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Sedimentary Geology 263-264 (2012) 45–55

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Sedimentary Geology

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Environmental controls on microbial community cycling in modern marine stromatolites

Emily M. Bowlin a,1, James S. Klaus b, Jamie S. Foster c, Miriam S. Andres a,2, Lillian Custals a, R. Pamela Reid a,⁎ a Rosenstiel School of Marine and Atmospheric Science, University of Miami, United States b University of Miami, United States c Space Life Sciences Lab, University of Florida, United States article info abstract

Article history: Living stromatolites on the margins of Exuma Sound, Bahamas, are the only examples of modern stromatolites Received 31 January 2011 forming in open marine conditions similar to those that may have existed on platforms. Six Received in revised form 11 July 2011 types have previously been documented on the surfaces of stromatolites along the eastern side Accepted 4 August 2011 of Highborne Cay (Schizothrix, Solentia, heterotrophic biofilm, stalked , tube diatom and Phormidium Available online 16 August 2011 mats). Cycling of these communities create laminae with distinct microstructures. Subsurface laminae thus Keywords: represent a chronology of former surface mats. Marine stromatolites The present study documents the effects of environmental factors on surface microbial communities of Microbial mats modern marine stromatolites and identifies potential causes of microbial mat cycling. Mat type and burial Community cycling state at 43 markers along a stromatolitic on the margin of Highborne Cay were monitored over a two- Lamination period (2005–2006). Key environmental parameters (i.e., temperature, light, wind, water chemistry) were Environment also monitored. Sedimentation Results indicated that the composition of stromatolite surface mats and transitions from one mat type to another are controlled by both seasonal and stochastic events. All six stromatolite mat communities at Highborne Cay showed significant correlations with water temperature. Heterotrophic biofilms, Solentia, stalked diatom and Phormidium mats showed positive correlations with temperature, whereas Schizothrix and tube diatom communities showed negative correlations. A significant correlation with light (photosynthetically active radiation, PAR) was detected only for the heterotrophic biofilm community. No significant correlations were found between mat type and the monitored wind intensity data, but field observations indicated that wind- related events such as storms and sand abrasion play important roles in the transitions from one mat type to another. An integrated model of stromatolite mat community cycling is developed that includes both predictable seasonal environmental variation and stochastic events. The long-term monitoring of mat communities on Highborne Cay stromatolites and the resulting model are an important step in understanding morphogenesis of modern marine stromatolites, with implications for interpreting patterns of stromatolite lamination in the geologic record. © 2011 Elsevier B.V. All rights reserved.

1. Introduction microbes, minerals and the environment, stromatolite formation has had a profound influence on the evolution and function of life Layered deposits of calcium carbonate known as stromatolites on this planet. A fundamental goal of stromatolite research is to use dominate the record for over 80% of Earth history (Walter, stromatolites to reconstruct ancient environments and understand 1994; Grotzinger and Knoll, 1999). Formed by interactions between how benthic microbial communities interacted with these environ- ments. Process-oriented studies of the morphogenesis of modern stromatolites are critical for such paleo-environmental interpreta-

⁎ Corresponding author at: Rosenstiel School of Marine and Atmospheric Science, tions (Grotzinger and Knoll, 1999). University of Miami, 4600 Rickenbacker Causeway, Miami, FL 33149 United States. Living stromatolites in Exuma Cays, Bahamas, are the only examples of E-mail addresses: [email protected] (E.M. Bowlin), modern stromatolites forming in open marine conditions similar to those fl [email protected] (J.S. Klaus), jfoster@u .edu (J.S. Foster), that may have existed on Precambrian platforms. Reid et al. (2000) [email protected] (M.S. Andres), [email protected] (L. Custals), proposed a model for lamination formation in Exuma stromatolites in a [email protected] (R.P. Reid). 1 Current affiliation ExxonMobil. study aimed at relating surface microbial communities to subsurface 2 Current affiliation Chevron Energy Technology Company. microstructure. They found that cycling of distinct microbial communities

0037-0738/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.sedgeo.2011.08.002 46 E.M. Bowlin et al. / Sedimentary Geology 263-264 (2012) 45–55 on the stromatolite surface creates laminae with distinct microstructures. The present paper documents the effects of environmental factors Subsurface laminae thus represent a chronology of former surface mats. on surface microbial communities of modern marine stromatolites The causes for the cycling of microbial communities on the surfaces of and identifies potential causes of microbial mat cycling. These results Bahamian stromatolites are currently unknown. Community shifts could are a critical step in understanding stromatolite morphogenesis. be biologically driven (intrinsic control) or environmentally driven (extrinsic control). Previous authors have speculated on the importance 2. Background of sedimentation for stromatolite growth in the open ocean conditions of , suggesting that periodicburialbysandpreventsovergrowth Modern marine stromatolites form along high-energy coasts and in by epilithic algae and grazing/burrowing invertebrates (e.g. Dravis, 1983; tidal channels along the margins of Exuma Sound (Fig. 1A; Dravis, 1983; Dill et al., 1986; Macintyre et al., 1996). Initial quantitative data on gross Dill et al., 1986; Reid and Brown, 1991; Reid et al., 1995). A series of sedimentation in the Stocking Island reef complex, at the south end of the investigations by RIBS researchers (see http://stromatolites.info) have Exuma Cay chain of islands, showed that stromatolites were buried to focused on stromatolite formation at Highborne Cay, at the north end of depths of 0.5 m for periods of up to 100 days, limiting recruitment and the Exuma Cays (Fig. 1B). Highborne Cay stromatolites form as columns colonization by macroalgae and corals (Steneck et al., 1998). Additionally, and ridges (Fig. 2A, B) and are part of a fringing reef complex that arigorousanalysisofthewaveandsedimentdynamicsalongthe stretches for 2.5 km along a sandy beach on the eastern shore of the Highborne Cay reef complex at the north end of the Exuma chain suggests island (Reid et al., 1999; Andres and Reid, 2006; Andres et al., 2009). that stromatolite growth may be restricted to a relatively narrow range of Three distinct morphological zones are recognized within the reef: reef flow energy and sediment transport conditions (wave speeds typically crest, reef flat, and back reef lagoon. The reef crest and reef flat are 10–70 cm s− 1, with short-lived surges up to 100 cm s− 1; gross composed predominantly of the coralline algae Neogoniolithon strictum; suspended sediment of 7–10 g/cm−2 day−1 or 4–6cmday−1; Eckman shallow subtidal stromatolites and intertidal (microbial et al., 2008). structures lacking a laminated fabric) are present in the back reef lagoon In 2003, the Research Initiative on Bahamian Stromatolites, (RIBS (Fig. 1C). project) initiated a comprehensive five-year program to investigate The reef complex is best developed in the southern 1 km of the intrinsic and extrinsic factors causing cycling of the surface Highborne Cay beach; where it was subdivided into ten research sites microbial communities forming marine stromatolites. An important (Fig. 1C). Sites 1 and 2 are 20–50 m wide, with width decreasing to component of this study was an intensive field monitoring effort, b10 m north of Site 2. North of Site 10 the reef forms only small isolated which included ‘A Year in the Life of a Stromatolite’. The ‘year’ patches. Sediments in the swash zone and shallow subtidal portions of evolved into two of almost continuous field monitoring in the reef at Sites 1–10 are skeletal grains and peloids, commonly with 2005 and 2006. oolitic coatings and a median grain size of 175–275 μm; grain size

Fig. 1. Location of stromatolites in a fringing reef at Highborne Cay, Bahamas. A) Google Earth images of the Bahamas Platform, showing Highborne Cay on the margin of Exuma Sound, at the north end of the Exuma Cays. B) Google Earth image of Highborne Cay, showing the location of reef complex. C) Aerial photo mosaic showing the ten study sites in the Highborne Cay reef; shallow subtidal stromatolites are located in the back reef lagoonal areas (purple). E.M. Bowlin et al. / Sedimentary Geology 263-264 (2012) 45–55 47

Fig. 2. Stromatolites and surface microbial mats of Highborne Cay, Bahamas. A) Pronounced columnar stromatolites at Site 1. B) Fields of stromatolite ridges at Site 8. C) Microbial mat (arrow) with smooth clean surface features indicating it is a crusty Solentia mat with adjacent growth of (m) in the upper right. D) Representation of stalked diatom mat as yellow “fur”. E) Tube diatom mat forming a blanket with pustular morphology (white arrows); note the gray-green layer of (black arrow) visible in the cut section. F) Phormidium mat forming a soft, coherent, pudding-like mound, encasing and surrounded by the macroalgae Batophora (b).

coarsens significantly north of Site 10 (Eckman et al., 2008). Tides are 2. Type 2 mats, or heterotrophic biofilms, are continuous surface films semidiurnal with a maximum range of approximately 1 m. of EPS dominated by diverse populations of heterotrophic aerobic and anaerobic (Baumgartner et al., 2009); these films overlie 2.1. Mat types moderately dense and diverse populations of filamentous and coccoid cyanobacteria (Foster et al., 2009; Stolz et al., 2009). RIBS studies have documented six microbial mat types on the surfaces Precipitation of microcrystalline calcium carbonate (micrite) within of Highborne Cay stromatolites (Reid et al., 2000; Stolz et al., 2009; Franks surface biofilms forms thin micritic crusts (20–50 μm thick), which et al., 2010). Three of these, referred to as “classic prokaryotic” mats by extend laterally across the stromatolite surface (Visscher et al., 2000). Stolz et al., 2009 were originally described by Reid et al., 2000 as Type 1, 2, 3. Type 3 mats, or Solentia mats, consist of an abundant population of and 3 mats; these three mat types have smooth, firm to crusty surfaces coccoid, euendolithic cyanobacteria, mainly Solentia spp., and that can be difficult to differentiate in the field (Fig. 2C). All three of these heterotrophic bacteria. Solentia mat types have been shown to classic mat types have distinctive populations of bacteria as detected contain the most diverse bacterial community of the three classic mat using both morphology and 16S rRNA gene sequencing (Baumgartner et types (Baumgartner et al., 2009; Foster and Green, 2011). The al., 2009; Stolz et al., 2009; Foster and Green, 2011). Three additional euendolithic cyanobacteria infest carbonate grains beneath a surface trapping and binding communities, which form soft to fluffy mats, were biofilm and micritic crust; a dense population of filamentous described more recently by Stolz et al., 2009 and Franks et al., 2010. cyanobacteria is also present below the surface film. Carbonate precipitation within euendolithic bore holes welds grains together, Classic Type 1, 2, and 3 mats forming a lithified horizon of micro-bored grains (Macintyre et al., 1. Type 1 mats, also known as Schizothrix mats, consist of a complex 2000). The crusty Solentia mats may become colonized with various microbial community with over 100 bacterial ecotypes (Baumgartner species of macroalgae and algal turf (Fig. 2C). et al., 2009). These mats are typified by the presence of a motile filamentous cyanobacterium, Schizothrix spp., which generates Additional trapping and binding communities copious secretions of extracellular polymeric substances (EPS). 4. Stalked diatom mats are characterized by surface communities of the Filamentous Schizothrix communities trap and bind sediment, stalked diatom Licmophora remulus Grunow and an underlying forming unlithified grain layers. network of cyanobacteria (Schizothrix). The appear as yellow 48 E.M. Bowlin et al. / Sedimentary Geology 263-264 (2012) 45–55

fuzz to fur with cyanobacteria forming a subsurface layer that is from westerly winds. Wind speeds were related to wave energy along caramel to green in color (Fig. 2D). The diatom network traps the reef in a concurrent study of sediment dynamics and suspended sediment grains, which are bound into the stromatolite framework sediment transport (Eckman et al., 2008). by the upwardly mobile Schizothrix, forming unlithified grain layers. 5. Tube diatom mats are formed by surface communities of Naviculid-like 3.1.4. Water chemistry tube diatoms, with and underlying gray/green layer of cyanobacteria Salinity and pH were measured on a monthly basis, using a Fisher (Schizothrix)(Fig. 2E). These mats form discrete pustules (referred to as hand held refractometer and calibrated Hanna Waterproof pH meter. In stringy pustules due to the presence of sand adhering to the sticky addition, 12 water samples were collected for nutrient analysis in 2006 diatom tubes) and blankets. Like the stalked diatom mats, the tube using sterile 50 mL syringes. The samples were filtered through 0.45 μm diatom network traps sediment grains, which are bound into the filters into acid washed glass vials and immediately frozen for analysis stromatolite framework by the upwardly mobile Schizothrix,forming by gas-segmented continuous flow autoanalyzer at the nutrient lab of unlithified grain layers. NOAA Atlantic Oceanographic and Meteorological Laboratory (AOML) + − − 3− 6. Phormidium mats are formed by thin-sheathed cyanobacteria in Miami. Concentrations of NH4 , NO2 , NO3 ,PO4 and Si(OH)4 were tentatively identified as Phormidium spp. based on microscopy. determined using a modified Alpkem Flow Solution, 5-channel gas- + The Phormidium network traps grains, forming soft coherent segmented auto-analyzer with colorimetric detection. NH4 was mounds on the stromatolite surface; these pudding-like structures determined by reacting with alkaline phenol and NaDTT at 60 °C to firm up in a matter of weeks as the mat becomes colonized by form indophenol blue in the presence of sodium nitroferricyanide as a − Schizothrix. Phormidium mats commonly form around a stalk of the catalyst and absorbance measured at 640 nm. NO2 was determined by green alga Batophora (Fig. 2F). diazotizing with sulfanilamide and coupling with N-1 naphthyl ethylenediamine dihydrochloride to form an azo dye and its absorbance − − 3. Methods was measured at 540 nm (Zhang, 2000). NO3 was reduced to NO2 by a custom-made cadmium column (Zhang et al., 2000) then analyzed for − − 3− To conduct an intensive field-monitoring program of the Highborne NO2 .NO3 concentrations were calculated by difference. PO4 was Cay reef, a small research station was constructed on the island in 2003. determined by reacting with molybdenum (VI) in an acidic medium to The initial plan was to monitor the reef one-week-per-month, however, form a phosphomolybdate complex, subsequently reduced with conditions along the reef tract proved far too dynamic for a one week per hydrazine at room temperature to form phosphomolybdenum blue month sampling scheme to be effective. Therefore, the program evolved and absorbance measured at 800 nm (Zhang et al., 2001). Si(OH)4 was to almost continuous monitoring for a two-year period from Jan 2005 to analyzed by reacting with molybdate in an acidic solution to form β- Dec 2006; data collected are outlined below. molybdosilicic acid, then reduced by ascorbic acid to form molybdenum blue and absorbance measured at 660 nm. The detection limits were + − − 3− 3.1. Environmental data 0.02 μM for NH4 , 5 nM for NO2 , 0.01 μM for NO3 , 0.01 μM for PO4 and 0.05 μM for Si(OH)4. In 2003 a weather station was installed at Highborne Cay a few meters above high tide on the east-facing beach near Site 6. Light, 3.2. Field observations temperature, wind speed, and wind direction were recorded every 15 min by a Campbell Scientific data logger (model CR10X). Data were At each of the ten study sites, fixed markers (i.e., galvanized stakes analyzed to provide hourly, daily, weekly, and monthly averages. A and nails) were driven into the reef for monitoring purposes. In addition long-term weather record for Highborne Cay, occasionally punctuated to the stakes and nails, stainless steel screws were used as temporary due to maintenance needs or storm damage, is available starting in markers. Marker names indicate site, stake or nail (S or N), and screws November 2003 and continuing to April 2008. Meteorological and differentiated by different colors of flagging tape; N8.6 orange, for other environmental data collected for the present study site are example, refers to Site 8, Nail 6, and a screw with orange tape. A total of outlined below. 43 stakes and nails were positioned on stromatolites in the back reef lagoon. Observations of mat type and burial state of the stromatolites at 3.1.1. Temperature these markers were recorded two to three times a week during 2005 and Air temperature was recorded at the weather station by an R. M. 2006, and at least once a month during 2007. Digital imagery captured Young temperature probe (model 41342). In addition, water with a Sony Cyber-shot camera in an underwater housing complemen- temperature in the back reef lagoon was recorded by HOBO Tidbit ted the written observations. Over 13,000 field images for 2005 and temperature loggers programmed to collect readings every 10 min. 2006 were entered into the database iView MediaPro. Combined data sets from Filemaker and iView were used to construct “barcodes” (i.e., a 3.1.2. Light record of mat type and burial-exposure status for each of the designated Measurements of photosynthetically active radiation (PAR) were stromatolites) for each of the 43 markers over a two-year period. recorded by a LI-Cor light sensor (model 190-S). PAR designates the spectral range (400–700 nm) of solar radiation that photosynthetic 3.2.1. Burial and exposure patterns are able to use in . PAR measurements at Based on visual observations at daily to weekly intervals, the Highborne Cay were quantified as micromoles of photons per square stromatolites at each of the 43 markers were designated as “buried”, meter per second (μmol m− 2 s− 1), which is a measure of the “exposed” or “sand-level”, as described in Reid et al. (2011). “Exposed” photosynthetic photon flux (area) density. PAR values were averaged denotes a monitored surface free of sediment accumulation. “Buried” hourly and hourly values were averaged to get weekly PAR. denotes more than 2 cm of sediment covering the monitored surface; based on Perkins et al. (2007) data showing that the mats are 3.1.3. Wind photosynthetically inactive at depths of 3 cm. “Sand-level”, a subset of Wind speed and wind direction were recorded by an R. M. Young exposed, denotes a surface at the level of the sand or buried to a depth of wind monitor (model 05103-5). The location of the weather station ≤2 cm. Surfaces at sand-level correspond to a transition between burial on the east-facing beach provided an accurate record of the dominant and exposure events and may be buried and unburied with shifting easterly winds. A sand ridge west of the station compromised the tides. accuracy of westerly winds, but the recorded data represent For each day during 2005–2006, stromatolites at each marker were conditions experienced by the stromatolites, which are also sheltered classified as buried, exposed, or sand-level (Reid et al., 2011). Days E.M. Bowlin et al. / Sedimentary Geology 263-264 (2012) 45–55 49 lacking recorded data were handled as follows: if the marker showed A 32 the same burial or exposure state on both ends of the data gap, the Water Temperature days within the gap were assigned this same value; if burial state 30 changed during the missing time interval, burial state was changed at 28 the mid-point of the gap. The number of days each marker was 26 exposed or buried in 2005 and 2006 was then calculated as a percent 24 of the two-year time span; sand-level was grouped with exposed. The average burial and exposure data for stromatolites at each site 22 were also classified into event types according to the duration of the Water Temperature (°C) 20 burial and exposure periods. Burial or exposure episodes of b7 days JFMAMJJASONDJFMAMJJASOND fi 2005 2006 were classi ed as daily events; burial or exposure episodes of 7 to B 700 30 days were classified as week-long events, and burial or exposure ) PAR episodes of N30 days were classified as month-long events. The -1 600 s frequency of each event type was then calculated as a percent of total -2 500 time exposed or buried, and averaged for all markers. 400 3.2.2. Mat type

300 No Data No Data

Mat types were designated using the terminology of Stolz et al., PAR (µmol m 2009 (Schizothrix, heterotrophic biofilm, Solentia, stalked diatom, tube 200 JFMAMJJASONDJFMAMJJASOND diatom, and Phormidium mats); if more than one community 2005 2006 colonized an individual marker location, major and minor mat types C 10.0 were designated. If the surface mat community could not be identified Wind Speed in the field a hand sample was collected for laboratory observation 8.0 using a stereomicroscope (Olympus SX12). 6.0 A total of 1232 mat observations were made in 2005 and 2006. To assess seasonality of the different mat types we calculated the weekly 4.0 relative abundance of each mat (percent abundance). Percent

2.0 No Data No Data abundance was calculated by dividing the number of observations Wind Speed (m/s) of each mat type for a given week by the total mat observations made 0.0 JFMAMJJASONDJFMAMJJASOND during that week. Pearson's product moment correlation coefficient 2005 2006 (r) was used to determine the relationship between the relative abundance of each mat type and the associated environmental Fig. 3. Weekly averages for three environmental parameters logged during the 2005 and monitoring data (i.e., temperature, PAR, wind intensity). A cut off of 2006 monitoring period at Highborne Cay. A) Water temperature. B) Photosynthetically pb0.05 was used to assess significance of correlations. active radiation (PAR). C) Maximum daily average wind speed.

4. Results fronts in the winter months brought significant north winds. Average weekly wind speeds ranged from 1.32 m/s (Sept 2006) to 8.45 m/s 4.1. Temperature (Dec 2006), averaging 4.18 m/s. The maximum values of daily average speed each week ranged from 2.44 m/s (Sept 2006) to 11.54 m/s (Nov Water temperatures were generally within one or two degrees of 2006), averaging 6.4 m/s (Fig. 3C). Strongest winds typically blew air temperature, showing pronounced seasonal cycles (Fig. 3A). The from November to January; calm periods occurred in any month. average weekly water temperature for the 2005–2006 monitoring September was typically calm, except for the passage of tropical period was 26.8 °C, with a minimum value of 20.3 °C in January 2005 and maximum value of 30.3 °C in September 2005. Weekly water 0 temperature averaged 26.4 °C in 2005, about 1 °C warmer than the 2006 average of 25.7 °C. Warmest water temperatures occurred in June through September, the coldest temperatures were in January 315 2005-2006 Wind Data 45 thru March.

4.2. Light

Wind speed (m/s ) Photosynthetically Active Radiation (PAR) exhibited a seasonal > 0 - 2 > 2 - 4 cycle over the 2005–2006 monitoring period, with higher values May 270 > 4 - 6 0% 90 through August, and lower values November through January > 6 - 8 2 1 > 8 - 10 4% (Fig. 3B). Average weekly values were 454 μmol m− s− with a > 10 − 2 − 1, minimum of 243 μmol m s in Dec 2006, and maximum of 8% 632 μmol m− 2 s− 1 in May 2005. PAR values were slightly higher in 2005 than 2006, with weekly averages about 471 μmol m− 2 s− 1 and 12 % 440 μmol m− 2 s− 1 respectively. PAR exhibited substantial short-term 225 16 % 135 fluctuations within the seasonal cycles. 20 % 4.3. Wind 180

Fig. 4. Wind rose showing wind speed and direction (simple coordinates) at Highborne Highborne Cay is within the easterly Trade Wind Belt and this is Cay reef for 2005 and 2006 combined. As the weather station was located east of a sand fl re ected in the wind data. Wind roses for 2005 and 2006 (Fig. 4) ridge, wind speed from the west is compromised. The wind speeds do, however, showed dominant winds from the east, northeast and southeast. Cold represent conditions experienced by the reef, which is also sheltered from west winds. 50 E.M. Bowlin et al. / Sedimentary Geology 263-264 (2012) 45–55 storms and hurricanes. Tropical Storms Katrina (Aug 23), Rita (Sept the year (Fig. 6A). On average, 65±21% of the exposure events were 19) and Wilma (Oct 24) passed directly over Highborne Cay in 2005. month-long (N30 days), 29±19% were week-long (7–30 days) and 6± At Highborne Cay Katrina was poorly organized with minimal wind, 5% were daily (b7days)(Fig. 6B). Burial events showed similar duration whereas Rita and Wilma were well-developed storms when they patterns, with 65±21% month-long, 29±19% week-long, and 6±5% of passed over Highborne and the weather station was dismantled to the burial events b7daysinduration(Fig. 6B). Individual burial-exposure avoid damage. patterns for all 43 stromatolite markers are presented in Bowlin, 2011; burial-exposure patterns throughout the Highborne Cay reef are 4.4. Water chemistry presented in Gaspar, 2007.

Seawater pH along the reef ranged from 8.1 to 8.2 with no significant 4.6. Mat type pH changes during the day and no seasonal trends. Salinity ranged from 35 to 38 ppt, with the higher values occurring in the back reef lagoon in As with the burial and exposure events, microbial mats on the + the summer. Nutrient values of b0.02–2 μM for NH4 , b5 nM–0.03 μM surfaces of Highborne Cay stromatolites were highly variable based on − − 3− for NO2 , 0.12–0.79 μM for NO3 , b0.01–0.5 μM for PO4 , and b0.05 μM position along the reef tract. Microbial mats colonizing stromatolites for Si(OH)4 confirm oligotrophic conditions typical of Bahamian at Site 1 and Site 8 for the 2005 and 2006 monitoring period are . shown in Fig. 7. Stalked diatom and tube diatom mats were abundant at Site 1, but rare at Site 8; Phormidium mat was present at Site 1 in 4.5. Burial-exposure patterns summer 2006. Site 8 was dominated by the classic Schizothrix, heterotrophic biofilm and Solentia mat communities. Migrating sand waves in the back reef lagoon buried and exposed Observations of mat type abundance at all sites throughout the the stromatolites for periods of days, weeks or months. Sedimentation reef (1232 records in 2005 and 2006), show seasonal distribution patterns were highly variable based on position along the reef tract. patterns (Fig. 8). Although Schizothrix mats are abundant throughout Burial and exposure events for stromatolites at Site 1 and Site 8 for the the year, they exhibit higher relative abundance in the cooler winter 2005 and 2006 monitoring period are shown in Fig. 5. Site 1 months (Fig. 8A). Heterotrophic biofilms with micritic crusts were stromatolites were typically exposed for long periods at a time, observed from May through September, peaking in May and June often several months in duration, with occasional sand-level intervals. (Fig. 8B). Solentia mats were also abundant throughout the year, with In contrast, Site 8 stromatolites experienced relatively short periods of no strong seasonal distribution (Fig. 8C). Stalked diatom mats showed exposure, typically lasting days to weeks, with frequent sand-level a strong seasonality, occurring primarily from June or July to events. Moreover, Site 8 stromatolites at sand-level typically December (Fig. 8D). Tube diatom mats were abundant December experienced abrasion as waves moved sand back and forth across through May, and August through November (Fig. 8E), with the the stromatolite surfaces. Burial episodes at Site 1 are typically week winter–spring tube diatoms forming pustular blankets, and the to month-long events, with burial at Site 8 being day, week or month- summer–fall occurrences forming stringy pustules that were often long in duration. Tropical Storms Rita (September 19–20, 2005) and mixed with stalked diatoms. Phormidium mats were relatively Wilma (October 24, 2005) buried stromatolites at Site 8 but not at Site uncommon, occurring June–August (Fig. 8F). 1(Fig. 5C). Tropical Storm Katrina had no impact on stromatolite burial at Highborne Cay. 4.7. Correlation of extrinsic factors and mat type Averages of burial and exposure data(i.e.,sand-levelgroupedwith exposed mats) for all 43 markers indicated that the stromatolites were The seasonality of the heterotrophic biofilm, stalked diatom, tube buried for an average of 44±15% of the year and exposed for 56±15% of diatom, and Phormidium communities suggest that mat composition may

A B

C JFMAFMAMJJ JSOND A A M J JSOND Site 1 1 Site

2005 2006 Site 8 Site JFMAFMAMJJ JSOND A A M J JSOND Rita Wilma buried exposed sand level no data

Fig. 5. Burial and exposure events at Site 1 and Site 8 during 2005 and 2006. A) Buried stromatolites at N1.2 on June 19, 2005; only the top of the nail is showing above the sand. B) Exposed stromatolites at nail N1.2 (arrow) on Oct. 10, 2005. C) Bar graphs for N1.2 stromatolites (Site 1; upper graph) and N8.6orange stromatolites (Site 8; lower graph). Note that exposure events are typically N30 days at N1.2 (Site 1) and b30 days at N8.6orange (Site 8). Tropical Storms Rita and Wilma in 2005 buried stromatolites at Site 8, but did not interrupt a long period of exposure at Site 1. E.M. Bowlin et al. / Sedimentary Geology 263-264 (2012) 45–55 51

A PAR. The presence of biofilms increased when observed PAR values 100 ranged between 400 and 650 μmol m− 2 s−1. Exposed vs. Buried Effects of wind on mat type showed no significant correlation 80 (Table 1). However, field observations indicated that the various mat types responded in characteristic ways to wave action, abrasion and 60 sediment movement, which are directly related to local wind conditions (Table 1). All of the classic mat types (Schizothrix, fi 40 heterotrophic bio lm and Solentia) thrived under strong wave action % Percent and burial events. Differences were detected, however, in response to abrasion. Both the heterotrophic biofilm and Solentia mat types 20 persisted in response to abrasion, whereas the Schizothrix mats transition to other mat types during sediment abrasion events. The 0 Exposed Buried other three mats. stalked diatom, tube diatom and Phormidium mats eroded under strong wave action and did not survive abrasion or B100 burial events. Exposure Events 80 5. Synthesis of environmental factors and mat cycling

Studies conducted in parallel with the 2005–2006 Highborne Cay 60 monitoring program provided additional information regarding the environmental conditions associated with microbial mat development. 40 % Percent For example, Eckman et al., 2008 related wind speed at Highborne Cay to local wave conditions and showed that sediment movement along the 20 Highborne Cay reef tract was largely a response to local wind events. The wave energy that impacted the reef was driven by local wind-forcing 0 and increased largely in response to the passage of atmospheric Monthly Weekly Daily disturbances that typically affect the region for a few days. Although C some wave energy was almost always noted (maximum horizontal 100 orbital speeds at the water–sediment interface are rarelyb10 cm/s), Burial Events wave conditions remained comparatively calm until local winds 80 increased above speeds of ~3–4 m/s, at which point maximum wave speeds rapidly increased to 50–80 cm/s. Wave speeds that increased 60 northward along the beach were 1.4 to 2 times higher north of Site 10 than at Site 1 (Eckman et al., 2008). Results from Eckman et al., 2008 also provide insight into mat 40 % Percent development at the various sites. This study showed that increasing wave energy northward from Site 1 accounted for more vigorous 20 abrasion of stromatolite surfaces in the sand-level zone compared to the more northern sites. Moreover, sand-level abrasion in the surf 0 zone showed an apparent correlation with biofilm formation Monthly Weekly Daily (Section 4.7; Table 1). Although local wind events appear to be

Fig. 6. Histograms showing burial and exposure of Highborne Cay stromatolites. A) Total largely responsible for sediment transport along the reef tract, time exposed versus total time buried. B) Duration of exposure events. C) Duration of attempts to predict burial patterns based on wind speed and direction burial events. Month-long events are N30 days; week-long events are 7–30 days; daily were unsuccessful as a result of complex reef topography (Mitsu events are b7 days in duration. Ogihara, personal communication). Additional studies by Kromkamp et al. (2007) and Perkins et al. (2007) support field observations of mat responses to wave action, be driven, at least in part, by the extrinsic factors of water temperature abrasion and sediment movement (Table 1). Specifically, these studies and/or PAR, which also exhibit strong seasonal trends (Fig. 3; Table 1; showed that diatom and Phormidium mats were eroded under strong Supplemental Fig. S1). Stalked diatom mats showed the strongest wave action and did not survive abrasion or burial, whereas positive correlation to temperature, with increasing abundance from 23 Schizothrix, biofilm and Solentia mats thrived under strong wave to 31 °C. This mat type formed when water temperature was N27 °C but action, and survived abrasion and burial. once established, persisted to temperatures as low as 24 °C; stalked Taken together, the results from the 2005 to 2006 field-monitoring diatom mats were most abundant at water temperature N26 °C. A program at Highborne Cay coupled with data from the concurrent positive correlation to temperature was also found for heterotrophic studies provide evidence that surface mats on stromatolites respond biofilms (25–31 °C), Phormidium mats (28–30 °C), and Solentia mats to both seasonal (i.e., temperature and PAR) and stochastic wind and (20–31 °C). Biofilms were particularly abundant in summer 2005, when wave-related events. Mats exist within specificenvironmental water temperatures were N28 °C and PAR was N600 μmol m−2 s−1. conditions and transitions between mat types coincide with changes Tube diatom mats showed the strongest negative correlation, with in these conditions. decreasing abundance from 20 to 31 °C. These mats formed as pustular Synthesis of environmental and mat type records at two specific blankets at temperatures b26 °C and as stringy pustules in temperature markers (N1.2, at Site 1 and N8.6orange, at Site 8; Fig. 9)providesabasis ranges N26 °C. Schizothrix mats, which ranged from 20 to 31 °C, also for interpreting depositional scenarios at the two sites and speculating on showed a negative correlation with temperature. factors causing transitions from one mat type to another. At Site 1 where In contrast to temperature, which showed both positive and the microbial communities on the surfaces of stromatolites at marker negative correlations with mat type, only one mat type, the N1.2 during 2005 and 2006 included Solentia, Schizothrix,stalkedand heterotrophic biofilm, showed a significant positive correlation with tube diatoms and Phormidium mats (Fig. 9), Solentia mats transitioned to 52 E.M. Bowlin et al. / Sedimentary Geology 263-264 (2012) 45–55

A B

1 cm 1 cm

C JFMAFMAMJJ JSOND A A M J JSOND

1 Site Site

2005 2006 Site 8 Site

JFMAFMAMJJ JSOND A A M J JSOND Rita Wilma Schizothrix mat Solentia mat stalked diatom mat heterotropic Phormidium mat tube diatom mat

Fig. 7. Mats at Site 1 and Site 8 during 2005 and 2006. A) Stalked diatom mat at Site 1, September 7, 2005. B) Schizothrix mat at the same location as (A) on September 21, 2005, two days after Tropical Storm Rita, which eroded the diatom mats; arrows in (A) and (B) mark the same location. C) Bar graphs showing mat types at N1.2 (Site 1; upper graph) and N8.6orange (Site 8; lower graph). Note that diatom mats are abundant at Site 1 and rare at Site 8; Site 8 is dominated by classic Schizothrix, heterotrophic biofilm and Solentia mats.

tube diatom mats (i.e., pustular blanket) in March 2005, when water mat. Stalked and tube diatoms colonized the surface of these mats during temperatures reached 22 °C. A burial event in late March 2005 killed the October and early November 2005, until temperatures fell below 27 °C. diatoms, and the underlying crusty Solentia mat was unburied in June For most of November and December 2005, when temperatures were 2005. In July 2005, with temperatures above 29 °C, stalked diatom mats less than 27 °C and PAR values were less than 400 μmol m−2 s−1, formed a yellow fuzz on the Solentia mats, with a base layer of Schizothrix. Solentia was the dominant mat type. In January 2006, when PAR values The yellow fuzz was eroded in late July 2005, possibly related to a wind started to rise, Schizothrix mats then became dominant. When PAR values event, exposing the underlying Schizothrix mat. Stalked diatoms reached 500 μmol m−2 s−1 and temperature was 24 °C, tube diatoms developed again and flourished until late September 2005, when they formed pustular blankets. During a period of long exposure, stalked were again eroded by high winds associated with the passage of Tropical diatom mats became dominant in June 2006, when water temperatures Storm Rita, once again exposing the underlying firmly-bound Schizothrix were above 27 °C. A brief episode of colonization by Phormidium at

ACB 100 100 100 Schizothrix Heterotrophic biofilm Solentia 80 80 80

60 60 60

40 40 40

20 20 20 Percent Abundance Percent Abundance Percent Abundance 0 0 0 JFMAMJJASONDJFMAMJJASOND JFMAMJJASONDJFMAMJJASOND JFMAMJJASONDJFMAMJJASOND 2005 2006 2005 2006 2005 2006 D EF 100 100 100

80 Stalked diatom 80 Tube diatom 80 Phormidium

60 60 60

40 40 40

20 20 20 Percent Abundance Percent Abundance Percent Abundance 0 0 0 JFMAMJJASONDJFMAMJJASOND JFMAMJJASONDJFMAMJJASOND JFMAMJJASONDJFMAMJJASOND 2005 2006 2005 2006 2005 2006

Fig. 8. Histograms indicating the seasonal distribution of each of the six mat types for the 43 stromatolite markers during 2005 and 2005: A) Schizothrix mats, B) heterotrophic biofilms and micritic crusts, C) Solentia mats; D) stalked diatoms mats, E) tube diatom mats, and F) Phormidium mats. Mat abundance indicates the percent of total observations represented by each mat type for each week. E.M. Bowlin et al. / Sedimentary Geology 263-264 (2012) 45–55 53

Table 1 Observed relationships between mat type and environmental factors. Pearson correlation coefficients (r) with p valuesb0.05 are significant. Relationships between mat type and wave action, abrasion and burial are anecdotal based on field observations; impacts are characterized as positive or negative: ++ mat thrived; + mat survived;− mat deteriorated or died.

Water temp °C PAR μmol m− 2 s− 1 Wind speed m/s Wave action Burial Abrasion

Schizothrix Range 20–31 200–650 2–12 ++ + − Pearson r (r=−0.353, n=96, p=b0.001) (r=−0.040, n=84, p=0.719) (r=−0.057, n=84, p=0.606) Biofilm Range 25–31 400–650 4–8 ++ + ++ Pearson r (r=0.255, n=96, p=0.012) (r=0.322, n=84, p=0.003) (r=−0.066, n=84, p=0.549) Solentia Range 20–31 200–650 2–11 ++ + ++ Pearson r (r=0.212, n=96, p=0.045) (r=−0.161, n=84, p=0.144) (r=0.196, n=84, p=0.073) Tube diatom Range 20–31 250–650 2–11 −−− Pearson r (r=−0.433, n=96, p=b0.001) (r=−0.028, n=84, p=0.801) (r=−0.103, n=84, p=0.350) Stalked diatom Range 23―31 200―650 2―12 −−− Pearson r (r=0.542, n=96, p=b0.001) (r=−0.008, n=84, p=0.943) (r=0.051, n=84, p=0.652) Phormidium Range 28―30 500―600 4―8 −−− Pearson r (r=0.236, n=96, p=0.021) (r=0.173, n=84, p=0.115) (r=−0.053, n=84, p=0.633) temperatures of about 28 °C was abruptly ended by a burial event in July, stalked diatom mats developed on the crusty Solentia mats. The stalked which eroded the Phormidium and stalked diatom mats. Stalked diatom diatom mats were negatively impacted during a burial event associated mats recolonized and were dominant through October 2006; when with Tropical Storm Rita in late September 2005. Heterotrophic biofilm temperature dropped below 27 °C, tube diatoms mats then became mat appeared to withstand the sand-level abrasion event and remained dominant again in November 2006. The transition to Solentia mats in dominant for most of October 2005. Burial and cooling associated with December 2006 corresponded to temperatures below 24 °C and PAR the passage of Tropical Storm Wilma corresponded to a transition to values about 300 μmol m−2 s−1. Schizothrix mats. The stromatolites were buried from December 2005 to A second example at Site 8 revealed a markedly different scenario May 2006, with Schizothrix mats dominant during brief exposed compared with that at Site 1. Mats at marker N8.6orange were intervals. In May 2006, with sand-level abrasion and water temperature primarily comprised of Schizothrix, heterotrophic biofilm and Solentia above 26 °C, a biofilm mat developed on the surface. In June 2006, with mats, with only one occurrence of stalked diatom mat in Sept 2005 continued exposure of the biofilm, a crusty Solentia mat formed below (Fig. 9). Schizothrix mats transitioned to biofilm mats in August 2005, the micritic crust. In June and July of 2006, during calm weather without which corresponded to a sand-level abrasion event and water abrasion, Schizothrix mats formed. Another heterotrophic biofilm temperatures above 29 °C. After 1–2 weeks, a Solentia crust developed formed during sand-level abrasion in late July 2006, with an eventual on the surface. After 3 weeks exposure and temperatures N29 °C, development of a Solentia mat in early August 2006. A burial event in

2005 2006

30 600 -1 s

28 -2 500 26 400 24 Temperature °C 300 PAR µmol m 22

20 200 Site 1

JFMAFMAMJJ JSOND A A M J JSOND Site 8

JFMAFMAMJJ JSOND A A M J JSOND 2005Rita 2006 Wilma BURIAL STATEATTYPE M exposed sand level Schizothrix mat stalked diatom mat buried no data heterotropic biofilm tube diatom mat Solentia mat Phormidium mat

Fig. 9. Synthesis of environmental and mat-type records at N1.2 (Site 1) and N8.6orange (Site 8) during 2005 and 2006. 54 E.M. Bowlin et al. / Sedimentary Geology 263-264 (2012) 45–55

Unlithified grain layers

Schizothrix long exposure with abrasion T= 20-31 °C temp <27 °C PAR= 200-650 µmol m-2 s-1 and temp >25 °C better if temp >28 °C or

abrasion with cold water (too cold for ) temp < 24 °C PAR < 400 µmol m-2 s-1 strong wind stalked diatom tube diatom or prolonged exposure, prolonged exposure, burial temp >27 °C temp <22 °C

Unlithified stop abrasion spring rise in grain layers or temp and PAR temp <25 °C Diatom stalk T= 23-31 °C, PAR= 200-650 µmol m-2 s-1 strong wind or tube T= 20-31 °C, PAR= 200-650 µmol m-2 s-1 burial

tube diatom stalked diatom prolonged exposure, prolonged exposure, Solentia temp <22 °C temp >27 °C Heterotrophic T= 20-31 °C Biofilm PAR= 200-650 µmol m-2 s-1 T= 25-31 °C PAR= 400-650 µmol m-2 s-1

Fused grain layers Micritic crusts prolonged periods of abrasion

Fig. 10. Summary of observed transitions between mat types on the surfaces of modern marine stromatolites and environmental factors responsible for these transitions; pb pustular blanket; sp stringy pustules; wk week.

August 2006 was followed by the growth of a Schizothrix mats in Water temperature and/or PAR are likely responsible for transitions September–October 2006. between Schizothrix and Solentia,withwatertemperaturesb24 °C and These temporal and spatial mat distributions coupled with the PAR b400 μmol m−2 s−1 favoring development of Solentia mats.Similarly observed transitions from one mat type to another at Sites 1 and temperature and PAR drive transitions between Schizothrix or Solentia and 8 indicate the importance of environmental controls (Table 1) in diatom mats, with temperatures N22 °C and PAR N500 μmol m−2 s−1 determining mat type and community cycling and provide a favoring tube diatoms, and temperatures N25 °C favoring stalked diatoms. fundamental basis for developing an integrated model of community Burial and wind events are also linked to transitions between cycling. (1) stalked diatom, tube diatom or Phormidium mats and (2) Schizothrix or Solentia mats. The eukaryotic diatoms cannot survive burial (Kromkamp et al., 2007; Perkins et al., 2007). Similarly the 6. Discussion and conclusions soft, loosely bound diatom and Phormidium mats are easily eroded by wave action at wind speeds greater than 10 m/s. Transitions between mat types on the surfaces of Highborne Cay Based on the model above, mat cycling on the surfaces of stromatolites and the likely causes for cycling between them are Highborne Cay stromatolites is driven by a combination of predict- summarized in Fig. 10; Phormidium mats are not included in the able environmental factors (temperature, PAR) and stochastic events summary diagram because insufficient data are available on cycling (storms, burial, abrasion). These results provide a theoretical basis between Phormidium and other mat types. Most transitions can be for predicting stromatolite lamination. Previous studies have linked to extrinsic factors such as abrasion, burial, wave action, and recognized three primary means by which surface mat communities changes in water temperature, and to a lesser extent PAR. contribute to stromatolite growth: 1) trapping and binding to form Schizothrix can be considered the default mat type, or the “stable state unlithified grain layers; 2) precipitation of micrite layers/crusts, and community” (Stolz et al., 2009)ofHighborneCaystromatolites.Rapid 3) microboring and reprecipitation to form fused grain layers (Reid et burial and exposure in a sand-level abrasion zone, combined with water al., 2000; Stolz et al., 2009). Schizothrix as well as the diatom temperatures N25 °C (preferably N28 °C) caused Schizothrix mats to communities contribute to trapping and binding, with rapid transition to heterotrophic biofilms with precipitation of micritic crusts. accretion characterizing stalked diatom mats (Stolz et al., 2009; Formation of EPS-rich biofilms in high-energy abrasion zones is Franks et al., 2010). Given the general abundance of stalked diatom consistent with reports that EPS serves to physically stabilize microbial communities during mid summer to fall, high rates of trapping and cells (De Winder et al., 1999; De Brouwer and Stal, 2002). Heterotrophic binding are predicted during this time period. degradation of EPS has, moreover, been linked to carbonate precipitation In contrast, lithified layers in modern marine stromatolites are (Decho et al., 2005; Dupraz and Visscher, 2005; Dupraz et al., 2009)and predicted to have both seasonal and stochastic distributions. Precipitation formation of thin micritic crusts within the biofilms. of micritic crusts is associated with heterotrophic biofilm communities E.M. Bowlin et al. / Sedimentary Geology 263-264 (2012) 45–55 55 that form May through September and thus record the summer season. Decho, A.W., Visscher, P.T., Reid, R.P., 2005. Production and cycling of natural microbial fi exopolymers (EPS) within a marine stromatolite. Palaeogeography, Palaeoclimatology, However, abrasion is also required for bio lm formation, in addition to Palaeoecology 219, 71–86. high water temperature, and many monitoring sites at Highborne Cay did Dill, R.F., Shinn, E.A., Jones, A.T., Kelly, K., Steinen, R.P., 1986. Giant subtidal stromatolites not develop heterotrophic biofilms during the summer. Thus micritic forming in normal salinity waters. Nature London 324 (11), 55–58. Dravis, Jeffrey J., 1983. Hardened subtidal stromatolites, Bahamas. Science 219, crusts represent summer events, but constitute an inconsistent seasonal 385–386. record. Dupraz, C.D., Visscher, P.T., 2005. Microbial lithification in marine stromatolites and Fused grain layers formed by the Solentia mat communities are hypersaline mats. Trends in Microbial Ecology 13, 429–438. similarly unpredictable. Solentia mats form as a result of two very Dupraz, C., Reid, R.P., Braissant, O., Decho, A.W., Norman, R.S., Visscher, P.T., 2009. Processes of carbonate precipitation in modern microbial mats. Earth Science different processes: 1) transition from a heterotrophic biofilm due Reviews 96, 141–162. to prolonged abrasion or 2) transition from a Schizothrix mat most Eckman, J.E., Andres, M.S., Marinelli, R.L., Bowlin, E.M., Reid, R.P., Aspden, R.J., Paterson, likely due to a drop in temperature and/or PAR. We therefore D.M., 2008. Wave and sediment dynamics along a shallow subtidal sandy beach inhabited by modern stromatolites. 6 (01), 21–32. predict 1) summer Solentia layers that are closely associated with Foster, J.S., Green, S.J., 2011. Microbial diversity in modern marine stromatolites. In: micrite layers formed by the heterotrophic biofilm community and Tewari, V., Seckbach, J. (Eds.), Stromatolites: interactions of microbes with 2) winter Solentia layers that separate trapped and bound sediment sediments. : Cellular Origin, Life in Extreme Habitats and Series, 18. Springer Publishing, New York, NY, pp. 385–405. are likely associated with a Schizothrix mat community. Thus, Foster, J.S., Green, S.J., Ahrendt, S.R., Golubic, S., Reid, R.P., Hetherington, K.L., Bebout, L., although microbial mat cycling at Highborne Cay is strongly 2009. Molecular and morphological characterization of cyanobacterial diversity in influenced by seasonal changes, the resulting laminations do not the marine stromatolites of Highborne Cay, Bahamas. The ISME Journal 3, 573–587. Franks, J., Reid, R.P., Aspden, R.J., Underwood, G.J.C., Paterson, D.M., Stolz, J.F., 2010. Ooid provide a consistent seasonal record. accreting diatom communities from the modern marine stromatolites at Highborne Verification of our theoretical predictions of lamination awaits Cay, Bahamas. In: Seckbach, J., Oren, A. (Eds.), Microbial Mats: Modern and Ancient results from a companion study of stromatolite accretion, which is in Stratified Systems. : Cellular Origin, Life in Extreme Habitats and Astrobiology Series, 14. Springer Publishing, New York, NY, pp. 277–285. presently in preparation. As part of the monitoring program at Gaspar, A.P., 2007. Stromatolites: unique seascapes of the Bahamas—Multiscale Highborne Cay, marker pigments were periodically added to surface mapping and management guidelines for a living example of an ancient ecosystem. mat communities. The resulting subsurface record will show how the MS Thesis, University of Miami, Coral Gables, Florida. various mat communities are preserved in the rock record (Bowlin, Grotzinger, J.P., Knoll, A.H., 1999. Stromatolites in Precambrian carbonates; evolutionary mileposts or environmental dipsticks? Annual Review of Earth and Planetary Sciences 2011). 27, 313–358. In summary, an intensive two-year monitoring program documenting Kromkamp, J.C., Perkins, R., Dijkman, N., Consalvey, M., Andres, M., Reid, R.P., 2007. Can microbial mats on the surfaces type of modern marine stromatolites at cyanobacteria survive burial? Aquatic Microbial Ecology 48, 123–130. Macintyre, I.G., Reid, R.P., Steneck, R.S., 1996. 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