The Cayman Islands: Natural History and Biogeography. Kluwer, Dordrecht, The Netherlands, pp. 13–49. Jones, B., 2009a. Cave pearls — the integrated product of abiogenic and biogenic processes. Journal of Sedimentary Research 79, 689–710. Jones, B., 2009b. Mineralized actinomycetes and phosphates in speleothems from Grand Cayman, British West Indies. Sedimentary Geology 219, 302–317. Jones, B., 2010a. The preferential association of dolomite with microbes in stalactites from Cayman Brac, British West Indies. Sedimentary Geology 226, 94–109. Jones, B., 2010b. Speleothems in a wave-cut notch, Cayman Brac, British West Indies: The integrated product of subaerial preciptiation, dissolution, and microbes. Sedimentary Geology 232, 15–34. Jones, B., 2010c. Microbes in caves: agents of calcite corrosion and precipitation. In: Pedley, H.M., Rogerson, M. (Eds.), Tufas and Speleothems: Unravelling the Microbial and Physical Controls: Geological Society of London, Special Publications, v. 36, pp. 7–30. London, England. Jones, B., MacDonald, R.W., 1989. Micro-organisms and crystal fabrics in cave pisoliths from Grand Cayman, British West Indies. Journal of Sedimentary Petrology 59, 387–396.
Melim, L.A., Northup, D.E., Spilde, M.N., Jones, B., Boston, P.J., Bixby, R.J., 2008. Reticulated filaments in cave pool speleothems: microbe or mineral? Journal for Cave and Karst Studies 70, 135–141. Melim, L.A., Liescheidt, R., Northup, D.E., Spilde, M.N., Boston, P.J., Queen, J.M., 2009. A biosignature suite form cave pool precipitates, Cottonwood Cave, New Mexico. Astrobiology 9, 907–917. Miyadoh, S., Tsuchizaki, N., Ishikawa, J., Hotta, K. (Editors), 1997. Digital Atlas of Actinomycetes. Society for Actinomycetes Japan, Akasura Publishing, Tokyo, Japan, 244 pp. Nagtegaal, P.J.C., 1969. Microtextures in recent and fossil caliche. Leidse Geologische Medelingen 42, 131–142. Peryt, T.M., 1983a. Coated Grians. Springer-Verlag, Berlin. Peryt, T.M., 1983b. Classification of Coated Grains. In: Peryt, T.M. (Ed.), Coated Grains. Springer-Verlag, Berlin, pp. 3–6. Peryt, T.M., 1983c. Vadoids. In: Peryt, T.M. (Ed.), Coated Grains. Springer-Verlag, Berlin Heidelberg, pp. 437–449. Reid, R.P., MacIntyre, I.G., 1998. Carbonate recrystallization in shallow marine environments: a widespread diagenetic process forming micritized grains. Journal of Sedimentary Research 68, 928–946. Riding, R., 1979. Origin and diagenesis of lacustrine algal bioherms at the margin of the Ries crater, Upper Miocene, southern Germany. Sedimentology 26, 645–680. Riding, R., 1983. Cyanoliths (Cyanoids) oncoids formed by calcified cyanophytes. In: Peryt, T.M. (Ed.), Coated Grains. Springer Verlag, Berlin, Heidelberg, pp. 277–283. Siesser, W.G., 1973. Diagenetically formed ooids and intraclasts in south African calcretes. Sedimentology 20, 539–551. Tresner, H.D., Davies, M.C., Backus, E.J., 1961. Electron microscopy of Streptomycetes spore morphology and its role in species differentiation. Journal of Bacteriology 81, 70–80. Walls, R.A., Harris, W.B., Nunam, W.E., 1975. Calcareous crusts (caliche) profiles and early subaerial exposure of carboniferous carbonates, northeastern Kentucky. Sedimentology 22, 417–440. Wright, V.P., 1989. Terrestrial stromatolites and laminar calcretes: a review. Sedimentary Geology 65, 1–13. Wright, V.P., 2008. Calcrete. In: Nash, D.J., McLaren, S.J. (Eds.), Geochemical Sediments and Landscapes. John Wiley & Sons, Chichester, England, pp. 10–45. Zhou, J., Chafetz, H.S., 2009. Biogenic caliches in Texas: the role of organisms and climate. Sedimentary Geology 222, 207–225.
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Sedimentary Geology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / s e d g e o
Biogenicity of terrestrial oncoids formed in soil pockets, Cayman Brac, British West Indies Brian Jones Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, Alberta, Canada, T6G 2E3
a r t i c l e
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Article history: Received 21 September 2010 Received in revised form 29 November 2010 Accepted 23 December 2010 Available online 7 January 2011 Editor: M.R. Bennett Keywords: Terrestrial oncoids Microbes Micrite Coated grains Reticulate filaments
a b s t r a c t Terrestrial oncoids, up to 85 mm long, are common in some of the soil-filled pockets found in the finely crystalline dolostones of the Cayman Formation on Cayman Brac. Each of these coated grains has a nucleus formed of a white, finely crystalline dolostone lithoclast (derived from the Cayman Formation) that is encased by a light brown to tan cortex that is formed largely of micrite and minimicrite, is vaguely laminated, and lacks obvious biogenic structures. The cortex, typically b 10 mm thick, is variable in thickness around individual grains and from grain to grain. On the surfaces of the oncoids there is a diverse microbiota that includes various reticulate filaments that are typically b 1 μm in diameter, cocci, some large-diameter collapsed and calcified filaments, sporangia-like structures, and locally, exopolysaccharides (EPS). In the subsurface parts of the cortices, however, filaments are very rare and there are only scattered cocci. Evidence derived from the surface microbes indicates that they played an active role in the growth of the cortical laminae by binding material to their surfaces, calcification of the microbes, providing substrates on which calcite was precipitated, and forming cavities in which calcite cement was later precipitated. In stark contrast, it is difficult to ascribe a biotic influence to the formation of the subsurface laminae because of the paucity of preserved microbes. The lack of microbes, however, probably reflects the fact that the formative microbes were destroyed during diagenesis. This example clearly demonstrates that the lack of preserved microbes cannot be taken as an indication that the grains formed as a result of abiogenic processes. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Microbes are mystical organisms that seem to have an influence on carbonate precipitation and accretion that is out of all proportion to their size. Nowhere is this more apparent than in the terrestrial realm where coated grains that form in many different settings, have been ascribed to various abiogenic and/or biogenic processes (Calvet, 1982; Calvet and Julia, 1983; Wright, 1989; Jones, 1991). Although microbes have clearly influenced the growth and development of some of these grains, others have cortices that appear structureless and devoid of any organic components. The biogenicity of coated grains is a critical issue because it has commonly been used as a basis for classification. Peryt (1983a, his Table 2), for example, used biogenicity as one of the main criteria for classifying coated grains and the names of different types of coated grains commonly reflect the principle microbe involved in their formation (e.g., Riding, 1983). It is commonly difficult, however, to locate microbes in the very fine-grained calcitic cortices of terrestrial/ pedogenic coated grains, especially if they are only assessed through low-magnification microscopy (Wright, 1989; Jones, 1991). Thus, such grains are commonly considered abiogenic — a decision that automatically influences their classification and notions regarding their origin.
E-mail address: [email protected]. 0037-0738/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.sedgeo.2010.12.009
This paper focuses on coated grains, up to 85 mm long, that are found in soil pockets in the finely crystalline dolostones (Cayman Formation) that form the land surface on the eastern part of Cayman Brac (Figs. 1 and 2). Although their nuclei and cortices are obvious (Fig. 2C), their cortices appear structureless and devoid of microbes when viewed at low-magnification (Fig. 2C and D). At high magnification, however, it becomes readily apparent that microbes are common on the oncoids surfaces and played a formative role in the growth and development of the cortical laminae. In contrast, the cortical laminae beneath the surface of the coated grains contain very few microbes and hence appear to be abiogenic in origin — a conclusion that is diametrically opposite to that derived from examination of the surface microbial mats. Such a contrast is of critical importance given that the issue of biogenicity is central to most classification systems (e.g., Peryt, 1983b) of coated grains. Accordingly, this study focuses on the Cayman coated grains with the view of explaining the dichotomy in the distribution of the microbes and the impact that that may have on the classification and interpretation of coated grains. 2. Terminology Many different names have been assigned to coated grains that have formed in terrestrial/pedogenic settings, including vadoids
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Fig. 1. Location maps. (A) Location of Cayman Brac (CB) in Caribbean Sea. (B) Geological map of Cayman Brac (Jones, 1994, his Fig. 2.3D) showing location where samples were collected (NRC) on Ann Tatum Road.
(Peryt, 1983c), pedogenic coated grains (Wright, 1989), terrestrial oncoids (Wright, 1989; Jones, 1991), and pisoids/ooids (Wright, 2008; Zhou and Chafetz, 2009). Selecting the most appropriate term for the Cayman coated grains is fraught with problems because many of these terms have inherent generic connotations or have been used without definition and therefore simply reflect the bias of the individual researcher. Herein the term “terrestrial oncoids” is applied to the Cayman coated grains because they conform to Wright's (1989) original definition of “…laminated, microbially formed structures that occur in vadose settings, either forming at the atmosphere-soil or sediment or rock interface, or within soil profiles”. As such they are a type of pedogenic coated grain, commonly found in calcrete soils, that are characterized by multiple coats of micrite (Wright, 1989). The microbes found in the Cayman terrestrial oncoids are herein described as filaments and cocci (spherical forms) with no implied taxonomic or genetic implications. The term “micrite” has been applied to carbonate crystals 1–4 μm long and “minimicrite” to carbonate grains b1 μm long (Folk, 1974; Reid and MacIntyre, 1998). Riding (1979), however, applied the term “minimicrite” to grains 0.2–1.0 μm long, Flügel (1982) used the term for grains b2 μm long, and Guo and Riding (1994) reserved it for grains b0.1 μm long. In this study, the terms “micrite” (1–4 μm) and “minimicrite” (b1 μm) are used as first defined by Folk (1974). 3. Geological setting Cayman Brac, the smallest of the Cayman Islands, has a core formed of Tertiary carbonates with an upper surface that slopes from a maximum elevation of ~40 m at its east end to sea level at its west end (Fig. 1). Limestones of the Ironshore Formation (Pleistocene), which onlap an erosional bench cut into the Tertiary carbonates, forms a flat apron along the south, west, and north coasts of the island. The Tertiary carbonates, which dip to the west at ~ 0.5° (Jones, 1994), belong to the Bluff Group that is formed of the Brac Formation (Lower Oligocene), the Cayman Formation (Upper Miocene), and the Pedro Castle Formation (Lower Pliocene). The coated grains, which are the focus of this study, came from an outcrop on Ann Tatum Road, which is located on the northeast side of Cayman Brac (Fig. 1B).
Construction of the road in 2008 provided clean, fresh sections through the white, finely crystalline dolostones of the Cayman Formation that forms the land surface in that area at an elevation of ~30 above sea level (Fig. 2A). Before construction of the road, the area was covered with a dense natural vegetation of tropical trees, bushes, and ground creepers that were rooted in potholes and root cavities that are filled with soil (Fig. 2A). The densely packed coated grains, of variable size and shape, were found in the soil pockets that are up to 0.5 m in diameter and up to 3 m deep and contain numerous roots (Fig. 2A and B). It should be noted, however, that the soil pockets (1) are highly variable in diameter and depth, (2) commonly merge or bifurcate below ground, and (3) have highly irregular walls. The poorly lithified soil is formed of red to dark brown clays that are mixed with biofragments (largely derived from land snails), and irregular fragments of dolostone that came from the surrounding bedrock. Given that the coated grains were collected only a few months after the rock, terra rossa, and coated grains had been exposed, there had had been little time for tropical weathering to modify them. 4. Methodology Large (7.5 × 5.0 cm) thin sections were made from three of the terrestrial oncoids so that their internal structures could be determined. Scanning electron microscope (SEM) analyses were conducted on a JOEL Field Emission SEM (JOEL 6301FE). An accelerating voltage of 5 kV was used for imaging because this is the optimal setting for high-resolution images. SEM samples were carefully extracted from the terrestrial oncoids with note being made of their location and orientation in the cortices. The samples were mounted on SEM stubs using double-sided tape and/or silver conductive glue. Samples were sputter coated with a very thin layer of gold or chrome prior to being examined on the SEM. This study is based largely on 845 SEM photomicrographs that were obtained from the terrestrial oncoids. Energy-dispersive X-ray (EDX) analyses were done using the Princeton Gamm-Tech X-ray analysis system that is attached to the SEM. These analyses were conducted with an accelerating voltage of 20 kV using the minimum beam diameter possible. Some analytical
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Fig. 2. Photographs of coated grains. (A) Outcrop showing white dolostones of upper part of Cayman Formation with pockets of soil in which trees and bushes (removed during road construction) were rooted. White letter B indicates position of Fig. 2B. (B) Terrestrial oncoids held in loose matrix amid root system. (C) Polished cross-sections through terrestrial oncoid showing nuclei formed of white fossilifereous dolostone derived from the Cayman Formation coated with light to dark orange cortex. (D, E) Thin section photomicrographs showing cortical laminae formed of micrite and scattered detrital grains of dolomite (white). Note vaguely defined laminae and Mn precipitates (arrows). Blue area is epoxy covering outside of grain. (F, G) Laminae in interior of cortices formed of small coated grains, micrite, and patches of calcite cement. Some coated grains have distinct nuclei formed of detrital dolomite/calcite (white) grains whereas others appear to be formed entirely of micrite.
problems were encountered because the volume of material analyzed (~1 μm3) is commonly larger than the diameter of the microbes being analyzed. Thus, the beam may penetrate through the microbes and detect elements that are located in the background or to one side of the object being analyzed. These problems were overcome by analyzing clusters of microbes rather than single filaments or cocci,
and/or obtaining separate analyses of microbes and their underlying substrate so that the exact location of the elements detected by EDX analysis could be determined. Any questionable analyses were disregarded. Adobe Photoshop CS © was used to adjust the brightness and contrast of the digital field, thin section, and SEM images.
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5. Terrestrial oncoids — morphology The terrestrial oncoids, which have a dull, light to medium brown surface color (Fig. 2B), are 7 to 85 mm long, 7 to 82 mm wide, and 5 to 44 mm high (Fig. 3). The small (b1 cm) coated grains are typically spherical whereas the larger grains range from elongate cylinders to large, flat, plate-like forms. The cortices are thin (typically b20%, rarely to 40%, of grain radius) and irregularly developed around the grain with one side commonly being two to three times the thickness on the other side (Fig. 2C). As such they are equivalent to the “superficial pisoids” of Zhou and Chafetz (2009). Many of the larger, highly irregular oncoids formed through the amalgamation of numerous smaller grains. They are akin to the “compound pisoids of Zhou and Chafetz (2009). 5.1. Nucleus Cross-sections through the terrestrial oncoids shows that each has a large nucleus that is encased by a thin, vaguely laminated cortex (Fig. 2C). The irregular-shaped nuclei are formed of white, finely crystalline fossilifereous dolostone that came from the Cayman Formation (Fig. 2A) of the surrounding bedrock (Fig. 2C). 5.2. Cortex The cream to light orange colored cortex contrasts sharply with the white dolostone nuclei (Fig. 2C). Vaguely defined laminae are highlighted by slight variations in color and/or disseminated black, Mn-rich precipitates. The cortices are formed largely of very finely crystalline calcite (minimicrite/micrite) along with minor amounts of clay, dolomite, and Mn oxides (Fig. 2C and D). Thin section analysis shows that the cortices are characterized by (1) dense, dark-colored
micrite with vaguely defined laminae that are evident because of slight color variations and/or minor concentrations of small detrital grains (Fig. 2D), (2) small (b0.1 mm long) detrital dolomite and/or calcite crystals concentrated in some laminae (Fig. 2E), (3) small (b0.5 mm long) biofragments, derived from gastropod shells, and (4) small, round to ovate coated grains that are ~0.1 mm diameter (Fig. 2F and G). Each of the micro-coated-grains has a well-defined nucleus that is encased by a cortex formed of micrite (Fig. 2F and G). Some nuclei are formed of detrital calcite or dolomite grains whereas others are formed of micrite that is slightly different in color from the surrounding cortex (Fig. 2F and G). In effect, these grains are miniature versions of the large coated grains. 5.3. Surface topography The surfaces of the terrestrial oncoids are irregular with elevated mounds and ridges separated by valleys (Figs. 2B and 4A and B). There is no pattern to the size, shape, or distribution of these features and there are no indications that one side developed in preference to another. The summits of the elevated areas are typically smooth and disrupted by desiccation cracks (Fig. 4C). Thin (b1 μm thick) mats, which appear to be calcified exopolysacchrides (EPS) films, overlie detrital calcite and dolomite grains, micrite, calcified filaments, and cocci that are commonly infused with EPS (Fig. 4D). Textural relationships indicate that the mats bound loose sediment to the surface of the coated grain. The valleys between the topographic highs are characterized by small (b0.1 mm diameter), loosely packed coated grains (Fig. 4B, E andF), micrite (Fig. 4G), filamentous microbes (Fig. 4E and H), detrital calcite and dolomite grains that are commonly encased with micrite (Fig. 4I and J), cocci, and sporangia. Patches of EPS are found throughout these areas and locally, there are secondary Mn-oxide precipitates (Figs. 2E and F and 4K). In many areas, filamentous microbes lie under and on top of these Mn precipitates (Fig. 4K). There is no pattern to the distribution of these components. 6. Terrestrial oncoids — biota
Fig. 3. Bivariant graphs for terrestrial oncoids showing relationship between (A) length and width, and (B) length and height. Dashed line indicates 1:1 ratio.
The surfaces of the terrestrial oncoids are populated by a diverse array of microbes (Figs. 5–10) that are highly variable in terms of their preservation. Some are completely collapsed with no evidence of any mineralization whereas others have been fully calcified. Determining if a microbe has been calcified posed significant problems because they are commonly b1 μm in diameter, and detection of light elements, including C, on the SEM system used is difficult. With these caveats in mind, however, determination of microbe mineralization was based on (1) whether or not the microbe was collapsed, (2) detection of elements in the microbe by EDX analysis, with such analyses being preferentially located in areas where there were intertwined filaments or clusters of cocci provide larger target areas for analysis, (3) the presence of C peaks on the EDX diffractograms, where evident, (4) the presence/absence of crystals, and/or (5) how the microbes react when the electron beam is placed on their surfaces — non-mineralization forms will commonly expand and burst open as the electron beam is placed on their surfaces (Melim et al., 2009; Jones, 2010a). Collectively, these features provide a very good indication of the preservation state of the microbes. Partly desiccated threads of EPS can produce structures that mimic filamentous microbes. Herein, tube-like structures were deemed to be filamentous microbes if (1) their diameter was relatively constant along their length and from specimen to specimen, (2) there was no evidence of distortion due to desiccation, and (3) they had the appearance of filaments as opposed to dried and curled EPS. Conversely, “filaments” were considered to be desiccated EPS if (1) curled edges were readily apparent, (2) there was radical changes in diameters along their length, and/or (3) their morphology was
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Fig. 4. SEM photomicrographs showing main features on exterior of terrestrial oncoids. (A) General view showing elevated smooth area, covered with EPS, surrounded by lower areas covered with porous, granular material. (B) Low-lying area covered with loosely bound grains of various sizes and shaped and filamentous microbes. (C) Smooth, desiccated EPS on surface of elevated area (from Fig. 4A). (D) Micrite and minimicrite that lies just beneath the EPS layer shown in Fig. 4C. (E) Loose grain on surface of coated grain (from area like that shown in Fig. 4B) coated with micrite, EPS, and filamentous microbes. Box labeled F indicates position of Fig. 4F. (F) Enlarged view from Fig. 4E showing EPS covering surface of grain. (G) Micrite and minimicrite coating surface of loose grain. (H) Filamentous microbes and micrite on surface of loose grain. (I, J) Small grains (boundaries indicated by arrows) partly coated with micrite and microbes (see Fig. 2F, G). (K) Mn-oxide precipitate (arrows) coating substrate. Note associated filamentous microbes and cocci.
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Fig. 5. SEM photomicrographs of reticulate filaments RF-C to J (see Table 1 for descriptions). Repeated EDX analyses of many different specimens indicate that these filaments are calcified.
inconsistent along their length or between specimens that were located close to each other. The microbial biota found on the surfaces of the terrestrial oncoids is divided into the (1) reticulate filaments, b1 μm in diameter, with walls characterized by a meshwork structure (Figs. 5–7), (2) large-diameter calcified filaments, up to 10 μm in diameter (Fig. 8A–F), (3) largediameter (3.5–4.0 μm wide, in flattened form), septate collapsed filaments that are partly calcified (Fig. 8G–I), (4) filamentous microbes formed of linked beads, up to 15 μm external diameter, with calcified walls (Fig. 8J–L), and (5) spherical to ovate cocci (Fig. 9), some of which are held in sporangia-like structures (Fig. 10).
6.1. Reticulate filaments These non-branching and possible septate filaments, typically b1 μm in diameter and commonly N500 μm long (Figs. 5–7), have walls formed of an open meshwork (Melim et al., 2008; Jones, 2009a). EDX analyses consistently showed that they are formed of Ca that is presumed to be in the form of calcite. The appearance of the filaments, their 3-dimensional form, and the paucity of collapsed forms support this suggestion (Figs. 5–7). The reticulate filaments are divided into nine different types based on their external diameter, surface ornamentation, and morphology of the meshwork (shape and size
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Table 1 Summary descriptions of reticulate filaments found in terrestrial oncoids from Cayman Brac with comparisons to previously described reticulate filaments. Mesh opening (nm)
Mesh wall thickness (nm)
Chamber shape and arrangement
500–700 350–450
60–70 40–50
60–70 40–60
RF-E 5 C
500–600
40–50
40–50
Diamond, spiral along length Rounded diamond, spiral along length Square, parallel to length
RF-F 5D
550–650
RF-G 5E,F
400–450
RF-H 5 G,H
750–850
RF-I 5I,J
Morphotype/figure
External diameter (nm)
RF-C 5A RF-D 5B
Wall thickness (nm)
Chambers hidden by surface ornamentation ~ 30
20–25
Square
200
50–60
45–55
Diamond, irregular
750–850
140–150
~ 20
15–25
Square to round, parallel to length
RF-J 5 K,L
500–550
200
RF-K 6A-C
500–750
150–200
Previous descriptions Group 1 Group 2 RF-A RF-B
of reticulate filaments 300–1000 300–1000 400–700 150–175 700–950
40–100 40–100 75–100
30–40 30–40 35–50
150–300
50–110
Distinctive feature
This paper This paper Mesh wall parallel to length forms discontinuous elevated ridge; not universally present Surface covered by ridges, 60–70 nm wide, discontinuous, slightly sinuous, spiral along length Continuous elevated ridge, 55–65 nm wide, spiral along length Surface ornamentation of straight to slightly curved, isolated spines up to 150 nm long Surface almost completely covered with short (~75 nm) blunt spines that are commonly linked to neighboring spine. Mesh only evident on interior wall of filament (Fig. 4J). Smooth outer surface with scattered pores (10–20 nm) that may be part of meshwork. Central mesh tube, encircled by regularly spaced discs (100 nm thick), small pillars (~25 nm diameter) between discs.
Hexagonal, parallel to length Diamond, spiral along length Hexagonal, spiral along length Rectangular to hexagonal, parallel to length
of open mesh, mesh pattern, thickness of mesh walls) that forms the filament walls (Table 1, Figs. 5 and 6). The morphological attributes of these filaments are considered to be taxa-specific because the different morphotypes, where intertwined with each other, each maintain their own characteristic features (Fig. 7). This would not be expected if the ornamentation reflected calcification patterns. Given that Jones (2009a) referred to two different forms as morphotypes RF-A and RF-B, the morphotypes from the Cayman terrestrial oncoids are herein labeled as RF-C to RF-K (Table 1, Figs. 5 and 6). 6.2. Large-diameter calcified filaments Calcified branching filaments, commonly N200 μm long, with an external diameter of up to 12 μm and an internal diameter of up to 10 μm, are common on some surfaces (Fig. 8A–F) but absent from most. The filament walls are formed of slightly elongate anhedral calcite crystals, up to 1 μm long, that generally have their long axis radiating outwards (Fig. 8C). The surfaces of the filaments are commonly coated with EPS, collapsed filamentous microbes, various types of reticulate filaments, various types of cocci, and detrital calcite, dolomite, and clay grains (Fig. 8A–F). The interior walls are smooth. 6.3. Large-diameter collapsed filaments These septate, non-branching filaments, 3.5 to 4 μm wide, commonly form bundles (Fig. 8G–I) that are very common on some growth surfaces in the terrestrial oncoids. Reticulate filaments, preserved in their 3-dimensional form are commonly found on the surfaces of these collapsed filaments. The filaments are covered, to varying degrees, by minimicrite and micrite that is formed of anhedral crystals (Fig. 8H and I). The calcite, which seems to have formed after collapse of the filaments, is highly variable in its distribution. Thus,
Reference
This paper
This paper
This paper This paper This paper
This paper This paper
Melim et al. (2008) Melim et al. (2008) Jones (2009a) Jones (2009a)
some parts of the filaments are devoid of calcite, other parts may only have a few scattered grains on their surface (Fig. 8H), and other filaments are almost completely encased with calcite (Fig. 8I). 6.4. Beaded filaments This filamentous microbe is the dominant microbe in some parts of the coated grains. At least 1 mm long, it is formed of linked “beads” that each have an external diameter of ~15 μm (Fig. 8J–L). Their calcified walls, at least 2 μm thick, seem to merge imperceptibly with the calcite of the surrounding groundmass (Fig. 8K). Individual “beads” are linked by a canal, ~1 μm in diameter, that is also encased by a calcitic wall (Fig. 8K). The “beads” are either hollow (Fig. 8J and K) or partly filled with small euhedral calcite crystals (Fig. 8L). 6.5. Cocci Numerous ovate to (sub)spherical cocci, 1–2 μm in diameter, are common throughout the cortices of the coated grains (Fig. 9). At least 20 different morphotypes (designated as C–A to C–T with prefix C indicating that they are coccus) are recognized based on their size, shape, surface ornamentation, and pores (Fig. 9). Some are spinose (Fig. 9B–E), some have smooth surfaces (Fig. 9F–H), whereas others are characterized by 30–50 nm diameter pores (Fig. 9J) that, in some morphotypes, are surrounded by a low rim (Fig. 9M and N) and/or spines (Fig. 9O). Repeated EDX analyses of numerous cocci indicate that they are calcified. That notion is supported by the three-dimensional form of the cocci with preservation of their delicate ornamentation (Fig. 9) and broken sections through them shows that they are formed of closely packed anhedral grains that are b50 nm long. Although the cocci are similar to spores in terms of their size and shape, they are unusual because (1) none are attached to filaments
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6.6. Sporangia-like structures Blister-like structures, up to 50 μm in diameter and 30 μm high, are commonly rooted on the surface or on growth surfaces in the coated grains (Fig. 10). Although the outer envelope is not always evident, the dense concentration of cocci in these small masses indicates that they may be sporangia. They typically contain one type of coccus (Fig. 10A–C), but some contain two or three different types of cocci and scattered filaments (Fig. 10D and E). Some of these microbes, however, may have been introduced after the sporangia-like structure had broken open. Many of the sporangia-like structures are characterized by (1) calcification of cocci (Fig. 10C and G), (2) precipitation of calcite between some of the cocci (Fig. 10B), and/or (3) calcite cements that partly to totally fill some of the cocci. The concentration of filamentous microbes around these sporangia-like structures suggests that the filamentous microbes may have used them as a food source.
6.7. Affinity of microbes
Fig. 6. SEM photomicrographs of reticulate filament RF-K (see Table 1 for descriptions). Repeated EDX analyses of many different specimens indicate that these filaments are calcified.
even though they are commonly found among the reticulate filaments and commonly have a main opening that could be interpreted as an attachment collar (Fig. 9B), (2) many of the cocci are rooted to the substrate by small strands (Fig. 9I, L, O and Q), and (3) the main opening is typically on top of the cocci and hence pointing away from the substrate (Fig. 9F–I and K). These cocci may be the basal spore of “spore chains” that once extended from the substrates; the implication being that all other “spores” in the original chain have broken away and dispersed. From the perspective of size, morphology, and ornamentation, it could be suggested that many of the cocci are related to the reticulate filaments that commonly occur around them. It is, however, impossible to verify this suggestion because none of them are connected to any of the filaments and there are no definitive morphological attributes that unequivocally allow attribution of the cocci to any of the filaments.
The reticulate filaments, by virtue of their perforate walls, are the most distinctive microbes associated with the Cayman terrestrial oncoids. RF-C, RF-D, and RF-G are akin to the “perforate filaments” and “spiral filament” described by Jones (1991, his Table 2 and Figs. 9E, 6B, 9F respectively). They are also comparable to reticulate filaments that Melim et al. (2008) described from speleothems found in many different caves throughout the world. Melim et al. (2008) divided these filaments into two morphotypes based largely on the filament diameter and the shape, size, and disposition of the openings in the meshwork structure. Jones (2009a) described two morphotypes (RF-A, RF-B) of reticulate filaments found in cave pearls from Old Man Village Cave on Grand Cayman. The nine morphotypes found in the terrestrial oncoids from Cayman Brac (Table 1) are different from those described by Melim et al. (2008) and Jones (2009a) with the possible exception of RF-C (Fig. 4A), which may be akin to RF-A of Jones (2009a). They are also similar to reticulate filaments found in stalactites and stalagmites that have grown in the wave-cut notch on Cayman Brac that is ~6 m above sea level and formed ~125,000 years ago (Jones, 2010b, his Fig. 11A–D). Clearly, the diversity of the reticulate filaments is far greater than that originally documented by Melim et al. (2008). Despite their distinctive morphology, the taxonomic affinity of these microbes remains open to debate. Melim et al. (2008) concluded that they probably belonged to an unknown group of microorganisms that prefer moist cave environments. Although the morphotypes documented herein do not provide any resolution to the issue of their taxonomic affinity, it does show that they are not restricted to caves.
Fig. 7. SEM photomicrographs showing different types of reticulate filaments intertwined with each other, indicating that their morphology and ornamentation are taxa-specific and not related to diagenetic overprinting.
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Fig. 8. SEM photomicrographs of large-diameter filamentous microbes associated with terrestrial oncoids. (A–F) Large-diameter bifurcating (arrow) calcified filament on surface of terrestrial oncoid (A, B). Walls formed of single layer (C) of radiating anhedral to subhedral calcite crystals (D), collapsed filamentous microbes (E), and detrital grains (F). (G–I) Collapsed large-diameter, non-branching, septate (arrows – H) filaments that are partly covered with micrite and minimicrite (H, I). (J–K) Large-diameter filament formed of connected “beads”. Fig. 8K shows connection between “beads” (arrows) and calcified walls. Hollow “beads” commonly partly filled with calcite cement (L).
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Fig. 9. SEM photomicrographs of cocci found on surface of terrestrial oncoids. Twenty different morphotypes (C–A to C–T) are defined by size, shape, ornamentation, and pores. Note that some cocci are “rooted” to the substrate with opening pointing away from substrate (e.g., Fig. 9I, O, Q). EDX analyses indicate that all cocci have been calcified.
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Fig. 10. SEM photomicrographs of sporangia-like structures found in terrestrial oncoids. (A) Ovate to round mass of cocci surrounded by micrite. W = gap once occupied by wall of sporangia-like structure. Box labeled B indicates position of Fig. 10B. (B) Group of calcified cocci from interior of structure shown in Fig. 10A. (C) Enlarged view of calcified coccus from sporangia-like structure. (D) Ovate mass of cocci (sporangia ?) in micrite groundmass. W = gap once occupied by wall of sporangia(?). (E) Calcified cocci from sporangia (?) shown in Fig. 10D. (F) Sporangia (?) holding group of smooth cocci. Box labeled G indicates position of Fig. 10G. (G) Broken coccus (see Fig. 10F), showing thin calcified wall and hollow interior. (H) Calcified cocci held in calcite cement that has filled a sporangia-like structure. Box labeled I indicates position of Fig. 10I. (I) Spar calcite cement encasing calcified coccus, from Fig. 10H.
Cocci are a common component of the Cayman terrestrial oncoids (Fig. 9). C–B (Fig. 9B) is morphologically akin to the “smooth spore with radiating spines” illustrated by Jones (1991, his Table 2 and Fig. 9E) whereas C–M (Fig. 9M) is similar to the “smooth spores with pores” illustrated by Jones (1991). Similarly, some of the cocci found in the terrestrial oncoids are morphologically akin to forms found in the notch speleothems on Cayman Brac (e.g., compare Fig. 9B and M of this paper with Jones, 2010b, his Figs, 11G, H, respectively) and cave speleothems from Old Man Village Cave on Grand Cayman (e.g., compare Fig. 9 of this paper with Jones, 2009b, his Fig. 8). Although it is not clear if these cocci are related to the reticular filaments it is interesting to note that this diverse arrays of cocci, with each morphotype characterized by distinctive ornamentation and/or pores, are invariably associated with the reticulate filaments found in cave pearls (Jones, 2009a), in notch speleothems (Jones, 2010c), and
in cave speleothems (Jones, 2010c). Many of the cocci are morphologically similar to the actinomycetid spores that are illustrated and described in the Digital Atlas of Actinomycetes (Miyadoh et al., 1997) and shown in SEM photomicrographs presented in other studies of these organisms (e.g., Tresner et al., 1961; Dietz and Mathews, 1969, 1971). 7. Interior cortical laminae The cortex interiors are formed largely of densely packed micrite and minimicrite that appears vaguely laminated when seen in thin section (Fig. 2D–G) but largely featureless when viewed on the SEM (Fig. 11). The micrite and minimicrite is formed of tightly interlocking anhedral calcite crystals that may, in part, be the result of recrystallization. Porosity is low, being restricted to submicron
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intercrystalline pores and scattered ovate to spherical pores that are similar in size and shape to many of the cocci found on the exterior of the coated grains (Fig. 11F). In some parts of the cortices there are spherical bodies, typically b1 μm in diameter, which may represent cocci (Fig. 11B–F). In rare examples, the presence of pores or other structures on the surfaces of these spherical bodies supports this notion (Fig. 11C). In most cases, however, the spherical grains are probably the internal moulds of cocci. Despite extensive searching, little or no trace of filamentous microbes were found in the interior parts of the cortices. The number of microbes evident in the cortex decreases with increasing distance from the surface of the coated grain. Examination of numerous cortices shows that the microbial layer that is rich in filaments and cocci is largely superficial. In most of the coated grains, preserved microbes (mainly cocci) are scattered throughout the outermost parts of the cortices (typically ~100 μm). Evidence of filamentous microbes in this zone is scant. Although impossible to determine with accuracy, the number of microbes evident in this outer zone is probably b5% of those found on the outer surfaces of the coated grains. In the innermost parts of the cortices, even fewer microbes are evident with widely scattered, poorly preserved cocci being present with no evidence of filaments. 8. Discussion Each of the terrestrial oncoids from Cayman Brac has a distinct nucleus encased by a finely crystalline calcite cortex that is formed largely of minimicrite and micrite, is only vaguely laminated, and lacks obvious biogenic features (Fig. 2C). High resolution, highmagnification SEM imaging, however, reveals a diverse microbiota (Figs. 5–9) dominated by cocci and filamentous microbes that are b1 μm in diameter (Figs. 5–9). Large-diameter calcified and collapsed
filaments (Fig. 8A–I), found only in a few laminae, form a minor part of the total biota. This biota is readily apparent on the outer surface of the terrestrial oncoids but hard to detect in the cortical lamina beneath the grain surfaces. The filamentous microbes, cocci, and their associated EPS contributed to the formation of these coated grains by binding material to the surfaces (Fig. 4), calcification of the microbes (Figs. 5, 6, 8A–F, 9 and 10), providing substrates on which calcite was later precipitated (Fig. 8G–I), and forming cavities in which calcite cement was precipitated (Fig. 8L). In addition, some of the particulate calcite in the cortices may have been derived from the breakdown of the calcified filaments and cocci. The terrestrial oncoids grew among plant roots in soil pockets that are housed in the finely crystalline dolostones of the Cayman Formation (Fig. 2A and B). Any model invoked to explain their genesis must acknowledge that (1) growth took place in the dark environments of the subsurface soil, (2) the zones between the terrestrial oncoids are filled with soil (Fig. 2B), (3) there was little free-flowing water (Fig. 2A and B), and (4) the oncoids seem to be stationary, being held in place by neighbouring oncoids, the soil matrix, and the plant roots (Fig. 2A and B). The fact that many of the larger terrestrial oncoids formed through the merger of smaller oncoids also indicates that they underwent little rotation or movement. Nevertheless, it is possible that growth of the plant roots, burrowing organisms (if present), and periods of exceptional high water flow after severe storms (e.g., hurricanes) may have caused some movement of individual oncoids. Irrespective of these nuances, the issue of growth space is important because the cavities between the coated grains are filled with soil, roots, and other debris (Fig. 2B). Thus, growth of the terrestrial oncoids could only be achieved if expansion caused displacement of matrix away from the growth surfaces, and/or the matrix material was assimilated into the cortical lamina. Although there is no direct evidence for displacement
Fig. 11. SEM photomicrographs showing fabrics in inner part of cortex of terrestrial oncoids. (A) Homogeneous cortex (C) with sharp boundary with dolomite (D) nucleus. Outer surface at top of image. (B) Dense, low porosity micrite in inner part of cortex with single possible coccus (arrow) evident. (C–E) Micrite with scattered spherical bodies that may be cocci (arrows). (F) Dense micrite with scattered pores that may be inherited from cocci.
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of the matrix during growth, the presence of small shell fragments, detrital dolomite grains, and coated micrograins (Fig. 2D–G) indicates that some of the matrix material was assimilated into the oncoids as they grew. Coated grains with cortices formed largely of micrite have been described from many successions, including those in Barbados (James, 1972; Harrison, 1977), Spain (Nagtegaal, 1969; Calvet and Julia, 1983), North Kentucky (Walls et al., 1975), South Africa (Siesser, 1973), and Florida (Coniglio and Harrison, 1983). In most cases, abiotic processes were deemed responsible for cortex formation. Calvet (1982), Calvet and Julia (1983), Wright (1989), and Jones (1991), however, argued that micritic cortical laminae commonly form through various biogenic processes. Each noted that the formative microbes, evidence of microbial calcification, and associated needle-fiber calcite crystals are most apparent in the outermost (i.e., youngest) layers. The inference is that direct evidence of the microbes is progressively lost as time passes and new cortical layers encase the grains. This is also apparent in the terrestrial oncoids from Cayman Brac with evidence of microbial activity being readily apparent on the outer surface, rarer in the outermost lamina (Figs. 5–10), and very scarce in the innermost lamina (Fig. 11). Such observations suggest that evidence of biogenicity may be progressively lost during early diagenesis due to (1) decay of the soft tissues of the microbes and/or EPS, (2) degradation and break up of calcified microbes, and/or (3) precipitation of calcite that gradually disguises and/or buries the microbes, even if calcified. In this context, scale is critically important because most of the microbes are b1 μm in diameter and hence become easily lost amid the surrounding micrite (1–4 μm) and minimicrite (b1 μm). Coated grains, irrespective of their place of origin, are morphologically unified by their simple internal structure wherein a nucleus is encased by a cortex. These grains grow in many disparate environments and it is becoming increasingly evident that a wide array of biogenic and abiogenic processes governs their genesis. This is especially true for coated grains that develop in terrestrial environments. The terrestrial oncoids from Cayman Brac are, for example, are superficially similar to cave pearls (up to 8 cm long) found in Old Man Village Cave on Grand Cayman (Fig. 1C). The cave pearls, described by Jones and MacDonald (1989) and Jones (2009a), have laminated cortices that are formed of prismatic calcite crystals that are up to 1 mm long, clusters of outward radiating columnar trigonal calcite crystals, crystal bushes, particulate calcite grains (detrital grains, fiber calcite crystals, calcified filaments, calcified cocci) up to 150 μm long (Jones, 2009a, his Figs. 3–5). The microbiota found in these cave pearls included four filamentous microbe morphotypes (including two reticulate filaments designated as morphotypes RF-A, RF-B), seven “spores” (morphotypes S1 to S7), and copious amounts of EPS (Jones, 2009a, his Figs. 6, 7). Although the fabrics and crystalline components of the terrestrial oncoids and the cave pearls are quite different, the microbiota are, in many respects, similar. Reticulate filaments are present in both and many of the cocci are morphologically identical. The terrestrial oncoids share some similarities with other types of speleothems found on Cayman Brac and Grand Cayman. Stalagmites and stalactites that adorn the wave-cut notch on Cayman Brac (Jones, 2010b), for example, are formed largely of micrite and minimicrite and contain a diverse microbiota that includes a diverse array of filamentous microbes, “spores”, and EPS (Jones, 2010b). Some of the reticulate filaments and spores in these notch speleothems are the same as those found in the terrestrial oncoids. Likewise, some of the “spores” found in stalactites in Old man Village Cave on Grand Cayman (Jones, 2009b) are morphologically similar to cocci found in the terrestrial oncoids. Comparison of the biotas found in the terrestrial oncoids with those found in cave pearls, notch speleothems, and cave speleothems shows that they share many elements in common, especially with respect to the reticulate filaments and the cocci. The widespread occurrences of these microbes may reflect microbes that (1) inhabit a wide range of habitats, or (2) live in one particular environment but
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are subsequently transported elsewhere by running water, wind, or animals. The latter possibility is certainly viable given that many of these microbes are b1 μm in diameter and hence easy to transport and move through even the smallest pore systems. Features that argue against significant transportation, however, include (1) long, delicate reticulate filaments that show little or no evidence of breakage or abrasion (Fig. 5), (2) filaments that are intricately entwined with each other and various components of their host substrate (Fig. 7), (3) cocci that are extremely well preserved with little or no evidence of abrasion or breakage (Fig. 9), and (4) copious amounts of EPS that coat the host substrates and are intimately associated with the filaments and/or cocci (Fig. 4A, C and F). The fact that many of these microbes are found in the terrestrial oncoids, the notch speleothems, and the cave speleothems suggests that they are capable of living in many different environments. It must be stressed, however, that this does not preclude the possibility that some transportation has taken place, as examples of broken filaments and cocci are present in some of the oncoids and speleothems. 9. Conclusions A detailed analysis of large terrestrial oncoids that have grown among plant roots in some of the soil-filled pockets found on Cayman Brac leads to the following important conclusions. • Each coated grain has a distinct nucleus that is enveloped by a vaguely laminated, thin cortex that is formed largely of micrite and minimicrite. • The surfaces of the coated grains are covered with a diverse array of reticulate filaments and cocci that are typically b1 μm in diameter, some large-diameter collapsed and calcified filaments, sporangialike structures, and in some areas, thin coatings of EPS. • The microbes on the surface of the coated grains promoted growth by binding grains to their surfaces, calcification of the microbes, providing substrates on which calcite was precipitated, and forming cavities in which calcite cement was later precipitated. • Many microbes found in the terrestrial oncoids are morphologically similar to microbes found in other terrestrial carbonates, including notch speleothems, cave stalactites and stalagmites, and cave pearls found elsewhere on Grand Cayman and Cayman Brac. • The subsurface cortical laminae appear to be abiogenic in origin because they contain only scattered cocci and virtually no evidence of filamentous microbes. It appears, however, that most of the formative microbes were destroyed during diagenesis. • The terrestrial oncoids provide yet another example of the complex and multifaceted processes that microbes mediate in the development of coated grains. • Evidence for the biogenicity of coated grains can commonly be difficult to detect, especially if early diagenesis disguises their presence or destroys them. Acknowledgements I am grateful to the Natural Sciences and Engineering Research Council of Canada, which funded this study (grant A6090), Hendrik van Genderen of the Water Authority of the Cayman Islands who helped me in the field, and George Braybrook (University of Alberta), who took the SEM photomicrographs used in this study. I am also indebted to Drs. Ana Alonso-Zarza and Michal Gradzinski who provided critical and thought provoking reviews of an earlier version of this manuscript. References Calvet, F., 1982. Constructive micrite envelope developed in vadose continental environment in Pleistocene eolianites of Mallorca (Spain). Acta Geologica Hispánica 17, 169–178.
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