DISCUSSION MICROBIALITE FORMATION IN SEAWATER OF INCREASED ALKALINITY, SATONDA CRATER LAKE, INDONESIA—DISCUSSION JO´ZEF KAZMIERCZAK1 AND STEPHAN KEMPE 2 1
Institute of Paleobiology, Polish Academy of Sciences, Twarda 51/55, PL-00818 Warsaw, Poland e-mail:
[email protected] 2 Institute for Applied Geosciences, Technical University Darmstadt, Schnittspahnstrasse 9, D-64287 Darmstadt, Germany
Arp et al. (2003) present data which confirm and refine the results of our long-time studies (field campaigns of 1986, 1993, 1996) on Satonda Crater Lake (summarized in Kempe and Kazmierczak 1993). They reiterate the importance of marine stratified water bodies in generating, through sulfate reduction, excess alkalinity, which in turns causes very high CaCO3 supersaturation levels. This geochemical process, called the alkalinity pump (Kempe 1990), was conceptually refined using the quasi-marine Satonda Lake as a geochemical model for some epicratonic marine basins from the geological past (Kempe and Kazmierczak 1994). The concept of an alkalinity pump is important for understanding the abundance of calcified benthic cyanobacterial mats in ancient shallow seas leading to the formation of a variety of marine calcareous microbialitic structures and fine-grained calcareous sediments accumulated on the seafloor (Kempe and Kazmierczak 1990; Kazmierczak et al. 1996). While principally agreeing with Arp et al.’s results, we strongly disagree with two of their major conclusions. The first major objection concerns Arp et al.’s scepticism with respect to the calcification potential of benthic cyanobacterial mats presently living in the lake. On the basis of samples gathered in 1993 and 1996, Arp et al. conclude that these mats calcify very weakly or, in some cases, do not calcify at all. This sharply contradicts our observations showing strong permineralization of the mats both with CaCO3 and silica (e.g., Kempe and Kazmierczak 1993, Pl. 6, figs. 3–6). Mat samples we took at the end of dry season 1986 demonstrate that calcification of the cyanobacteria occurred in vivo. Masses of minute grains of CaCO3 (predominantly Mgcalcite) were observed not only on the mat surface but also within the common mucilage sheaths (glycocalyx) surrounding aggregates of living cyanobacterial coccoid cells (classified as representatives of Pleurocapsales). Minute CaCO3 grains were even observed on siliceous sponge spicules dispersed over the cyanobacterial mats. SEM pictures of surface and cross sections of the living coccoid cyanobacterial biofilm (Fig. 1A, B) show that, although patches of calcium carbonate grains cover the mat surface, most precipitated CaCO3 occurs within the mucilage as densely packed submicrometer-size granules (Fig. 1A inset, F). This makes the mucilage relatively stiff and resistant to desiccation collapse, as evidenced by the air-dried sample shown in Figure 1A. Our observations indicate that CaCO3 mineralization of cyanobacterial biofilms in Satonda Lake is not directly linked to their photosynthetic activity, as is widely accepted for in vivo calcifying cyanobacterial mats (see, e.g., Merz 1992). Rather, CaCO3 precipitates inside of the common mucilage sheaths (glycocalyx) and only occasionally on the biofilm surface, as visible in our 1993 samples (Fig. 1C, D). A similar mode of CaCO3 precipitation inside the mucilage has been noticed in other in vivo calcified cyanobacterial mats and biofilms (Cohen et al. 1977; Jørgensen et al. 1983; Fenchel and Ku¨hl 2000; Kazmierczak et al. 2001; Paerl et al. 2001; Dupraz and Reid 2002; Ku¨hl et al. 2003). In at least some of these examples, organically controlled precipitation occurs in the mucilage, forming granular submicron CaCO3, followed by abiotic precipitation of more crystalline forms, such as aragonite needles. CaCO3 precipitation on the biofilm requires the photosynthetic uptake of CO2 and /or HCO3– coupled with other environmental factors, like high JOURNAL OF SEDIMENTARY RESEARCH, VOL. 74, NO. 2, MARCH, 2004, P. 314–317 Copyright q 2004, SEPM (Society for Sedimentary Geology) 1527-1404/04/074-314/$03.00
Ca 21, pH, and alkalinity levels, which, together, create extremely high supersaturation with respect to the solubility products of calcium carbonate minerals. Therefore, not all in vivo calcifying cyanobacterial biofilms show CaCO3 precipitates on their surfaces, and microscale differences in intensity of this process are visible even on more or less contemporaneously growing colonies (cf. Fig. 1C, D). Arp et al.’s samples, on which their conclusions concerning the weak or lacking calcification potential of Satonda Lake benthic cyanobacteria rest, were taken at the end of the dry season in 1993 and mostly from the end of the wet season in 1996. At the latter time the epilimnion was apparently diluted significantly and had a lower CaCO3 supersaturation during the preceding months than during the dry-season sampling. But even during that time surfaces of some older living cyanobacterial colonies were covered densely with in vivo precipitated granular Mg-calcite whereas others, newly grown, remained free of mineral precipitates. These seasonal alterations in epilimnion calcium carbonate supersaturation level produce, according to our interpretation (Kempe and Kazmierczak 1993; Kazmierczak and Kempe 1990, 1992), the characteristic fine lamination of Satonda Lake microstromatolites composed of aragonitic layers alternating with calcitic layers (the latter often with some admixture of SiO2 or Mg-silicate). The potential of Satonda Crater Lake to support an in vivo calcification of benthic cyanobacterial mats thriving there throughout the year is further supported by our exposure experiments. Platelets of various materials were exposed to the lake water for a period of almost three years (1993–1996). Coccoid cyanobacterial biofilms, up to one millimeter thick, overgrew glass and limestone platelets (Fig. 1E). They are distinctly permineralized with ultra-small granules of Mg-calcite (Fig. 1F, G) similar to those observed permineralizing the 1986 mats (Fig. 1A inset). It is therefore possible that in 1986 more severe evaporative conditions prevailed and a higher CaCO3 supersaturation existed in the lake epilimnion than between 1993 and 1996, and that the mineralization of cyanobacterial biofilms in 1996 was weaker compared to the samples recovered 10 years earlier. Arp et al.’s questioning the potential of present-day Satonda Lake to support cyanobacterial calcification curiously contradicts the title of their own paper, announcing boldly ‘‘microbialite formation in seawater of increased alkalinity.’’ Because by definition (e.g., Kennard and James 1986) ‘‘microbialite’’ denotes in this case a biosedimentary structure originated by microbially induced mat mineralization, the logic of the authors’ message is rather difficult to understand. The second major point we criticize is Arp et al.’s (2003) attempt to reinterpret the cystous subfossil calcareous structures from Satonda Crater Lake, which we described (Kazmierczak and Kempe 1992) as modern cyanobacterial counterparts of microfossils known as Wetheredella or Wetheredella-like forms, as gemmules of suberitid sponges. This reinterpretation is unfounded and easily refutable. Gemmules are sponge reproductive structures that can survive adverse conditions, such as desiccation or extreme cold. They are not typically produced by marine sponges. As a rule, in the marine tropical realm sponges propagate sexually. Typical gemmules are equally-size spherical or subspherical bodies encased in a double or triple layer of collagenous substance (spongin) armored often with spicules (for
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FIG. 1.—SEM photomicrographs showing examples of calcium carbonate permineralized cyanobacterial (pleurocapsalean) biofilms from Satonda Crater Lake sampled during field campaigns 1986, 1993, and from plates exposed to the water column from 1993 to 1996. A) Surface and cross section of an air-dried biofilm sampled at the end of dry season 1986 (sample S-23, depth 11.3 m). The surface is sparsely covered with anhedral grains of Mg-calcite whereas the main mass of calcium carbonate precipitated by the mat occurs within the common mucilage sheaths (glycocalyx) as densely packed ultra-small grains of Mg-calcite (see inset photograph). The holes in this picture represent spaces occupied in freshly sampled biofilm by the coccoid cells. B) Highly magnified fragment of air-dried biofilm surface showing outlines of the coccoid cells and submicrometer size of the in vivo precipitated CaCO3 grains. C) Surface of an air-dried living pleurocapsalean biofilm sampled at the end of dry season 1993 (sample S-311, depth 19 m). The surface is covered densely with in vivo precipitated anhedral grains of Mg-calcite. D) Surface of air-dried freshly grown pleurocapsalean biofilm from the same depth without CaCO3 precipitates. The ovoid depressions represent encapsulated coccoid cells. E) Surface of pleurocapsalean biofilm grown on a piece of limestone exposed to the lake water between fall 1993 and summer 1996 at a depth of 7 m. F) The common mucilage sheaths (glycocalyx), which surround groups of cells, are strongly permineralized with ultra-small grains of Mg-calcite and silica as indicated in by the EDS spectrum shown in G) taken from the window indicated in F); the EDS spectrum shows a dominance of Ca and Mg with only small amounts of Si. The Mg/Ca ratio is indicative of high-Mg calcite. All samples have been air-dried. Scale bars: A) 10 mm (inset 1 mm), C, D) 10 mm, B, F) 2 mm, E) 50 mm.
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FIG. 2.—Examples of subfossil silicified Wetheredella-like structures from Satonda Crater Lake identified as permineralized colonies of modern capsular coccoid cyanobacteria. All pictures represent transmitted-light micrographs of vertical thin sections (sample S-288, depth 10 m). A) A group of Wetheredella-like hemispheric calcareous and siliceous cysts gradually growing up from a silicified layer of capsular cyanobacteria (indicated by red arrow heads). B) Magnification of a cyst with distinct envelope (indicated by arrow). The cyst is filled with fibrous aragonite with a silicified cluster of coccoid cyanobacterial cells preserved at the base (red arrow head). C) A cluster of capsular bodies from the silicified layer of pleurocapsalean cyanobacteria shown in Part A). D) Two silicified Wetheredella-like cystous structures with remnants of dense aggregates of coccoid cyanobacterial cells preserved inside; note the well preserved envelopes (arrows). E, F) Two examples of silicified Wetheredella-like cysts with well-preserved silicified remnants of encapsulated structures directly comparable to colonies of modern coccoid cyanobacteria. Arrows indicate thick envelopes surrounding capsular remains of highly degraded pillow-like coccoid colonies. Scale bars: A) 500 mm; B, D) 100 mm; C, E) 50 mm; F) 20 mm.
DISCUSSION details see Simpson and Fell 1974). Arp et al. fail to demonstrate that the Wetheredella-like structures they illustrate show any of these features. Not excluding the possibility of gemmule production by suberitid sponges (Connes et al. 1978), even by those living in Satonda Lake, clear-cut evidence should have been presented. Concerning the large population of sponges in the lake, it should be easy to find their living gemmules, if such exist, and to illustrate all of their typical features. Because fossilization potential of the collagenous walls of gemmules, as in most collagenous substances, is low, it would however be difficult to find identifiable remnants of these structures in fossil or even subfossil state. The calcareous structures we described from Satonda Lake as analogs of the Paleozoic Wetheredella are of varying size and shape and of incomplete circumference, lacking a structured wall and often passing gradually into horizontal microstromatolitic laminae (cf. Fig. 2A). In light of our previous observations (Kazmierczak and Kempe 1992) we can now confirm, on the basis of new findings from Satonda Lake, that the variety of ancient structures similar to Wetheredella and Wetheredella–like microfossils (e.g., Helm and Schu¨lke 1998; Rodriguez and Gutschick 2000) may represent cystous or pillow-like growth stages of colonies of benthic coccoid cyanobacteria resembling representatives of such modern genera as, for example, Chlorogloea, Myxosarcina, or Xenococcus known from marine and fresh-water biotopes (cf. Koma´rek and Montejano 1994; Koma´rek and Anagnostidis 1999). A variety of different preservational stages of coccoid colonies can be observed in the newly studied samples. Some cysts are completely silicified, showing whole or partial preservation of capsules or even individual coccoid cells (Fig. 2C, D, F). Some are partly filled with pure silica (Fig. 2E), whereas in others aragonite replaces tightly packed clusters of original minute cells (Fig. 2B). It should also be stressed that the gradual transition of the Wetheredella-like coccoid cyanobacterial cystous bodies into well-laminated microstromatolitic structures visible in many places in Satonda Lake microbialites (Fig. 2A) strengthens our earlier suggestion (Kazmierczak and Kempe 1990) that Satonda microstromatolic structures may also represent modern analogs for other common enigmatic Paleozoic fossils described as stromatoporoids. REFERENCES ARP, G., REIMER, A., AND REITNER, J., 2003, Microbialite formation in seawater of increased alkalinity, Satonda Crater Lake, Indonesia: Journal of Sedimentary Research, v. 73, p. 105– 127. COHEN, Y., KRUMBEIN, W.E., AND SHILO, M., 1977, Solar Lake (Sinai). 4. Stromatolitic cyanobacterial mats: Limnology and Oceanography, v. 22, p. 635–656. CONNES, R., CARRIE`RE, D., AND PARIS, J., 1978. E`tude du development des gemmules chez la demosponge marine Suberites domuncula (Olivi) Nardo: Annales des Sciences Naturelles, Zoologie, Paris, v. 20, p. 357–387.
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