Introduction

Reef organisms take up and use nutrients from their environment in order to support their metabolism, to grow and to reproduce. Even though the concentrations of dissolved inorganic nitrogen and phosphorus (DIN and DIP) are very low in the water washing over coral reefs, they are still sufficient to maintain very high rates of primary productivity. This high rate of productivity necessitates a high availability of essential nutrients such as carbon, nitrogen and phosphorus. One of the sources of these materials for coral reefs, as examined last month, is the land located near most coral reefs. Not all reefs are located near land, however, so land cannot represent the only possible source of essential nutrients for reef ecosystems. Indeed, it does not. Coral reefs are connected not only to nearby land, but also to the sky above them. Reef organisms actively take up nutrients that originate in the overlying atmosphere and some amount of nutrients from reefs is lost to this pool as well.

It's Raining… Nitrogen?

Before the advent of the Haber-Bosch industrial nitrogen fixation process, the vast majority of the combined nitrogen available to any ecosystem was first made available due to the biological fixation of atmospheric nitrogen by N-fixers. Actinomycetes and rhizobium bacteria, along with lichens (symbiotic cyanobacterial and fungal associations), were, and still are, the primary N-fixers on land, while cyanobacteria are much more important in aquatic ecosystems. However, life evolved before the biological ability to fix atmospheric nitrogen. The combined nitrogen available to early life forms was fixed primarily by lightning. As lightning travels through air it produces nitric oxide (NO) and nitrogen dioxide (NO₂) (collectively known as NO_x-rhymes with box) from molecular nitrogen and oxygen. Much of the nitric oxide produced by lightning can be oxidized to nitrogen dioxide by ozone, or even molecular oxygen, to produce nitrogen dioxide (Hill et al, 1980). The NO₂ can then react with water molecules to form nitric acid. The nitrate ion resulting from the formation of nitric acid is then deposited dry as an aerosol or wet in rainwater. This atmospheric source of nitrogen, which was of major importance to the first life forms, is still formed today. While it is not nearly as substantial a source of nitrogen as biological fixation, it is ubiquitous, accounting for about 4% of the nitrogen available to the biosphere (Bezdicek and Kennedy, 1998).

A more substantial mode of atmospheric nitrogen deposition occurs due to combustion on land. Burning releases NO_x and other nitrogen-rich aerosols. Combustion of, primarily, plants and plant detritus on land has occurred for hundreds of millions of years. Little of the world's total vegetation burned in a typical year, until a few thousand years ago. The area burned every year, however, has substantially increased in the past several thousand years due to altered land-use practices by people. The area burned every year can even be the majority of some countries' land area (e.g., Madagascar). Combustion of vegetation accounts for approximately 8% of the combined nitrogen in the biosphere, though only part of this becomes available as aerosols in the atmosphere (Bezdicek and Kennedy, 1998).

In addition, the combustion of fossil fuels, such as in car engines, produces NO_x. Catalytic converters substantially reduce the amount of NO_x released from cars by catalyzing the conversion of NO_x to N₂ and O₂ gases. Industrial applications can also release large quantities of NO_x, especially if they have not installed or maintained pollution control devices that limit the release of these substances. NO_x are, after all, major air pollutants causing illness and even death for hundreds of thousands of people around the world every year, especially when concentrated, as in metropolitan or industrial areas. Atmospheric deposition of NO_x from industrial applications and motor vehicles accounts for, on average, more than 20% of the total amount of fixed nitrogen available to the biosphere (Bezdicek and Kennedy, 1998). This deposition pattern is highly spatially heterogeneous, however. That is, in areas far from anthropogenically produced sources of NO_x the contribution may be very small. For example, a tiny island in the middle of the Pacific, outside the areas of NO_x fallout from industrialized countries, might receive very little nitrogen from this source. On the other hand, areas close to industry and population centers, or "downwind" from them, so-to-speak, may receive substantial nitrogen enrichment from this source. We might therefore expect a coral reef off Sri Lanka to receive substantially more nitrogen originating through atmospheric deposition than Bikini atoll in the middle of the Pacific. At least a small amount does reach every corner of the globe, though.

This large spatial heterogeneity is significant in determining the impact of NO_x on ecosystem function. If the NO_x were evenly spread over the entire globe, it is unlikely it would cause major problems in many, if any, of the world's ecosystems. However, because this is not the case, the release of NO_x has caused substantial damage in some places due primarily to acid rain and secondarily by the effects of dramatically higher nitrogen availability. These problems have been most acute in forested ecosystems with low soil alkalinity and freshwater ecosystems with low alkalinity (soil and water alkalinity neutralizes acid rain and ameliorates its effects).

It's Sprinkling…Phosphorus and Iron

As I mentioned in the first article in this series, phosphorus lacks a significant gaseous stage in the biosphere. This is in stark contrast to the major pools of carbon and nitrogen in the atmosphere. Iron, too, lacks a significant gaseous state in the atmosphere. The air, however, does not stay still. Indeed, the sun's uneven heating causes convection currents to travel through the atmosphere-otherwise called wind. When blowing forcefully, wind has the power to move even very large objects. However, even when weak, wind has the power to pick up and carry dust and dirt, often over substantial distances. What is in the dust and dirt that the wind is constantly blowing around? You guessed it; among other things, it contains phosphorus and iron. Just how much, and how significant can this transport possibly be? Schlesinger (1997) estimates the amount of phosphorus carried as dust in the atmosphere to be on the order of 1.0 Tg P yr^-1, or about 1 billion metric tons of phosphorus per year. A billion metric tons is a lot of anything. To be fair, not all of this phosphorus will become biologically available and 1.0 Tg P, while a lot, pales in comparison to the amount of phosphorus actively cycled in ecosystems or available in most sediments.

Just as with NO_x deposition, the deposition of P- and Fe-rich dust is quite heterogeneous over the globe, with some places receiving substantially more dust than others. The two regions that supply most of the dust in circulation in the atmosphere are Northern Africa and the arid interior parts of Asia, though atmospheric dust can originate from any exposed land surface. This dust's deposition dramatically affects the productivity of the ecosystems where it settles. The subtropical and temperate Atlantic Ocean is relatively productive compared to much of the ocean, thanks, in part, to Saharan dust. As discussed in Part II of this series, the Southern Ocean has very low rates of productivity due to a lack of iron. This is due primarily to prevailing wind patterns, which blow from the northwest. The only land northwest of the Southern Pacific are tiny island dots in an expanse of blue ocean. The Southern Ocean is Fe-limited because it does not receive significant inputs of Fe-rich dust, and it cannot receive these inputs because the wind is simply blowing in the wrong direction-over thousands of miles of ocean. The dust coming off Asia reaches some, but certainly not all, of the islands in the northern and western Pacific. This leads to substantially different natural soil fertilities on different islands throughout the region. The effect can be so dramatic that these differences may have contributed to the perseverance or collapse of certain island societies in the Pacific (Diamond, 2005).

Some Quintessence of Dust

The amount of atmospheric dust in circulation has steadily increased since the last Ice Age due to the increased area of arid land. At the height of the last Ice Age much of the Sahara was covered in grassland and scrub, similar to what much of sub-Saharan Africa looks like today. As the climate warmed from ice age to pre-industrial conditions, the arid central portion of Africa grew, replacing grassland and scrub with desert. It is thought that land use practices by people living in the region at the time may have contributed to this transformation and caused the Sahara to expand more widely than it otherwise would have, though it is uncertain to what degree. Changes in land use by people over the past century have dramatically increased the amount of arid land area around the world (a process called desertification), and these land use practices are projected to increase the area of arid land even more substantially over this century.

As an example of how land use practices can affect the amount of atmospheric dust in circulation, let us consider how the major agricultural region of the United States became the Dust Bowl during the 1930s. The Great Plains, like many grasslands, are prone to occasional droughts. Starting in the 1920s the Great Plains experienced what ended up as a decade-long drought. The Southern Plains were much more affected than the Northern Plains, but the drought affected the entire region. Normally during years of drought, plants that can withstand the dry weather survive, while plants that are less tolerant perish. In general, however, the soil remains firmly locked in place by the living plants' root systems, and wind erosion is minimal. However, plowing this land leaves the soil completely exposed to the wind. In years of average or above average rain in the Great Plains crops such as wheat quickly rooted and grew on the exposed surfaces, reducing topsoil's wind erosion to a modest amount. Due to the drought the crops failed, and they failed for about a decade. This left huge areas of topsoil completely exposed, allowing extraordinarily high rates of wind erosion and, hence, the Dust Bowl. Practices that lead to similar erosion problems are still commonplace throughout most of the world. This problem is particularly concerning when the rate of erosion is factored against the rate of soil formation. A few bad years may cause the loss of topsoil that took literally thousands of years to form and that will take thousands of years to replace. The increasing availability of this dust may be good news for some marine phytoplankton starved of phosphorus or iron (though the effect is not expected to be that great), but it is pretty bad news for the six billion people who rely on agriculture for food. With luck, more sustainable land use practices that have already been devised will be more widely utilized in the near future.

This dust can also have health consequences. Saharan dust reaches all the way across the Atlantic. In fact, children living in parts of Florida and the Caribbean have higher incidences of asthma and other respiratory diseases than would be predicted due to anthropogenic air pollution. Many people in these same areas also have more problems with allergies than those living in other regions. A significant contributing factor to these problems, if not the major cause, is the high amount of Saharan dust in the air. This dust may prove problematic for wild organisms, too. Not only phosphorus and iron are deposited with this dust, but anything else that was in the soil as well. Aspergillosis, a disease affecting Caribbean sea fans and gorgonians, is caused by a soil fungus of the genus Aspergillus. One of the reservoirs for this fungus is Saharan dust. This disease can be fatal, though recovery is also possible. The incidence of this disease appears to have increased in recent years throughout much of the Caribbean and tropical Atlantic (Alker et al, 2001; Bruno et al, 2003; Geiser et al, 1998; Hayes and Goreau 1998; Jolles et al, 2002; Kim and Harvell, 2002; Kim et al, 2000a; Kim et al, 2000b; Nagelkerken et al, 1997a; Nagelkerken et al, 1997b; Petes et al, 2003; Rosenberg and Ben-Haim, 2002; Shinn et al, 2000; Smith et al, 1998; Smith et al, 1996).

In addition to the atmospheric deposition of terrestrial dust, pollen is also a significant transporter of nutrients through the air. A variety of plants (especially grasses and temperate trees) rely on wind pollination for reproduction. In order to be effective, however, these plants must produce a significant excess of pollen beyond what they actually need for reproduction. These "surplus" granules make their way into worldwide circulation and can be a significant source of phosphorus for certain oligotrophic ecosystems in particular, though probably not most coral reefs. Crashing ocean waves and a number of other processes can also create aerosols of phosphoric and other salts, which are transported by the atmosphere. These aerosols cause a loss of nutrients such as phosphorus from the ocean, which can be deposited either in a faraway part of the ocean or on land. Indeed, the sky is made of much more than just air. Truly, it is a thin soup consisting of gases, particles, aerosols and even living organisms, and its circulation transports all of these substances, sometimes over many thousands of miles.

Don't Forget Sulfur

A major connection between the ocean (including coral reefs) and the atmosphere involves the element sulfur. In order to form a droplet, water vapor must have a nucleus on which to condense. In order to form a cloud, there must be a lot of water droplets and, hence, a lot of condensation nuclei. Over land, dust and aerosols from land satisfy this need. Clouds form over the open ocean, too, and this occurs far away from land where terriginous dust could have a major influence. What is providing the nuclei for cloud formation far from land? The surprising answer is phytoplankton. Or, better said, the process of producing condensation nuclei begins with phytoplankton.

A few types of aquatic plants and many types of algae, especially coccolithophorids and dinoflagellates in the ocean, produce a chemical called dimethylsulfoniopropionate (yes, there are 26 letters in that word and no, you don't need to memorize it), or DMSP for short. This chemical has been implicated in several metabolic processes. Upon death DMSP is quickly converted to methanethiol and dimethyl sulfide (DMS) by bacteria. Methanethiol tends to be used up by bacteria quickly to produce sulfur-containing proteins (sulfur is present in the amino acids cysteine and methionine and, hence, in proteins) while DMS is used more slowly. Some DMS may be oxidized to dimethyl sulfoxide (DMSO) while another portion escapes to the atmosphere as an aerosol. This becomes oxidized to sulfate and provides nuclei for cloud formation. During mass bleaching events, when a large number of zooxanthellae (dinoflagellates of the genus Symbiodinium) from corals and other symbiotic organisms are dying, the substantial release of DMS may actually induce cloud formation over the reef. Even during non-bleaching events, however, there is turnover of zooxanthellae and other algae on the reef, which releases DMS and has the potential to affect local weather patterns (Hill et al, 2000; Hill et al, 2004).

Sulfur aerosols (generally referred to as SO_x-pronounced "socks"…oddly enough) are also released by industry and motor vehicles, and these sources account for the major portion of SO_x in the atmosphere at temperate, northern latitudes. These SO_x produce acid rain just as NO_x do. In the tropics, and especially in the southern hemisphere, which has less land area and less industry than the northern hemisphere, natural production of SO_x dominates. NO_x and SO_x (not to mention volatile organic compounds, or VO_x-no, I'm not making these names up) originate from volcanic as well as biological and industrial sources. The amount of these substances in atmospheric circulation due to volcanism varies from year-to-year, depending on volcanic activity. Human and natural sources overshadow volcanic ones during most years, though large volcanic eruptions such as of that of Mt. Pinatubo in 1991, while infrequent, can be very important over the short-term of several years.

Carbon Dioxide and Photosynthesis

A series of articles could easily be written examining just the role of this gas in influencing the ecology and biology of marine organisms. Despite this I will try to curb my enthusiasm and report only what I consider the essentials for appreciating carbon dioxide's influence on reefs.

I hate to always refer to paleobiology in these discussions, but I believe that it is instructive, so here we go. As the first life arose on the planet the concentration of CO₂ in the atmosphere was much higher than it is now. In fact, at ca. 39.8 matm (milliatmospheres, 1/1000^th of an atmosphere) during the late Archaean and early Proterozoic eons (2.75 - 2.2 billion years ago) it was about 100 times greater than today's concentration (about 378 µatm) (Rye et al, 1995). That is a lot of CO₂! Soon after this period photosynthetic life began to develop and draw down this concentration. The earliest photosynthetic organisms were cyanobacteria. They may be ugly as mats when found growing in an aquarium or in nature, but they sure are neat from an esoteric point of view.

The process of photosynthesis uses an enzyme to fix carbon dioxide, along with water, into organic carbon compounds. The enzyme is named ribulose-1,5-bisphosphate carboxylase/oxygenase (another horrible name you needn't remember) which is usually shortened to RuBisCO (rubisco) or even simply RuBP. The general form of this reaction is:

CO₂ + H₂O + light à CH₂O + O₂

This leaves the photosynthetic organism with organic carbon that it can use for energy metabolism, for tissue growth and repair, and for reproduction. However, as suggested by its longer name, rubisco is not only a carboxylase but also an oxygenase, meaning it can cause the reaction to proceed in the reverse direction and burn up organic carbon. Ironically, rubisco actually has a higher affinity for oxygen than for carbon dioxide! This means that to work properly there must be more CO₂ than O₂. For the first cyanobacteria this wasn't a major problem because CO₂ was abundant and O₂ was essentially absent from the atmosphere. Today, however, oxygen constitutes 20.9% of the atmosphere while carbon dioxide makes up just 0.0378%, 553 times less than oxygen. The situation is a little bit better for aquatic photosynthesizers. Oxygen is much less soluble than carbon dioxide in water, and even less so in sea water, while carbon dioxide is more soluble. In sea water at equilibrium with the atmosphere at a salinity of 35 and a temperature of 25 C there will be about 206 µmol kg^-1 O₂ and about 10.78 µmol kg^-1 CO₂. A factor of about 19 still separates the two, but this is much less of a hurdle to overcome compared to the one that land plants must negotiate. In order to allow the above reaction to proceed correctly, modern CO₂ users employ one or several mechanisms to concentrate CO₂ around rubisco and, in many cases, mechanisms to quickly eliminate oxygen. Many aquatic autotrophs also utilize bicarbonate as a source of carbon dioxide. These organisms have the advantage of bicarbonate being far more abundant than either oxygen or dissolved carbon dioxide in sea water. At S = 35, t = 25 C and total alkalinity, TA = 2300 µmol kg^-1 (considered average for the ocean), sea water contains about 1761 µmol kg^-1 bicarbonate-about 8.5 times the amount of oxygen and about 163 times the amount of carbon dioxide.

Some marine algae and seagrasses utilize dissolved CO₂ primarily, though not necessarily exclusively. Many marine algae use both dissolved CO₂ directly and bicarbonate indirectly as sources of CO₂. For a more thorough discussion of the use of carbon dioxide and bicarbonate by marine autotrophs as a source of carbon I direct readers to Randy Holmes-Farley's recent and excellent review of the subject here.

Rising CO₂ and Photosynthesis

As I discussed in the first part of this series, the concentration of carbon dioxide in the atmosphere rose over the last century and is expected to continue rising at an accelerating rate over this century due primarily to the burning of fossil fuels. Prior to the industrial revolution the concentration of CO₂ in the atmosphere was 280 µatm. Its concentration now is about 378 µatm, an increase of more than 35%. The atmospheric concentration is expected to reach 560 µatm, double the preindustrial concentration, as early as 2065. Many CO₂ users such as land plants and seagrasses, because of the relatively low abundance of CO₂, are thought to be slightly carbon-limited. Increasing the partial pressure of CO₂ (pCO₂) should therefore increase these plants' rate of production. Indeed, increased rates of productivity have been measured in a variety of Free-Air CO₂ Enrichment (FACE) experiments, as well as in mesocosm and laboratory studies. However, this increased productivity is not necessarily manifested in a way that offers more food to organisms that are higher up the food chain. For instance, the increased rate of productivity in many land plants often manifests as a disproportionate increase in belowground production. In other words, the roots grow faster but the parts usually eaten, and that provide most of the nutrients to the ecosystem, may not grow much faster (Canadell et al, 1995). Increased rates of productivity based on carbon may also prove not to be useful or even to be detrimental due to the production of lower quality food. Most plant foliage tends to be very rich in C and poorer in N and P compared to the tissues of autotrophs. Because autotrophs' tissue composition can vary somewhat, depending on the availability of nutrients, increased production based on carbon availability is likely to skew the C:N:P ratio even higher in favor of carbon. Herbivorous and omnivorous animals that already have a difficult time extracting sufficient amounts of N, P and other nutrients besides carbon from their diets may have a difficult time coping with food of even lower quality. The nutrient stoichiometry of food has already been shown to be a powerful structuring agent in some communities (Jannicke Moe et al, 2005).

Because most reef algae, including zooxanthellae, can utilize bicarbonate as a source of CO₂, it is thought that they are not generally carbon-limited. Thus, increased partial pressure of CO₂ (pCO₂₎ should not stimulate higher rates of primary production on coral reefs. Most studies on corals (Burris et al, 1983; Goiran et al, 1996) and on reef assemblages (Leclercq et al, 2002; Reynaud et al, 2003) have found that net production does not increase, while Langdon and Atkinson (2005) found a greater than 20% increase in net production of carbon in a coral assemblage at pCO₂ of about 790 µatm. The previous studies used net oxygen production as a proxy for net primary production, which is standard protocol, whereas Langdon and Atkinson (2005) measured net production of carbon directly. They found that net oxygen production did not change, in agreement with the previous studies, though the net production of carbon increased. This may be due to an increase in the production of carbon-rich compounds by zooxanthellae, thereby increasing the C:N and C:P ratio of photosynthate translocated. As discussed with land plants above, if the net production of carbon truly does increase in corals under increased pCO₂ it may come at no nutritional benefit to the coral. This does support the hypothesis that corals are generally carbon-limited in natural sea water and may help explain a variety of observations involving photosynthesis and calcification in corals.

Rising CO₂ and Calcification

Elevated carbon dioxide has been shown experimentally to reduce the rate of calcification in coccolithophorids (a class of phytoplankton important to oceanic productivity), foramaniferans, coralline red algae, scleractinian corals and reef assemblages (reviewed by Kleypas et al, 2006). Of particular interest to reef aquarists, the calcification rate of reef communities has been found to decrease by up to 65% (Langdon et al, 2000) from the rate at preindustrial pCO₂ to the projected pCO₂ for 2100 of 700 µatm, though the consensus estimate is near a 17-37% decrease (Gattuso et al, 1999; Kleypas et al, 1999). This is a level of carbon dioxide easily attained in reef aquaria at night, even with significant aeration, or especially when employing calcium reactors. The pH of the surface ocean (assuming S = 35, t = 25 C, pCO₂ = 378 µatm and TA = 2300 µmol kg^-1-a carbonate hardness of about 6.6 dKH) is currently 8.20. If these parameters are held constant but pCO₂ is increased to 700 µatm, the pH will fall to 7.98. Many aquariums dip below pH = 8.0 at night, and many, if not most, employing just a calcium reactor to maintain calcium and carbonate experience pH = 8.0 or lower for significant periods of time. This may be a very bad thing if our goal is to induce rapid calcification in reef organisms, especially corals. I should mention that aquarists (and most of the world) use a different pH scale than oceanographers. Aquarists use what is called the NIST scale, whereas oceanographers use either the total scale or the seawater scale (these two are essentially the same). This is significant because these scales arrive at different pH values in sea water. The values I have reported are calculated with the NIST scale used by aquarists, so no transformation is needed to interpret these numbers. The total and seawater scales tend to give values around 0.1-0.2 units lower than the NIST scale (hence pH = 8.06 and 7.84 for current and future pH, respectively, on the total scale).

The pH of sea water has been demonstrated to exert a major influence on the calcification of many reef organisms, including corals. In general, higher pH increases calcification while lower pH decreases calcification, though a pH either too high or too low will likely cause physiological stress to corals and other reef organisms, not to mention making it very difficult to stop spontaneous, abiotic precipitation of calcium carbonate at high pH. For instance, it is doubtful that a coral or other reef organisms would tolerate very high (say, above 11.0) or very low (say, below 6.0) pH for any significant length of time, even if such conditions could be provided. Therefore, don't try replacing a few gallons of tank water with kalkwasser. This probably will not lead to faster calcification rates in your aquarium, but might be very effective at killing things. Also, the pH on most coral reefs (especially in shallow areas such as reef flats) is usually not constant over a 24-hour period. In fact, the pH on a reef flat may vary from less than 8.0 to more than 8.6 within 24 hours with no significant deleterious effects on the animals. Sometimes it is stressed that all water parameters in a reef aquarium must be kept very stable to have success. If this were true about pH (and many other parameters), then nature would be failing miserably at growing reef organisms. Reef animals can easily tolerate a daily pH fluctuation. The reason for the fluctuation in pH on reefs, just as in reef aquariums, is that during the day the rapid consumption of CO₂ by photosynthesis reduces its concentration faster than it can diffuse into the water from the atmosphere, while at night community respiration with no consumption due to photosynthesis raises the amount of CO₂ in the water faster than it can diffuse out to the atmosphere. Calcification also continues at night in corals, though at about one-half to one-third its daytime rate. This is significant because calcification produces about 0.8 mol CO₂ for every mol CaCO₃ deposited.

One difference between the chemistry of aquarium water and sea water that must be considered is aquarium water's generally higher total alkalinity (though recently there has been a growing trend among some hobbyists to adopt a total alkalinity nearer that of natural sea water (NSW) in the aquarium). Increasing the alkalinity of sea water, for instance, through the addition of sodium bicarbonate, has been shown to increase the rate of calcification in corals (Marubini and Thake, 1999). Again, this suggests that corals may be carbon-limited in NSW. An alkalinity higher than that found in NSW has never been shown experimentally to be deleterious. In addition, overwhelming anecdotal evidence suggests that an alkalinity higher than that of NSW is not necessarily deleterious to corals or other reef organisms in the aquarium. Elevated ammonium and nitrate have been implicated in reducing calcification in corals in many studies. Marubini and Thake (1999) demonstrated that the addition of bicarbonate allows corals to overcome the deleterious consequences of elevated ammonium and nitrate on calcification. Can maintaining a higher alkalinity in the aquarium allow us to offset the effects of lowered pH? Depending on CO₂'s mechanism in poisoning calcification, the answer is maybe yes and maybe no.

The Saturation State Hypothesis

Currently, most of the literature (reviewed by Kleypas et al, 2006) suggests that the cause of reduced calcification in marine organisms at elevated pCO₂ is a reduction of calcium carbonate's saturation state. Saturation state is described by the equation:

W = [Ca²⁺][CO₃^2-]/K_sp

where [Ca²⁺] is the concentration of calcium, [CO₃^2-] is the concentration of carbonate and K_sp is the solubility product of aragonite or calcite, depending on the form of calcium carbonate produced by the calcifying organism (e.g., corals produce aragonite so the K_sp of aragonite is used for them; coccolithophorids produce calcite so the K_sp of calcite is used for them). In sea water the concentration of calcium is highly conserved, so it depends mostly on salinity. That is, if the salinity is higher, the calcium concentration is higher because the entire seawater solution becomes more concentrated, and vice versa if the salinity is lower. The solubility product, K_sp, varies depending on several factors (salinity, pressure, temperature, etc.). Of these, temperature affects K_sp the most (in a meaningful way) in the context of a reef aquarium. Calcium carbonate, unlike most substances, is actually less soluble at higher temperatures. Thus, as temperature increases, K_sp decreases and W increases. Changes in Ksp over a degree or two are relatively minor, though. The carbonate concentration is determined largely by alkalinity and pH. When pCO₂ increases, it shifts the equilibrium percentages of carbonate toward bicarbonate and carbonic acid/CO₂ as described by this equation:

CO_2(aq) + H₂O ↔ H₂CO₃ ↔ H+ + HCO₃^- ↔ 2H⁺ + CO₃^2-

Thus, increasing pCO₂ decreases the concentration of carbonate and the saturation state of calcium carbonate if alkalinity is not adjusted. If pCO₂ is increased and alkalinity is also increased to the proper level, the two offset each other in terms of their effects on the carbonate concentration.

Current models for the calcification of calcareous algae such as Halimeda suggest that the saturation state hypothesis may adequately explain lower rates of calcification at elevated pCO₂. In these calcifiers photosynthesis removes carbon dioxide, raising the pH and, thus, the carbonate concentration and saturation state in a confined area, which leads to the precipitation of calcium carbonate. The changes in carbonate concentration have also been invoked to explain changes in the calcification rate in corals and other marine invertebrates as well. Physiological data suggest, however, that corals take-up bicarbonate, not carbonate, from sea water. Also, more than 70% of the carbon that corals use for calcification may originate from metabolically produced CO₂, with the remainder being provided by seawater bicarbonate (Furla et al, 2000). If the change in carbonate concentration leads directly to reduced calcification in corals and other marine invertebrates, then current models of calcification must be dramatically modified and the mechanism of carbonate transport must be identified. Paradoxically, Reynaud et al (2003) found that at a temperature of about 28° C (82.4° F) the rate of calcification in Stylophora pistillata decreased by 50% at a pCO₂ = 798 µatm (control at 470 µatm), while calcification actually increased by 5% in corals maintained at about 25° C (77° F) under similar carbon dioxide concentrations. This suggests to me a lot of regulation by the coral host, or perhaps mechanisms at play that are not yet known.

On the other hand, many cellular processes are highly dependent on pH, with many enzymes and processes being highly sensitive to pH. It is very likely that corals use a Ca-ATPase enzyme to pump calcium ions into the calcifying fluid in exchange for protons (H⁺) (McConnaughey and Whelan, 1997). If the external sea water's pH falls and the (H⁺) concentration increases, does the calcium pump become less efficient? Does some other rate-limiting step in calcification (perhaps the production of the organic matrix) depend upon a specific pH range? I wish I knew, but further investigation is required to determine the mechanisms at work. Suffice it to say that this is far from the final word on calcification in marine organisms.

Conclusion

A constant and vital exchange of materials occurs between the atmosphere and the ocean. Nitrogen, phosphorus and iron that are transported and deposited by the atmosphere into the water overlying coral reefs is an important source of these nutrients to reefs and helps them to sustain high rates of primary productivity and thereby proper function. Carbon dioxide from the atmosphere also dissolves into sea water and provides carbon for photosynthesis. Many reef autotrophs use not only dissolved CO₂, but also derive CO₂ from bicarbonate. While many reef algae may not be carbon limited, corals which support both photosynthesis and calcification (both processes require inorganic carbon) may be carbon-limited at NSW levels. Corals calcify faster when the availability of inorganic carbon in the external sea water increases due an increase in total alkalinity. This is likely true for many other marine calcifiers as well. When the amount of organic carbon is increased due to increased pCO₂ (and the associated drop in pH), however, just the opposite is observed. For marine calcifiers (considering only calcification and not photosynthesis) it is neither the pCO₂ nor the total alkalinity that is directly important to them. Rather, it is the availability of the species of carbon they use for calcification and the pH that actually affect their calcification mechanisms. Raising the alkalinity in an aquarium with depressed pH may be sufficient to offset a decrease in calcification due to low pH in all marine calcifiers, or perhaps only in some. In corals, the marine calcifiers of greatest interest to most aquarists, it is not clear whether raising alkalinity is sufficient to ameliorate the negative effects of reduced pH. For that reason, it may be prudent to keep the aquarium water's pH near or above that of natural sea water. I would suggest that another take-home message should be that we cannot separate the ocean or the aquarium water from the air overlying it. Keep this in mind when stirring up dust or introducing aerosols and noxious gases and fumes in the vicinity of an aquarium, or when noxious substances are used outside a home with open windows. Anything in the air invariably ends up in the ocean or in the aquarium, for better or worse.

References:

Alker, AP, GW Smith and K Kim. 2001. Characterization of Aspergillus sydowii (Thom Et Church), a Fungal Pathogen of Caribbean Sea Fan Corals. Hydrobiol 460 (1-3): 105-111.

Bruno, JF, LE Petes, CD Harvell and A Hettinger. 2003. Nutrient Enrichment Can Increase the Severity of Coral Diseases. Ecology Letters 6: 1056-1061.

Bezdicek, DF and AC Kennedy, in Microorganisms in Action (eds. JM Lynch & JE Hobbie). Blackwell Scientific Publications, 1998.

Burris, JE, JW Porter and WA Laing.1983. Effects of carbon dioxide concentration on coral photosynthesis. Mar Biol 75: 113-116.

Canadell, JG, LF Pitelka and SI Ingram. 1995. The effects of elevated CO₂ on plant-soil carbon belowground: A summary and synthesis. Plant and Soil 187(2): 391-400.

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