Biological participation in the global carbonate cycle

Report

The carbonate cycle can be subdivided conveniently into two subcycles — the carbonate cycle sensu stricto (left figure) and the carbonate – silicate cycle (right). In both figures the continents are on the left side, and the ocean is on the right. The asterisks indicate where the involvement of life is prominent.

In broad principle, the carbonate – silicate cycle operates as follows. On the continents, large quantities of calcium silicate (CaSi0) are exposed as components of continental rocks. In the presence of air and water this substance is unstable; it readily weathers awaу and dissolves in ground water. In that process, two units of carbon dioxide, or CO₂, are taken up from the air per unit of calcium silicate. The dissolved weathering products, two units of bicarbonate (ICI;), one of calcium (Ca++) and one of silicic acid (Н₄SiO₄) are transported by rivers from the continents into the ocean. If the ocean were only taking up these materials, its composition would continuously change over time, and this is not what happens. To maintain the chemical balance of the oceans, the materials that enter the ocean have to leave it in equal amounts. In seawater, calcium and bicarbonate react to form limestone (CaC0) and CO₂. The limestone is deposited on the ocean floor and the CO₂ goes into the atmosphere. The silicic acid comes out of the ocean by sedimentation of silica (Si0₂) on the ocean floor. Note, incidentally, that magnesium may substitute for calcium in both subcycles; this is not indicated in the figures.

It is at this point that the forces in the deep earth come into play. The ocean floor slides under the continent and the sediments on top of it are heated under enormous pressures in depth. Under these conditions the limestone and silica react on their turn to form calcium silicate and CO₂. The CO₂ escapes roto the atmosphere through volcanoes, and the calcium silicate moves to the continental surface. A new cycle can begin. All the compounds in the system are recycled and nothing is lost. Consider, for example, CO₂. Weathering uses up two units of that compound, and these are subsequently returned to the atmosphere: one upon the formation of limestone and the other one through the volcanoes. Consequently, the system may run unchanged for billions of years. Yet, as we shall see, important changes have occurred in this system over geological time.

Atmospheric CO₂ is widely known as an important greenhouse gas. The Earth’s climate becomes warmer as the concentration of CO₂ increases. Another aspect to remember is the fact that this scheme consists of two compound processes, which operate on entirely different time scales. Whereas weathering and sedimentation equilibrate within a few thousand years, the processes in the deep earth work on time scales of millions of years. Hence, these two processes are uncoupled, so that the quantity of CO₂ released by the volcanoes is independent of what happens on the surface of the continents and in the oceans. Suppose now that the Earth is cool, and that the volcanoes blow a large quantity of CO₂ into the atmosphere. Climate will warm up as a result. At higher temperatures all chemical reactions speed up. This general rule will also apply to weathering. Hence, this process will tend to consume the extra CO₂. Thus, the carbonate — silica cycle operates as a regulatory mechanism of the global climate, a thermostat for the entire earth. Deviations of the СО₂-content in the atmosphere are automatically counterbalanced.

The carbonate cycle sensu stricto (left figure) is relatively simple in its operation. Instead of calcium silicate, continental limestone (СаС0₃, calcium carbonate) is weathered, and this process removes only one unit of CO₂ from the atmosphere. The reaction products, bicarbonate and calcium ions, are washed by runoff into the ocean and subsequently removed by carbonate sedimentation and the re-emission of CO₂ into the atmosphere. To close the cycle, the continental carbonate reservoir is replenished by uplifting. Note that volcanism plays no role in this cycle, and that this system cannot function as a long-term thermostat, because all the CO₂ removed by weathering is readily returned by the CO₂ emissions related to limestone sedimentation.

The role of life in weathering

The cycles illustrated in Fig. !a and b can, in principle, operate in the absence of life. But on the modern Earth, and throughout most of Earth history, biology has played important roles in the weathering of continents as well as the precipitation of CaCO₃ and Si0₂ in the oceans. Organisms and soils are major reservoirs of carbon, and the organic carbon and carbonate carbon buried in modern seafloor sediments are almost exclusively of biological origin. In consequence, life is crucial to long-term environmental control (including the control of climate), and evolutionary innovations may be considered as principal agents of change in Earth’s environmental history.

As soon as rocks appear on the continental surface, they are immediately overgrown by microorganisms, lichens and finally vascular plants. These organisms concur in extracting the nutrients on which they depend from the minerals. A versatile array of mechanisms are dеployed to fragment the rocks and suck the precious nutrients out of them until a soil, a life­bearing mash of clay and land is left over. As the retrieved nutrients are passed on from one organism to the next one, they distribute themselves over the entire continent and finally fertilize the ocean. Weathering is the mining for life, and we all join in the eating.

We already saw that calcium silicate reacts with CO₂. But the atmosphere contains only vert’ little of this gas. The organisms involved in weathering suck the CO₂ out of the air and pump it into the ground. Thus, on a micro-scale, the CO₂­concentration in the sol mash mat’ increase enormously. The asterisk in figure 3 means that this biological activity speeds up the degradation of calcium silicate. Now, suppose again that the earth is cold. The weathering organisms are relatively inactive. A sudden emission of СО2 from the volcanoes increases the temperature, an immediate outburst of biotic aсtivity follows, weathering rates increase and atmospheric СО2 decreases. As a result, the global thermostat is far more efficient than without life.

Trend in weathering rates over geological time

At the meeting, Robert Berner discussed his GEоCARB model (Berner, 1991, 1994) that attempts to quantify the various processes affecting the weathering component of the silicate — carbonate cycle. These processes include (1) the uplift of mountains as they affect relief, climate and silicate weatherability; (2) the rise and evolution of vascular plants as thеy affect the rate of silicate weathering; (3) changes in size and position of the continents as they affect rainfall and temperature on land; (4) the evolution of the sun as it affects global warming; and (5) variations of atmospheric СО2 as they affect plant growth and global temperature plus river runoff via the atmospheric greenhouse effect. The model predicts as a likely scenario, that in the period from 600 to 450 million yеars ago the concentration of atmospheric CO₂ was 15 to 20 times as high as today. Then, between 450 and 300 million yеars ago, there was a sudden decrease until the present level is reached. This minimum corresponds with the Permo­Carboniferous ice age. During the subsequent Mesozoic there was a relatively modest rise in CO₂, and in the Tertiary CO₂ decreased again until the present ice age was reached. The model indicates that the spectacular decrease of CO₂ between 450 and 300 million years ago was caused by the origin and evolution of the vascular plants. It was in this period that extensive woods began to civet the continents. The plants with their deep roots and evapo-transpiration aсtivity are indeed capable of enhancing weathering rates considerably. Berner estimated from field studies that plants increase weathering rates by a factor between 3 and 7.

Nico van Breemen (Wageningen University, the Netherlands) highlighted the effect of ectomycorrhizal fungi, which have a symbiotic relationship with plant roots. Hе showed that weatherable minerals in podzol soils are often perforated by many open, tubular pores, 3-10 min width. The pores would be formed by complex-forming, low-molecular weight organe acids exuded by the fungal hyphae. These mycelia greatly extend the surface area for the absorption of nutrients. Thеy create microsites which are inaccessible to plant roots and isolated from bulk soil solution phenomena. The retrieved nutrients would be transferred to the host plant roots, bypassing the soil solution and avoiding competition for nutrient uptake by other organisms. These observations would provide further support to the idea that plant growth enhances weathering rates. Surprisingly, however, recent studies in New England, USA, by van Breemen and his collaborators did nit confirm their earlier conclusion that ectomycorrhizae play an important role in weathering.

Sierd Cloetingh (Free University, Amsterdam) and Marc Budding (Bloemendaal, the Netherlands) discussed the effect of tectonics and the relief of the earth surface on the rates of weathering and transport of weathering products to the ocean. Relief is required for the transport and repeated exposure of rocks while thеy are transported down slope towards the ocean. In principle, weathering may be strongly reduced in the absence of relief, even when vegetation is heavy. Weathering would then be strongly activated by tectonic aсtivity. The contributions of these participants led to lively discussions on the question whether the tectonic effect was sufficiently taken into account in the field studies by Berner, and if the involvement of plants was his overestimated in the GEоCARB model.

Philippe Amiotte Suchet, Université de Bourgogne, Dijon, France, reviewed an impressive body of French research on carbon fluxes from sons via river transport to the ocean. Their Global Erosion Models (GEMs) reliably predict ffluxes of carbon in watersheds as derived from carbonate, silicate and organic carbon weathering. The fluxes differ markedly according to rock composition, hydrology, runoff and the slope of the terrain. Extrapolation of the regional results to the global scale led to the conclusion that the effect of acid rain was minimal (although it could be substantial locally). They also found that the overall atmospheric CO₂ consumption by continental erosion was at least 10 to 15% lower during the Last Glacial Maximum than today, mainly because of reduced global runoff during that period. This research provides an excellent starting point for the quantitative analysis of the carbon fluxes on land over geological time scales. As yet, however, the results are difficult to accommodate with Berner’s approach, because the biological effects are not made explicit in the GEM models.

Peter Westbroek, Leiden University, the Netherlands, pointed out that, if Berner’s GEOCARB results are correct, the negative feedback on atmospheric CO₂ concentrations exerted by continental weathering of calcium and magnesium silicate would follow a distinct trend over the last 600 million years. If, as Berner implies, the origin and evolution of vascular plants were indeed largely responsible for this phenomenon, the trend would reflect an increasing dominance of the continental biota over the global carbon cycle. This increasing dominance is also apparent in associated changes in patterns of runoff and in the hydrological cycle, as land vegetation also deeply effects these processes. Furthermore, it is likely that this increasing biological involvement had a long preceding history, as soil formation and weathering is also influenced by the асtivity of microorganisms and lichens atone.

The extensive discussions throughout the meeting on land processes revealed that our present knowledge is still in its infancy and that further research may yield new and exciting surprises. In particular, the biological involvement in these phenomena remains poorly understood. It is too early to take Berner’s conclusions for granted, although his approach provides an excellent vantage point for the future. Preliminary plans were developed for a joint study of biologically enhanced weathering in a model field location, preferably on a volcanic island in the ocean.

General trend in silica deposition

As Westbroek pointed out, the deposition of silica (SiO₂) on the ocean loir also followed a distinct trend over geological time (figure 1 right). Some 600 million years agi this material simply precipitated from the seawater. We still fend thick crusts of it in the rocks of those times. It is easy to imagine that those spontaneous precipitates were most uncomfortable for living creatures in the ocean. They threatened to destroy the delicate tissues that were exposed to the water. Yet, in the course of geological time, ever more organisms appeared in the sea, which were capable to suck the dissolved silica from the water and used it in the production of their finely sculptured skeletons. Of particular importance were the sponges, the radiolarians and in particular the unicellular diatom algae, with their gigantic blooms in the Recent Ocean. Inc such silica shell, a hundredth of a millimeter in diameter, is shown in figure 2. This delicate structure does not precipitate spontaneously from the seawater, but is assembled with utmost precision inside the living cell. In the Recent ocean all silica is sucked out of the water and removed by organisms such as this one. The hazard is overcome. Spontaneous precipitation no longer occurs. The seawater itself is strongly undersaturated — it is a silica vacuum.

General trend in carbonate sedimentation

During the meeting the sedimentation of calcium carbonate (СаС0₃, figure 1) was subject to many detailed presentations and discussions. It became apparent that a similar, but not identical, trend must have occurred as in silica deposition in the ocean Like silica, much of this material precipitated spontaneously out of the sea 600 million years ago, without any strong intervention of organisms. In addition to calcium and magnesium carbonate crusts, stromatolites, irregular buildups of limestone, were produced under the influence of bacterial communities. Hete too, the spontaneous incrustations formed a hazard for life in the ocean. But the biotic response was slightly different than in the case of silica. In the course of evolution an almost internally contradictory development emerged.

Today, the ocean water is replete with slime, and this substance, excreted by innumerable marine organisms, efficiently inhibits the spontaneous precipitation of limestone. Furthermore, the Recent ocean water is replete with other inhibitors, such as humic acids and metal ions (of magnesium, in particular). Together, diese inhibitors have the effect to inhibit spontaneous incrustations on the soft tissues, a function referred to as ‘anti-calcification.’ Thus, the precursors of limestone are not sucked away, and the sea is not depleted with calcium and bicarbonate, as was the case for silica. Calcium and carbonate are not removed from the ocean water spontaneously, because the formation of limestone is arrested in open water. Inside their cens and tissues, however, some of the marine organisms make microscopic vesicles where the limestone is allowed to precipitate. Figure 3 shows one such a сеll, the coccolithophore alga Emiliania huxleyi. Thus, the production of limestone was brought under an inсreasingly strict biological regime over the last 600 million years, while spontaneous precipitation was eliminated from the ocean.

Evolution and the development of carbonate sedimentation

John Grotzinger (MIT, USA) refocused the group’s attention on large scale patterns in the history of the carbonate cycle. Detailing the sedimentological distribution of carbonates in precambrian oceans, he showed that the overall workings of the carbonate cycle and the broad pattern of sedimentary accumulation of carbonates on the ocean floor have not changed vert’ much in the past three billion years. That is, the evolution of organisms that form skeletons of calcium carbonate changed the loci of carbonate deposition, but not the overall abundance of carbonates. The major exception to this is the coccolithophorid algae, whose mesozoic radiation focused carbonate deposition on the deep ocean floor for the first time in Earth history. Carbonate sedimentation did change during the long Precambrian interval, however, as early seafloor precipitates gradually gave way to carbonate muds formed mostly in the water column. Grotinzger concluded that this change reflects Earth’s environmental history, espeсially atmospheric CO₂levels and die oxygen profiles of ocean basins.

Andrew Knoll (Harvard University, USA) continued this discussion, overlaying Grotzinger’s sedimentological pattern with a broad perspective of ecosystem evolution from the earliest appearance of lite in the geological record (some 3.8 billion years ago) up to the Recent. His reconstruction was based on a combination of fossil, stable isotope and geological evidence. The biological view complements that drawn from sedimentology, leading us to concentrate on global environmental change as much as biological evolution in our efforts to understand the development of the marine carbonate cycle. Knoll also pointed out that the marine silica cycle has changed through time in much the same way: die evolutionary take-over of silica deposition by skeleton-forming organisms changed the distribution of silica in sediments and undoubtedly left surface ocean silica concentrations at lower levels than in the Precambrian. However, it has had few discernable effects on the overall function of the Earth’s silica cycle.

William Hay (GEOMAR, Kiel, Germany) developed a sedimentological perspective on carbonate deposition during the part 500 million years, based principally on the impressive documentation of organic carbon and carbonate accumulation in Phanerozoic basins compiled by Ronov and his associates at the Vernadsky Institute of Geochemistry of the Academy of Sciences in the USSR. This work, painstakingly completed in the 1950s to 1970s, is little known in the West. But provides a valuable perspective on relatively recent Earth history. Hay applied these geological data to a carbon cycle model in an effort to understand how various fluxes and reservoirs in the marine part of the cycle have changed through time in response to tectonic, climatic, and biological forcing factors.

Several conclusions can be drawn from these geological observations. First, there is a clear vector through time in the environmental loci and mechanisms of carbonate (and silica) deposition. Seafloor precipitation of carbonate minerals, at least in part facilitated by microbial processes was a dominant feature of the marine carbonate for the first half of Earth history but less important thereafter, regaining its importance only transiently (but significantly) later in Earth history, in association with Neoproterozoic glacial events and Permian­Triassic mass extinction. Changes in Earth’s physical environment exert a first-order control on this pattern. Beginning near the end of the Proterozoic Eon, perhaps 550 million years ago, skeleton-forming animals and algae began to evolve, accelerating in the Early Paleozoic to the point where carbonate deposition became a predominantly biological process. Nonetheless, Paleozoic carbonate platforms have an architecture his unlike those of earlier eras, underlining the continuing importance of tectonics, climate, and oceanic composition in controlling the carbonate cycle. By refocusing carbonate deposition on the open ocean, coccolithophorid algae brought genuine biological change to the carbonate cycle in the Mesozoic, as diatoms did to the silica cycle on the same time frame. Deep sea sediments are prone to subduction; thus, coccolithophorid evolution has had particular consequences for the completion of the modern carbon cycle.

Calcification mechanisms

The general trend in oceanic carbonate deposition over geological time, from spontaneous precipitation in the open ocean water to suppression of that precipitation by inhibitors and controlled mineralization in biological tissues was further illustratеd by contributions on calcification mechanisms in three broadly different settings.

Jean Trichet, Université d’Orléans, France, summarized the work of his group on carbonate precipitation in brackish lakes at the surface of reef islands of atolls in French Polynesia. Whereas crystallization was inhibited in the oversaturated surface water, it did take place inside laminated microbial eсosystеms, but, remarkably, in an alternating, stromatolitic, pattern. Non-carbonated, red layers, produced by sulfur oxidizing bacteria, alternated with permineralized laminae. Both types of laminae are about 1 cm thick. Trichet hypothesized that sulfate ions released by the sulfur oxidizing bacteria inhibit precipitation, while insoluble bacterially derived organic matter rich in acidic polysaccharides and diacidic amino acids (aspartic and glutamic) would provide a substrate for epitaxia1 carbonate crystаllization in both mineralized and non mineralized layers.

During the discussion, the idea was raised that spontaneous carbonate deposition could also be inhibited in non-carbonated layers by significant amounts of dissolved acidic (macro)molecules (anti-calcification). Whу this anti-calcification process is only active in certain (non-carbonated) layers, alternating with carbonated orles, is still unknown. Bacterial scavenging of these inhibitors from the interstitial solution deeper in the mat would provide an opportunity for spontaneous crystallization in laminae where no sulfate was released (because well under the sulfur oxidizing zone). Eventually, these processes might explain the widespread occurrence of finely crystaшne carbonate (micrites) in many platform limestones.

Frédéric Marin (Leiden University, the Netherlands) discussed highly organized calcification as it occurs in many animal phyla, in particular marine corals and mollusks. Hе gave evidence suggesting that, while profuse anti-calcifying muci are excreted by the soft tissues exposed to the sea water, the same inhibitory macromolecules are used to fine-tune the actual calcification process. Thus, the molecular machinery needed for organized calcification mаy be derived, at least in part, from precursors with a different function in the non-calcified ancestral stocks. Marin went on discussing the finding by Lopez and co-workers that the bivаlviаn mother-of pearl can induce the synthesis of bone tissues by osteoblasts (bone forming cells in the vertebrates). These data suggests that the nacre contains one or more signal-molecules capable of activating the osteoblasts. These molecules are рrobablу part of ancient rеgulatory system, which antedates the metazoan radiation prior to the Cambrian. At the Precambrian/Cambrian transition, this signаlling system would have been modified for driving the cаlcifying process. This scenario might explain how the complex calcifying machinery could emerge in many animal stocks independently.

The sponges lie at the base of the animal tree, and throughout much of the Phanerozoic Bon they have been major contributors to reefs, so an understanding of sponge biology and evolution is particularly relevant to a geobiologial understanding of carbonates. Joachim Reitner (Gёttingen Universit~t, Germany) provided an integrated perspective on sponges, showing how sponge-bacterial consortia function, how calcification occurs in these organisms, and how sponges have participated in the carbonate cycle for the past 540 million years or longer. Reitner’s presentation underscored the need for better data on the molecular biology of carbonate and silica precipitation by sponges.

Rachel Wood (Cambridge, UK) generalized the discussion on reefs, reviewing how reefs have changed over than past 540 million years. Sponges are part of this change, but so are many other groups, including corals, bryozoans, mollusks, and red algae. Woods sees reefs as a “localized biological occupation of space” — that is a сommunity of organisms that accretes vertically as a result of massive skeleton formation by benthic organisms. These is, in Wood’s view, no ecological congruence among reefs of various ages. Rather, they reflect the evolution of organisms capable of precipitating massive skeletons. Strong environmental influences can be discerned in the geological record, with sea level and ocean chemistry (which controls the formation of cements) having major influences on the distribution of reefs in time and space.

Gilles Dromart (Lyon, France) completed the presentations on marine carbonates with a remarkable dissection of carbonate accumulation in the Jurassic of the Paris Basin in France. For this interval, excellent outcrop and detailed seismic data combine to produce a detailed three-dimensional picture of sedimentation through time. Biostratigraphy, calibrated by volcanic ashes, permits fine time slices to be cut through this

basin geometry. In consequence, Dromart was able to detail how rates of carbonate accumulation (both skeletal and non­skeletal) changed in response to environmental influences through a fifty million year interval of the Mesozoic Era. This work helps greatly to connect process-level observations made on the modern oceans with histgrica1 observations of large scale pattern in Earth history.

The top-down systems approach of geobiology

The question whether biological evolution follows a trend over geological time from simple towards ever more complex life forms is an old controversy in the life sciences. Recently, this discussion was brought back into the open by Gould (1996), who argued that all evolutionary change after the establishment of full-fledged bacterial metabolism was of minor importance. It is noteworthy that Gould only considers evolution as it is expressed in the organisms per se, and ignores the geological context in which these organisms operate. (For an alternative view, focussed on ecosystem function, see Bambach and Knoll, in press).

At this meeting, discussions of the global carbonate cycle clearly demonstrated the need to consider biological evolution and environmental change in concert. Throughout our planet’s development, distinct trends in evolution have become apparent as soon as the geological environment of life is included. Weathering, transport and the sedimentation of both silica and carbonates show dramatic trends over the last 600 million years, and the changes were largely due to the evolution of eukaryotic life. All these changes brought an increased involvement of life in the geological environment and an improved adaptation of the earth to biological requirements. The colonization of the continents by vegetation greatly enhanced the availability of mineral nutrients in the biosphere, intensified the water cycle, moderated runoff and sediment transport and provided extra biological controls on the carbon cycle and climate. During the same span of geological time, the biological domination of silica and carbonate sedimentation vastly increased with eukaryotic and in particular animal evolution. This latter development is likely to have improved the habitability of the oceans, as spontaneous mineral precipitation was arrested, and replaced by biologically regulated skeleton formation.

The last fifty years have brought major advances in biological practice. The spectacular success of molecular biology in particular marked the transition from an idealistic to a materialistic science of life. However, a comprehensive predictive theory of life is  available. Westbroek pointed out that such a theory could only emerge when life is consistently placed in its geological context. It should provide a consistent understanding of biological-geological organization at the (macro)molecular, the organismal, the ecosystemic and global levels of aggregation. A top-down systems approach is needed to the cyсling of matter in the outer earth and to the role of life in regulating the global environment. In recent years, geobiology is attracting a great deal of attention and funding. This interdisciplinary field provides the appropriate scientific milieu in which biological theory maуbe generated.

Bas Kooijman (Free University, Amsterdam) discussed his Dynamic Energy Budget (DEB) theory, which starts the geobiological top-down systems approach at the level of the individual organism. According to DEB, the energy and nutrient metabolism of each organism can be exhаustively and consistently described by a vert’ limited set of mathematical rules. Any organism has to obеу these rules for survival. The theory also provides a mechanism explaining scaling relationships between different species, i.e. the parameterizations of DEB models for two species are related to their maximum body size. The simplicity and predictive value of the DEB models are striking in view of the very complex network of metabolic pathways undеrlying the organismal organization. Kooijman also showed how DEB тау be used to explain suborganismal organization down to the molecular level, as well as the functioning of eсosystems, and at the longer term, the global system. As a simple example of ecosystemic organization, he analyzed calcifying/zooxantellae symbiosis.

A final, and most important, conclusion of the meeting was a call for integrated geobiological research on the complexities of the carbonate cycle. What is needed is a location where a well circumscribed catchment area on land feeds a lake or isolated marine water body. In this way, short- to intermediate-scale variations in weathering, erosion, and the flux of ions into the water body can be related to changing patterns of carbonate precipitation. Experiments can help us to elucidate the interactions between biological and physical processes at both ends of the system. Such a coordinated research effort could do much to eliminate current conceptual and observational uncertainties in or understanding of geobiolоgy.

Excursion

This fruitful meeting in the beautiful setting of ‘les Treilles’ was preceded by a geological excursion of one dау in the Marseilles region. Dr. J.P. Masse of the University of Marseilles gave a verу livelу expert introduction into the Mesozoic and Tertiary geology of the area, with special emphasis on the many and well-exposed carbonate platforms.