The preferential association of dolomite with microbes in stalactites from Cayman Brac, British West Indies

Sedimentary Geology 226 (2010) 94–109

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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

The preferential association of dolomite with microbes in stalactites from 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 31 October 2009 Received in revised form 25 February 2010 Accepted 5 March 2010 Available online 15 May 2010 Communicated by G.J. Weltje Keywords: Caves Stalactites Microbes Dolomite Calcite Aragonite

a b s t r a c t Nani Cave, located in dolostones of the Cayman Formation (Miocene) on Cayman Brac, contains numerous stalactites that are formed largely of aragonite and calcite along with lesser amounts of calcium-rich dolomite, gypsum, and minor amounts of Mg–Si needles. Morphologically, the dolomite is divided into blocky, filamentous mat, crust, and “beehive” types whereas the gypsum is divided into the tabular and sheet types. A diverse array of filamentous microbes and spores (probably actinomycetids) and their associated exopolysaccharides (EPS) are unevenly distributed throughout the stalactites. Although microbes are commonly present on the surfaces of the calcite and aragonite crystals, none were found inside these crystals. Similarly, no microbes were found with the gypsum. The common association of the dolomite and the Mg–Si needles with the microbes and their EPS suggests that the microbes played a formative role in the precipitation of the dolomite and Mg–Si needles. The intimate association of microbes and dolomite in these stalactites has significant implications for the origin of dolomite under low-temperature and low-pressure conditions. © 2010 Elsevier B.V. All rights reserved.

1. Introduction The vast array of minerals found in speleothems (Hill and Forti, 1997) is testimony to the variable hydrochemical conditions found in caves. Temporal changes in the mineralogy and/or crystal morphologies of stalactites have typically been attributed to variations in the composition of the cave waters and/or the physiochemical conditions in the cave (Fischbeck and Müller, 1971; Bar-Matthews et al., 1991). Even though caves are inhabited by diverse microbial biotas (e.g., Barton et al., 2001; Jones, 2001; Barton and Jurado, 2007; Barton and Northup, 2007; Jones, in press), the roles that they may play in the precipitation of the diverse and ever-changing spelean mineral/ crystal assemblages are commonly ignored. Many stalactites from Nani Cave on Cayman Brac (Figs. 1 and 2) are formed of aragonite, calcite, dolomite, gypsum, and Mg–Si needles along with a diverse microbial biota and exopolysaccharides (EPS) that are mineralized to varying degrees. Today, the cave is dry and it is therefore impossible to assess the chemical composition of the waters from which these minerals were precipitated. Thus, the relationships between the minerals and the microbes must be assessed by examining the distribution patterns, at the micron to sub-micron scale, of the (1) minerals and different crystal forms, (2) diagenetic fabrics, and (3) microbes and their associated EPS. These analyses show critical associations between minerals, crystal forms, and

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microbes and highlight the close association between dolomite and the Mg–Si needles with the microbes and their associated EPS. 2. Geological setting The stalactites used in this study came from Nani Cave on Cayman Brac, which is located ∼20 m above sea level (Fig. 1B). It has been little disturbed by people since being discovered in 2006. The cave, ∼ 50 m long, ∼ 25 wide, and up to 7 m high, is developed in finely-crystalline dolostones of the Cayman Formation (Jones, 1994). The rock above the cave, no more than 3 m thick, has a phytokarsted surface with sharp pinnacles and ridges around depressions and potholes that are commonly filled with terra rossa. There is a dense vegetation cover with plants being rooted in the soils that fill the depressions and potholes. Tarhule-Lips (1999) divided the caves on Cayman Brac into the “notch caves” and the “upper caves” according to their elevations relative to the distinctive Sangamon wave-cut notch that is located 6 m above sea level. The “notch caves”, located at or close to the wavecut notch, formed 1400 to 400 ka, whereas the “upper caves”, located at various elevations above the notch, are thought to have formed during the Late Tertiary to early Quaternary. Nani Cave belongs to the “upper caves” as defined by Tarhule-Lips (1999). The incredible arrays of stalactites, stalagmites, columns, and flowstone clearly attest to the large volumes of water that once flowed through the Nani Cave (Fig. 2). Today, however, there is no evidence of any water flow or dripping through this cave and it is therefore

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Fig. 1. Location of Nani Cave. (A) Map showing location of Cayman Brac in Caribbean Sea. (B) Geological map of Cayman Brac (modified from Jones, 1994, his Fig. 2.3D) showing location of Nani Cave, developed in Cayman Formation in the central part of the island. (C) Cross-section through Cayman Brac (modified from Jones, 1994, his Fig. 2.7), from North East Point to West end Point showing location of cave.

impossible to obtain water samples for analysis. Although other caves on Cayman Brac lack flowing water, Tarhule-Lips and Ford (2004) provided analyses of drip waters and condensation waters from those caves (Table 1). Based on these data, Tarhule-Lips and Ford (2004) showed that these waters had variable Mg and Ca concentrations and ranged from being undersaturated to saturated with respect to both calcite and dolomite (Table 1). Thus, some waters have the potential of dissolving calcite and dolomite whereas calcite and/or dolomite may be precipitated from other waters. 3. Methodology The morphology and distribution of the minerals in the stalactites from Nani Cave were initially established from two thin sections (one transverse and one parallel to long axis) that were made from one stalactite that was carefully collected from the roof of the cave. Collection of stalactites was restricted in order to minimize damage to the cave. Small fracture samples were carefully extracted from the stalactites with note being made of their locations and orientations so that (1) their mineralogical composition could be assessed by X-ray diffraction (XRD) analysis, (2) high resolution, high-magnification images could be obtained on the scanning electron microscope (SEM), and (3) the elemental content of selected spots could be obtained by energy-dispersive X-ray analysis (EDX) on the SEM. In some cases, the sample was first analyzed on the SEM and then subjected to XRD analysis. Although this process meant that the SEM sample was destroyed it did ensure that the XRD analysis came from the sample studied on the SEM rather than from another sample that may or may not be formed of exactly the same minerals. XRD analyses, using a quartz plate, were done using a Rigaku Geigerflex sealed-tube X-ray generator with a Co tube, run at 40 kV and 35 mA. The samples used for SEM analyses were mounted on stubs using double-sided tape and/or silver conductive glue, depending on the size and nature of the sample. Samples were sputter coated with a very thin layer of gold prior to being examined on a JOEL Field Emission SEM (JOEL 6301FE) with an accelerating voltage of 5 kV,

which is optimal for obtaining high-magnification images. Some images were taken while using an accelerating voltage of 20 kV so that the precise location of each EDX analysis could be recorded. 701 SEM photomicrographs were used in this study. Elemental content was determined from energy-dispersive X-ray (EDX) analyses obtained from the Princeton Gamm-Tech X-ray analysis system that is attached to the SEM. Analyses were obtained at an accelerating voltage of 20 kV using a beam diameter of ∼ 1 µm, which is the minimum size that can be used with this system. This posed some problems for analyses because this beam size is typically larger than the microbes being analyzed. Furthermore, the penetration depth of the beam means that some of the detected elements may be located in the background or to one side of the object being analyzed. These potential problems were overcome by (1) analyzing clusters of microbes rather than single filaments or spores, (2) ensuring that the thickest part of any given coating was analyzed, with preference being given to those areas that were N1 µm thick, and/or (3) undertaking separate analyses of coatings and the substrate that they covered in order to pinpoint the exact location of the elements detected by EDX analysis. In addition, 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. 4. Results 4.1. Stalactite structure The stalactites are formed of alternating light brown crystalline laminae, up to 5 mm thick, and white laminae b2 mm thick (Fig. 3). Concentric laminae formed primarily of calcite and aragonite (Fig. 3) encase the central, open soda-straw. Corrosion surfaces, which separate some of the laminae, are characterized by (1) irregular surface topography, (2) solution-widened boundaries between neighbouring calcite crystals, (3) concentrations of microbes, and (4) concentrations of finely-crystalline precipitates (cf. Jones, 2009b).

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Fig. 2. Speleothems in Nani Cave, Cayman Brac. (A) General view of stalactites, columns, and stalagmites. (B) Column (right side), flowstone on channel floor (lower left), and numerous stalactites. (C) Ceiling with numerous stalactites. (D) Cave ceiling with numerous, closely packed stalactites — with soda-straw visible in many of them.

In the outermost part of the stalactite, clusters of radiating aragonite crystals are intercalated with trigonal, prismatic calcite crystals (Fig. 3A, B). The aragonite crystal bundles, up to 3 mm long and 2.5 mm in diameter, are formed of elongate aragonite crystals, up to 2 mm long but b0.1 mm wide (Fig. 3A). There is no readily discernable pattern to the distribution of these clusters (Fig. 3A). Trigonal prismatic calcite crystals, up to 1 mm long and 0.2 mm wide, commonly encase the aragonite clusters (Fig. 3B). The boundaries between the aragonite and calcite crystals are sharp and there is no textural evidence to indicate that the calcite formed by aragonite inversion (Fig. 3B). In the older, interior parts of the stalactite, large

calcite crystals commonly encase the aragonite clusters (Fig. 3D). In those situations, however, the textural features indicate that most, if not all, of the aragonite has inverted to calcite. Such features include ghost-like aragonite crystals that are poorly defined when viewed in plane polarized light and, the lack of clearly defined aragonite crystals when viewed in crossed-polarized light (compare Fig. 3D and B). 4.2. Microbes The microbial mats, primarily associated with the white laminae in the stalactite, are formed of filaments, spores, and EPS. Most microbes

Table 1 Chemical analyses of drip and condensate waters from various caves on Cayman Brac. Data from Tarhule-Lips and Ford (1998, Table 1). Sample Cave

Total Ca (mmol/l)

Saturation index for calcite

Saturation index for dolomite

Min

Mean

Max

Min

Total Mg (mmol/l) Mean

Max

Min

Mean

Max

Min

Mean

Max

Rainwater Drip water Peter's Cave Tibbetts Turn Cave Cross Island Road Cave Skull Cave Rebecca's Cave Bats Cave Great Cave Condensation water Peter's Cave Tibbetts Turn Cave Great Cave

0.01

0.03

0.04

0.0

0.0

0.01

− 4.22

− 3.59

− 2.80

− 6.68

− 6.68

− 8.62

0.46 0.48 0.23 0.07 0.66 0.42 0.56

0.76 0.85 0.76 0.65 0.71 1.38 0.73

1.24 1.10 2.09 2.01 0.77 2.67 1.04

0.30 0.14 0.14 0.00 0.02 0.17 0.33

0.60 0.41 0.34 0.31 0.15 0.50 0.58

0.85 0.65 0.71 1.12 0.29 1.19 1.03

− 0.27 − 0.13 − 0.51 − 1.58 − 0.08 − 0.11 0.06

− 0.02 0.17 0.12 − 0.22 0.19 0.46 0.19

0.30 0.46 0.95 1.05 0.42 1.07 0.40

− 0.50 − 0.51 − 0.47 − 2.76 − 0.89 − 0.43 0.18

0.11 0.23 0.19 − 0.56 − 0.30 0.71 0.49

0.67 0.88 1.67 1.79 0.64 1.83 1.04

0.24 0.41 0.44

0.43 1.16 1.25

0.55 2.94 3.32

0.00 0.00 0.18

0.03 0.22 0.30

0.08 0.42 0.46

− 0.97 − 1.06 − 0.77

− 0.77 0.50 0.04

− 0.46 0.31 0.77

− 2.53 − 2.87 − 1.69

− 1.09 − 1.18 − 0.26

− 1.97 − 0.17 0.58

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Fig. 3. Thin section photomicrographs showing main components of stalactites from Nani Cave, Cayman Brac. A) Outermost part of stalactite showing clusters of aragonite needles intercalated with calcite crystals. White letter B indicates position of panel B. B) Interface between aragonite needles and calcite crystals. C) Aragonite and calcite crystals coated with dark brown to black precipitate. D) Interior part of stalactite showing clusters of aragonite needles (arrows) embedded in large calcite crystals. Textural features indicate that aragonite is inverting to calcite.

are well preserved with their three-dimensional form and surface ornamentation readily apparent (Fig. 4). Some microbes, however, are partly collapsed due to desiccation. Six microbe morphotypes (M1– M6, defined if numerous specimens displayed the same morphological attributes — Jones, 2009a) were recognized. Many of these microbes are morphologically similar to the microbes found in stalactites from other caves on Grand Cayman and Cayman Brac (see Jones, 1995, 2009a,b). As with those microbes, the six microbial morphotypes found in the stalactite from Nani Cave are morphologically similar to actinomycetes illustrated and described in the Digital Atlas of Actinomycetes (Miyadoh et al., 1997) and SEM photomicrographs presented in other studies of these organisms (e.g., Tresner et al., 1961; Dietz and Mathews, 1969, 1971). Given that these microbes are probably actinomycetids, the term hyphae is used to describe the filamentous forms.

Recognition of hyphae as opposed to partly desiccated threads of EPS can be difficult. In this study, structures were regarded as hyphae if (a) their diameter was relatively constant along their length and from hyphae to hyphae, (b) there was no clear evidence of distortion due to desiccation, and (c) they had the appearance of hyphae as opposed to dried and curled EPS. In some cases, the problem of recognizing hyphae was exacerbated by the fact that EPS partly covered some of the hyphae masses (e.g., Fig. 4A, B). Some “filamentous” forms were deemed to be partly desiccated EPS if (a) curled edges were readily apparent, (b) their diameters changed radically along their length and/or if the diameters varied significantly from “filament” to “filament”, and (c) there was no consistency in their morphology. Preservation of the microbes is highly variable; some appear to be formed largely of organic material whereas others have been partly or

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Fig. 4. SEM photomicrographs of microbes (morphotypes M1 to M6) associated with stalactite from Nani Cave, Cayman Brac. A, B) Morphotype M1 with three-dimensional array of branching hyphae covered with EPS. C) M1 hyphae with lateral nodes of spores/branches. D–F) M2 with branching hyphae with longitudinal surface striations. Many hyphae are partly collapsed. G) M3 with mat formed of three-dimensional branching hyphae that encase large spores. H) M3 with isolated specimen of M4, which is a smooth spore. I) Septate (?) and spiral M3 hyphae. J, K) M5 with ornate, spiral hyphae. L) Bacteriform M6 with cell division.

fully mineralized. This problem is compounded by (1) the sub-micron size of the microbes, which is less than the 1 µm beam size used during EDX analysis, and (2) the difficulty in detecting light elements,

including C, on the SEM system used in this study. Assessment of the mineralization of the microbes was based on (1) whether or not the microbe was collapsed, (2) detection of elements, such as Ca and Mg,

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in the microbe by EDX analysis, with great care being taken to ensure that such analyses were not detecting elements in background substrates, (3) the presence of C peaks on the EDX diffractograms, where evident, (4) the presence/absence of crystals, and/or (5) how the microbes reacted 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. Collectively, these features provide a very good indication of the preservation state of the microbes. 4.2.1. Morphotype M1 With hyphae ∼ 200 nm in diameter, this branching microbe forms a three-dimensional meshwork that is commonly covered with EPS (Fig. 4A, B). Individual hyphae commonly extend across the substrate from the main meshwork. Small nodes of curled hyphae/ spores that commonly arise from the sides or the ends of such hyphae (Fig. 4C) may be the formative stage of the hyphal networks (Fig. 4A). This microbe is similar to morphotype H1 that Jones (2009b, his Fig. 5A–I) described from stalactites found in Old Man Village Cave on Grand Cayman. The microbes from Nani Cave, however, generally have more associated EPS than those found in the Old Man Village cave. This difference may, however, be largely a function of preservation. 4.2.2. Morphotype M2 These branching hyphae, up to 500 nm in diameter, form dense, three-dimensional networks (Fig. 4D–F). Many hyphae are slightly deflated due to desiccation and their exteriors have a wrinkled appearance with minute ridges that parallel the length of the hyphae (Fig. 4E, F). Locally, spore-like bodies up to 1.5 µm long, with wrinkled exteriors, are associated with the hyphae (Fig. 4F). Some of these microbes are covered by mats formed of M1. 4.2.3. Morphotype M3 The branching hyphae, up to 250 µm in diameter, form threedimensional arrays (Fig. 4G–I). Some hyphae appear septate whereas others seem to spiral slightly (Fig. 4I). Spores, 2–8 µm in diameter, that are commonly enmeshed in tangled hyphal masses (Fig. 4G–H), have distinctive surfaces formed of randomly interwoven fibrils that are b50 nm in diameter (Fig. 4H). Thin layers of EPS coat some spores. The recurring association of these spores and hyphae suggests that they may be related even though there is no obvious connection between them (Fig. 4H). Although superficially akin to M1, M3 lacks the copious amounts of EPS that is typically found with M1, commonly enmeshes large spores that are not found with M1, and lacks the lateral and terminal nodes of contorted hyphae/spores found with M1 (Fig. 4C). 4.2.4. Morphotype M4 These smooth spores, up to 5 µm in diameter and commonly found with M3 (Fig. 4G), occur singularly or in pairs, with some being partly collapsed. There is no indication that they are genetically related to M3. Although morphologically akin to microbe S3 that Jones (2009a, his Fig. 8I) found in cave pearls in the Old Man Village Cave on Grand Cayman, this microbe is slightly smaller. The paucity of distinct morphological features precludes a definitive assessment of their similarity. 4.2.5. Morphotype M5 The hyphae of this microbe, up to 300 nm in diameter, are wound into a tight coil that is up to 800 nm in diameter (Fig. 4J). The hyphae are covered with small nodes that are ∼50 nm in diameter (Fig. 4K). Their consistent morphology and distribution on the same specimen

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and between different specimens indicates that they are a feature of the original microbe, not artifacts of mineral precipitation. This microbe has also been found in the biofilm that covers the walls in the twilight zone of Old Man Village Cave (Jones, 1995, his Fig. 2K, L). 4.2.6. Morphotype M6 This bacilliform microbe, up to 750 nm long and 300 nm in diameter, reproduces through binary fission (Fig. 4L). It has a smooth exterior and is commonly embedded in EPS that coats the crystal surfaces (Fig. 4L). 4.3. Mineralogy X-ray diffraction analyses of small samples extracted from the outermost white laminae of the stalactite showed that it is formed of aragonite, calcite, gypsum, and Ca-rich dolomite (Fig. 5). SEM and EDX analyses confirm the presence of these minerals and also revealed the presence of Mg–Si needles that were not detected by XRD analysis. 4.3.1. Aragonite and calcite Distinguishing between aragonite and calcite on the SEM is, by necessity, based solely on crystal form (Figs. 5 and 6). The aragonite crystals, up to 500 µm long and b25 µm wide, form radiating bundles up to 200 µm wide (Fig. 6A–E). Each crystal has a (sub)hexagonal cross-section. The aragonite crystals seem to merge, almost imperceptibly, with the larger calcite crystals that are up to 750 µm long and 250 µm wide, that are formed of subcrystals (Fig. 6). Many calcite crystals are characterized by well defined, crystallographically controlled etch zones (Fig. 6A, F, H). Transitions from aragonite to calcite and from calcite to aragonite are evident laterally along and across individual laminae (Figs. 3A, B, 5A, B, and 6A, B). The calcite crystals in the outer part of the stalactite are considered to be products of direct precipitation as they do not exhibit any textures indicative of formation through aragonite inversion (cf. Rehman et al., 1994). 4.3.2. Dolomite X-ray diffraction analysis shows that these stalactites contain Carich dolomite (Fig. 5C). On the SEM, dolomite was identified through EDX analyses that produced high-Mg and Ca peaks that are consistent with those obtained from dolomite. These analyses also showed that other elements, such as Fe, were not present. The dolomite is divided into four morphological types (Figs. 7–9). The “blocky dolomite” is characterized by systematically arranged subcrystals that are up to 2 × 2 × 2 µm (commonly b1 × 1 × 1 µm) in size, exhibit smooth faces, and have sharp crystal edges formed by the crystal faces that are at ∼90° to each other (Fig. 7A–E). Some of the larger subcrystals may have formed through the merger of smaller subcrystals. The subcrystals are systematically arranged so that their crystal faces are consistently oriented, possibly in directions that define cleavage (Fig. 7A–E). Many subcrystal faces are covered with microbial mats that are formed of interwoven, branching fibrils, 25– 50 nm in diameter, and EPS (Fig. 7F, G). Concentrations of these mats between neighbouring subcrystals give the junction a rounded appearance rather than the sharp junction that would be expected where two subcrystals intersect (Fig. 7C, D). Locally, bacilliform microbes (M6) lie on the biofilm (Fig. 7H). The “dolomitized mats” are formed of branching hyphae (morphotype M1?), 250–500 nm in diameter, and their associated EPS. Although crystalline dolomite was not evident, numerous EDX analyses of these mineralized mats consistently yielded high Ca and Mg peaks that are consistent with dolomite or high-calcium dolomite (Fig. 8A–I). No Mg was detected in the underlying substrate. In some of the larger calcite crystals, which are devoid of microbes, there are

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Fig. 5. SEM photomicrographs and XRD analysis of laminae from the outer part of stalactite from Nani Cave, Cayman Brac. A) SEM photomicrograph of laminae showing blocky calcite crystals overlain by dolomite–gypsum layer. B) SEM photomicrograph of fracture surface that is ∼ 90° to surface shown in panel A. Note elongate aragonite crystals. C) XRDdiffractogram derived from sample shown in panels A and B.

thin growth zones (b15 µm thick) formed of mineralized branching M1(?) hyphae (Fig. 8G–I). EDX analyses of these hyphae consistently yielded high Ca and Mg peaks. No Mg was detected in the underlying substrate. The “dolomite crusts” (up to 10 µm, most ∼5 µm) cover the exterior surfaces of many calcite crystals (Fig. 8J–L). The boundary between the calcite and dolomite is always sharp and there is no indication that the dolomite replaced the calcite. EDX analyses consistently revealed high Ca and Mg peaks in the dolomite crusts but only Ca in the calcite crystals. The crusts are generally nondescript and only locally display possible microbes or blocky crystals (Fig. 8K, L). Scattered filamentous microbes (morphotype M1?) are apparent in the basal part of some of these crusts (Fig. 8L). The “beehive dolomites”, found on the surfaces of some calcite crystals, are domal structures up to 75 µm in diameter and 100 µm high that have a slightly crenulated surface and superficially resemble

“beehives” (Fig. 9A–C). These structures typically have their flat bases attached to a calcite crystal face. There are, however, subspherical forms that are not obviously attached to a substrate. Repeated EDX analyses of many different “beehives” consistently produced high Ca and Mg peaks whereas no Mg was detected in the underlying substrates. Cross-sections through the beehive structures reveal a core (typically ∼75% of diameter) that is encased by concentric laminae (Fig. 9D–I). Some cores are finely laminated (Fig. 9E), others are featureless (Fig. 9F), whereas others are formed of blocky dolomite. The cortices, formed of laminae up to 2 µm (typically ∼1 µm) thick, include gaps that seem to represent laminae that are now missing (Fig. 9E–J). Some cortical laminae contain hints of blocky dolomite. Mats formed of hyphae (mostly morphotype M1) are commonly associated with the beehive dolomite (Fig. 9A–I). In some cases, the hyphae are preferentially located in the open cortical laminae. Although mats cover the exteriors of some beehives, it is

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Fig. 6. SEM photomicrographs showing spatial relationships between calcite and aragonite in stalactites from Nani Cave, Cayman Brac. A) General view showing distribution of calcite and aragonite. Box labeled B shows position of panel B. B) Calcite overlying and encasing aragonite crystals. C) Enlarged view of corroded aragonite crystals. D) Aragonite crystals covered with hyphae and EPS. E) Etched aragonite crystals. F) Large, blocky calcite crystals with deep etch zones. G) Top of calcite crystals showing in panel F, showing trigonal morphology. H) Etched calcite crystal.

difficult to determine if they were actively involved in the precipitation of this dolomite or developed after the dolomite had been formed. 4.3.3. Gypsum The gypsum was recognized by crystal morphology and EDX analyses that showed the presence of Ca and S. Two morphological forms (tabular and sheet) were defined according to the appearance of the crystals (Fig. 10). The “tabular gypsum” crystals, up to 250 µm (typically 100– 150 µm) long, are recognizable by their tabular structure that is readily apparent along their edges where preferential growth and/or dissolution have formed slot-like reentrants (Fig. 10A). The crystal surfaces are smooth and there is no evidence of associated microbes. “Sheet gypsum” is present between some of the calcite crystals (Fig. 10B). These sheets are smooth, display no evidence of internal crystal structures, and devoid of microbes.

4.3.4. Mg–Si needles Some calcite crystal faces are covered with bundles of needles that yield high Mg and Si peaks when subjected to EDX analysis (Fig. 11). No Mg or Si was detected in the underlying substrates. The Mg–Si needles, 50–100 nm wide and up to 2 µm long, are arranged in bundles formed of two or more crystals, of variable length, that lie side-by-side. The bundles, however, lie at various orientations. The mineralogy of these needles is open to debate. Mg–Si-rich precipitates found with aragonite and calcite in caves in the basalts of Hawaii have been identified as kerolite (Mg3Si4O10[OH]2.nH2O) (Léveillé et al., 2000a,b). Described as a fine-grained, massive, hydrated, poorly crystalline, non-expanding talc-like polysilicate that is intimately associated with microbial mats, kerolite was identified by XRD analysis (Léveillé et al., 2000b) and/or the presence of high-Mg, Si, and O peaks on EDX analyses obtained during SEM examination (Léveillé et al., 2000a). In the case of the Cayman stalactites, XRD analyses failed to reveal the presence of kerolite or

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Fig. 7. SEM photomicrographs of blocky dolomite from stalactites from Nani Cave, Cayman Brac. A) Layer of blocky dolomite overlying calcite. B) M3 mat at interface between calcite and blocky dolomite. C) Blocky dolomite with microbial mat covering interfaces between neighbouring subcrystals. White letters D and E indicate positions of panels D and E. D) Microbial mat between dolomite subcrystals. E) Dolomite subcrystal covered with microbial mat. F) Microbial mat with framework of fibrils coating surfaces of blocky dolomite. White letter G indicates position of panel G. G) Fibrils merging with microbial mat. H) Bacteriform microbes (M6) resting on microbial mat covering blocky dolomite.

any similar mineral, probably because it is present in amounts that are below detection limits. Although EDX analyses of the Cayman needles produced high Si, Mg, and O peaks akin to those shown for kerolite (Léveillé et al., 2000a, their Fig. 7B, C), the physical appearance of the Cayman precipitate is significantly different from the Hawaiian precipitates described by Léveillé et al. (2000a,b). Thus, the mineralogical affinity of the Mg–Si needles must remain debatable. 4.4. Mineral and microbe distributions The variable internal fabrics of the stalactites from Nani Cave reflect complex precipitation patterns and, to a lesser extent, diagenetic modifications of some of the aragonite. The aragonite in the older parts of the stalactites has largely inverted to calcite (Fig. 3D) and therefore contrasts with the aragonite in the outer parts of the stalactites that shows no evidence of inversion to calcite

(Fig. 6A, B). Dolomite commonly covers the surfaces of many calcite crystals (Figs. 8J–L, 9) and the peripheral zones of some of the larger crystals are characterized by alternating calcite and dolomite zones (Fig. 8G–I). Available evidence indicates that dolomite is a primary precipitate, and did not form by dolomitization of calcite. Textural evidence indicates that gypsum probably formed after the calcite but before the beehive dolomite (Fig. 10A). The Mg–Si needles are preferentially associated with biofilms that coat calcite crystal faces (Fig. 11). In some areas, scattered, irregular-shaped grains of calcite, typically b1 µm long, are intimately associated with the Mg–Si needles and microbial mats (Fig. 11A, B). Microbes are commonly present on the surfaces of calcite (Fig. 4A–F) and aragonite (Fig. 6D). Despite this, no microbes were found inside the calcite or aragonite crystals. Many of the microbial mats found throughout the stalactites are mineralized with dolomite (Fig. 8A–I) and microbial mats commonly cover the surfaces of the blocky dolomite

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Fig. 8. SEM photomicrographs of dolomitic microbial mats from stalactites from Nani Cave, Cayman Brac. C = calcite, D = dolomite, BD = beehive dolomite. A–F) Dolomite filamentous mat on surface of calcite crystal. Note sharp boundaries between calcite and dolomite (A, D) and distinct filaments embedded in EPS (B, C, E, F). G) Cross-section through calcite crystal with thin dolomite zone in outer part and surface covered with beehive dolomite. Box labeled H indicates area shown in panel H. H) Dolomitic filamentous mat in outer part of calcite crystal. Box labeled I indicates position of panel I. J) Finely laminated dolomite crust on surface of calcite crystal. K) Dolomite crust covering terminal face of calcite crystal. Square labeled L indicates area shown in panel L. L) Sharp boundary between dolomite crust and calcite crystal with rare hypha in basal part of crust (arrow).

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Fig. 9. SEM photomicrographs of beehive dolomite from stalactites from Nani Cave, Cayman Brac. C = calcite, D = dolomite, BD = beehive dolomite. A) Outer surface of calcite lamina covered with beehive dolomite. B) Calcite crystal covered with beehive dolomite. Square labeled C indicates area shown in panel C. C) Beehive dolomite showing internal layering, outer surface, and associated microbial mat. D) Calcite crystal covered with beehive dolomite. Box labeled E indicates area shown in panel E. E, F) Transverse section through beehive dolomite showing nucleus encased by cortical laminae — note gaps that represent missing laminae. G) Gap between two calcite crystals partly filled with beehive dolomite. Boxes labeled H and I indicate area shown in panels H and I. H, I) Cross-sections through beehive dolomite showing nuclei, cortical laminae, and missing laminae. J) Fragment of cortex from beehive dolomite. K) Transverse section through beehive dolomite with cortical laminae formed of blocky dolomite. L) Loose, spherical form of beehive dolomite.

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Fig. 10. SEM photomicrographs of gypsum from stalactites from Nani Cave, Cayman Brac. G = gypsum, C = calcite, D = dolomite. A) Tabular gypsum crystal with irregular edges located between calcite crystals and overlain by dolomite. B) Outer edge of gypsum crystal showing tabular substructure related to preferential growth and/or dissolution.

(Fig. 7C–H). Similarly, microbes are commonly found inside and around the beehive dolomite (Fig. 9C, G–I). No microbes are associated with the gypsum (Fig. 10). 5. Discussion The precipitation of aragonite as opposed to calcite in caves has been attributed to Mg poisoning (e.g., Fischbeck and Müller, 1971; Filipov, 1979; Seemann, 1985; Hill and Forti, 1997; Rowling, 2004), high Mg, Fe, and Mn in karst solutions in closed and partly flooded caves (Bosák et al., 2002), Sr concentrations (Urbani, 1997), temperature (Moore, 1956), humidity levels (Pobéguin, 1955,

1957), sulfate poisoning (Siegel, 1965; Rowling, 2004), saturation levels and precipitation rates (Rowling, 2004), CO2 content of the cave air (Cabrol, 1978; Hill and Forti, 1997), substrate type (Craig et al., 1984), and the composition of the bedrock in which the cave is located (Niggerman et al., 1997). Interpretation of stable isotopes has also provided conflicting viewpoints. Siegel (1965) attributed the systematic alternation between aragonite and calcite laminae to annular changes without specifying the underlying reason for the cyclicity. In contrast, Cilek and Smejkal (1986) argued that isotopes from their stalactites indicated that calcite formed because of CO2 outgassing with minimal evaporation whereas the aragonite formed due to slow evaporation. Frisia et al. (1997), however, argued that aragonite

Fig. 11. SEM photomicrographs of Mg–Si needles from stalactites from Nani Cave, Cayman Brac. A) General view of surface of calcite crystal covered with Mg–Si needles, micrite, and hyphae. Box labeled B indicates position of panel B. B) Coating formed of bundles of Mg–Si needles and micrite. C) Mg–Si needles embedded in layer of EPS that bridges gap between two calcite crystals. Box labeled D indicates position of panel D. D) Interlayered Mg–Si needles at edge of EPS mat. E) Group of Mg–Si needles partly buried in EPS. F) Bundle of Mg–Si needles.

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precipitation due to evaporitic conditions was difficult to explain in caves with no wind, constant temperature, and very high humidity. Instead, based on speleothems from French caves, they suggested that aragonite was precipitated only if the cave was located in dolostone bedrock and where the drip rate was slow. Similarly, Niggerman et al. (1997) and Tásler (1998) noted that aragonite only seemed to be found where the caves were in dolostone bedrock. Although Nani Cave is also located in dolostone bedrock, it is impossible to pinpoint the underlying cause of the systematic alternation between aragonite and calcite precipitation without having any analyses of the formative waters. Dolomite and ankerite have been reported from speleothems from caves in the U.S.A. (Halliday, 1961; Deal, 1962; Thrailkill, 1965; Thrailkill, 1968; Vineyard and Williams, 1968; Hill, 1973; Gonzalez and Lohmann, 1987), Hawaii (Léveillé et al., 2000a,b), South Africa (Martini, 1987, 1993), France (Pobéguin and Gèze, 1961), Austria (Seemann and Eberl, 1985), South Korea (Kashima et al., 1986), Hungary (Takácsné Bohler, 1985), Russia (Filipov, 1979), Israel (BarMatthews et al., 1991), and Spain (Alonso-Zarza and Martín-Pérez, 2008). Dolomite is commonly associated with huntite, aragonite, (Pobéguin, 1960; Moore, 1961; Léveillé et al., 2000b; Alonso-Zarza and Martín-Pérez, 2008), magnesite (Pobéguin, 1960; Takácsné Bohler, 1985; Léveillé et al., 2000b), hydromagnesite (Filipov, 1979; Seemann and Eberl, 1985; Léveillé et al., 2000b), high-Mg calcite (Thrailkill, 1968), ankerite (Takácsné Bohler, 1985; Kashima et al., 1986), protodolomite (Thrailkill, 1968), calcite (Filipov, 1979; Léveillé et al., 2000b), and/or saponite (Filipov, 1979). In many speleothems, aragonite and calcite precipitation is followed by low-Mg calcite, high-Mg calcite, dolomite, nesquehonite (Mg(HCO3)(OH).2H2O), huntite (CaMg3(CO3)4), or hydromagnesite (Mg5(CO3)4(OH)2.4H2O) (Fischbeck and Müller, 1971; Bar-Matthews et al., 1991; Casas et al., 2001; Alonso-Zarza and Martín-Pérez, 2008). This succession has commonly been attributed to a progressive increase in the Mg/Ca ratio generated by the preferential removal of Ca as aragonite and calcite were precipitated. Bar-Matthews et al. (1991) suggested that precipitation of these minerals probably took place from very thin adsorbed surface solution films where significant temporal and spatial variations in the Mg/Ca ratio could be generated. Caves are complex environments where precipitation is controlled by many different factors and it is probably unrealistic to attribute the precipitation of different minerals to variance in a single parameter. Furthermore, most explanations for the precipitation of aragonite, calcite, and Mg-rich carbonates in speleothems have largely ignored the possibility that microbes may have, in some manner, affected precipitation. Siegel (1965), for example, in assessing the cause of aragonite–calcite couplets in speleothems, noted the presence of bacteria but did not implicate them in mineral precipitation. Similarly, Alonso-Zarza and Martín-Pérez (2008) argued that it was impossible to assess the role of microbes in dolomite and huntite precipitation in the Castañar Cave because organically and inorganically laboratoryproduced crystal habits and mineralogical sequences are the same, and only rare microbes were found with the dolomite and huntite in the Castañar speleothems. Conversely, Léveillé et al. (2000a,b) suggested that the microbial mats may have affected aragonite– calcite–dolomite precipitation in caves on Hawaii by (1) inducing precipitation through microenvironmental moderation, (2) the microbes and their associated EPS providing nucleation sites, or (3) producing conditions that favoured the production of hydrous, gel-like phases (e.g., kerolite). Potentially, microbes can influence the growth of speleothems by microbe mineralization, by trapping and binding detrital grains on the substrate, and/or mediating mineral precipitation (Léveillé et al., 2000a,b; Cañaveras et al., 2001; Jones, 2001; Jones, in press). In the stalactites from Nani Cave, there is no evidence of trapping and binding of detrital grains by the filamentous microbes or EPS and there is no evidence of mineral encrustation around the hyphae. It has

often been argued that the metabolic activity of microbes may trigger mineral precipitation by microscale modification of mineral saturation levels in the fluid or by negating factors that inhibit precipitation (Bosak and Newman, 2003, 2005; Barton and Northup, 2007). Although verified by numerous experiments (e.g., Castanier et al., 1999; Ercole et al., 2001; Groth et al., 2001; Rautaray et al., 2003; Ahmad et al., 2004; Rautaray et al., 2004; Baskar et al., 2006), the process of microbes indirectly influencing precipitation is difficult to demonstrate for old samples that formed from waters that are no longer available for collection and analysis. Jones (2009a, in press), however, suggested that a causative relationship between microbes and precipitates can be reasonably inferred if there is a strong spatial correlation between certain precipitates and the microbes. In the stalactites from Nani Cave the dolomite and the Mg–Si needles are invariably located in or close to microbes and their mats (Figs. 8A–I, 11). In contrast, the aragonite and calcite are largely devoid of microbes. Such spatial relationships suggest that microbial activity may have been directly or indirectly responsible for precipitation of the dolomite and/or Mg–Si needles. The dolomite, gypsum, Mg–Si needles, and microbes are largely concentrated on corrosion surfaces produced by seepage waters and/ or condensates that were probably undersaturated with respect to calcite and/or aragonite (cf., Ford and Williams, 1989; Dublyansky and Dublyansky, 1998; Tarhule-Lips and Ford, 1998; Dublyansky and Dublyansky, 2000; Tarhule-Lips and Ford, 2004; Ford and Williams, 2007). Microbes flourished in the sheltered, micro-niches where seepage and/or condensate waters locally dissolved the substrate. That many of these microbes and their EPS have been replaced by dolomite and/or host the Mg–Si needles suggests a causative relationship between the microbes and the precipitates. Determining the physiochemical attributes of the waters that parented these precipitates is impossible because the stalactites are not actively forming today, as the cave is dry. Even if waters were flowing through the cave it would be difficult to show that they were responsible for all of the minerals found in the older parts of the stalactites. The only possible indication of the water chemistry comes from modern waters collected from other caves on Cayman Brac (Table 1). The microscale variations in the precipitates that form the stalactites (Fig. 12) clearly show that the formative processes operated at a microscale. This is feasible given that the thin films of water on the surfaces of the stalactites were probably prone to significant temporal and spatial changes in composition, as suggested by Bar-Matthews et al. (1991). Inorganic dolomite precipitation under low-temperature and lowpressure conditions has generally been deemed impossible because of kinetic factors (McKenzie, 1991; Land, 1998; Arvidson and MacKenzie, 1999). Dolomite precipitation has, however, taken place in natural marine settings or laboratory experiments if bacteria are present (Vasconcelos et al., 1995; Vasconcelos and McKenzie, 1997; Warthmann et al., 2000; van Lith et al., 2002; van Lith et al., 2003b; Moreira et al., 2004; Vasconcelos et al., 2005; Warthmann et al., 2005). It has been argued that this occurs because actively growing bacteria alter their surrounding microenvironment by changing the pH and increasing metabolic products and/or actively concentrating Ca2+ and Mg2+ ions around their cells (van Lith et al., 2003a,b). In particular, van Lith et al. (2003b) drew attention to the close relationship between newly formed dolomite crystals and the EPS associated with the bacteria used in their experiments. Such dolomite commonly has complex crystal forms with composite dumbbell (van Lith et al., 2003a, their Fig. 3B; 2003b, their Fig. 1B) or “twisted structures formed of successive planar layers” (van Lith et al., 2003b, their Fig. 2B) crystals being common. This parallels the atypical crystal morphologies of the dolomite that is associated with the microbes in the Cayman stalactites. Systematic variations in the elemental content of the calcite that forms stalactites have commonly been used as proxies of seasonal climate changes that have been deemed responsible for the

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Fig. 12. SEM photomicrograph showing complex, microscale distribution of calcite (C), dolomite (D), and gypsum (G) from stalactites from Nani Cave, Cayman Brac. Composition of all points verified by EDX analysis.

composition of the waters that flow through the caves (e.g., Roberts et al., 1998; Huang et al., 2001; Treble et al., 2003, 2005; Borsato et al., 2007). An abiogenic origin of the calcite has been assumed in virtually every case with no consideration being given to the possibility that microbes may have directly or indirectly concentrated various elements in the host calcite. This study shows that local concentrations of Mg may be directly related to microbial activity that leads to the formation of various types of dolomite and Mg–Si needles.

research, the Department of Environment, Cayman Islands who directed me to the cave, Breanna Uzelman who assisted in the field, George Braybrook (University of Alberta) who took the SEM images used in this study, and Drs. Michal Gradzinski and Leslie Melim who critically reviewed an earlier version of this manuscript.

6. Conclusions

Ahmad, A., Rautaray, D., Sastry, M., 2004. Biogenic calcium carbonate: calcite crystals of variable morhology by the reaction of aqueous Ca2+ ions with fungi. Advanced Functional Materials 14, 1075–1080. Alonso-Zarza, A.M., Martín-Pérez, A., 2008. Dolomite in caves: recent dolomite formaton in oxic, non-sulfate environments, Castañare Cave, Spain. Sedimentary Geology 205, 160–164. Arvidson, R.S., MacKenzie, F.T., 1999. The dolomite problem: control of precipitation kinetics by temperature and saturation state. American Journal of Science 299, 257–288. Bar-Matthews, M., Matthews, A., Ayalon, A., 1991. Environmental controls of speleothem mineralogy in a karstic dolomite (Soreq Cave, Israel). Journal of Geology 99, 189–207. Barton, H.A., Jurado, V., 2007. What's up down there? Microbial diversity in caves. Microbe 2, 132–138. Barton, H.A., Northup, D.E., 2007. Geomicobiology in cave environments: past, current and future perspectives. Journal of Cave and Karst Studies 69, 163–178. Barton, H.A., Spear, J.R., Pace, N.R., 2001. Microbial life in the underworld: biogenicity in secondary mineral formations. Geomicrobiological Journal 18, 359–368. Baskar, S., Baskar, R., Mauclaire, L., McKenzie, J.A., 2006. Microbially induced calcite precipitation in culture experiments: Possible origin for stalactites in Sahastradhara caves, Dehradun, India. Current Science 90, 58–64. Borsato, A., Frisia, S., Fairchild, I.J., Somogyi, A., Susini, J., 2007. Trace element distribution in annual stalagmite laminae mapped by micrometer-resolution Xray fluorescence: implications for incorporation of environmentally significant species. Geochimica et Cosmochimica Acta 71, 1494–1512. Bosak, T., Newman, D.K., 2003. Microbial nucleation of CaCO3 in the Precambrian. Geology 31, 577–580. Bosak, T., Newman, D.K., 2005. Microbial kinetic controls on calcite morphology in supersaturated solutions. Journal of Sedimentary Research 75, 190–199. Bosák, P., Bella, P., Cílek, V., Ford, D.C., Hercman, H., Kadlec, J., Osborne, A., Pruner, P., 2002. Ochtiná aragonite cave (western Carpathians, Slovakia): morphology, mineralogy of the fill and genesis. Geologica Carpathica 53, 399–410. Cabrol, P., 1978. Contribution à l'étude du concrétionnement carbonaté des grottes du Sud de la France, morphologie, génèse, diagénèse. Mémoir Recherches Géologie Hydrogéologie, 12. University of Montpellier. 275 pp. Cañaveras, J.C., Sanchez-Moral, S., Soler, V., Saiz-Jimenez, C., 2001. Microorganisms and microbially induced fabrics in cave walls. Geomicrobiological Journal 18, 223–240.

Analysis of stalactites from Nani Cave on Cayman Brac has produced the following important conclusions: • the stalactites are formed primarily of aragonite and calcite along with lesser amounts of dolomite and minor amounts of Mg–Si needles, • some of the aragonite in the central, older parts of the stalactites has inverted to calcite, • although microbes and their associated EPS are commonly found on the surfaces of the aragonite and calcite crystals, there is no evidence of microbes inside the crystals, • many of the microbes and their associated EPS have been mineralized with dolomite, • the Mg–Si needles, although rare, are always embedded in EPS, and • the intimate spatial relationship between dolomite and Mg–Si needles with microbes and their associated EPS suggests that they are genetically related. The available evidence indicates that microbes directly or indirectly promoted dolomite precipitation through modification of their surrounding microenvironment or by providing suitable nucleation sites. Conversely, the microbes seem to have exerted little influence over precipitation of the aragonite and calcite. Acknowledgements I am grateful to the Natural Sciences and Engineering Council of Canada (grant A6090) who provided the financial funding for this

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