In this final part of my series on the food of coral reefs and of corals, I literally tackle an enormous subject. In spite of that, it will become apparent that it describes a relatively unimportant source of nutrition to corals (for a number of reasons). The production, decompositions, flux and uptake of dissolved nutrients involves not just corals, but the whole coral reef, and involves everything from sediments to the water column, and from bacteria to fishes. Therefore, the introduction to this article is at best limited to a most brief overview of the subject.

Introduction

Dissolved nutrients are composed of both organic and inorganic forms. By "nutrients" I mean that any molecules that can be taken up and used as "food" - catabolized or used as building locks for metabolic processes. Dissolved organic material, commonly known as DOM, must by definition, contain carbon, and often contains hydrogen, oxygen and nitrogen, as well. Dissolved inorganic material is composed of those substances lacking the carbon component, and may be simple free ions, such as nitrate (NO3-), as well as other types of material.

One of the difficulties in ascertaining the amount of dissolved organic materials in seawater, or their uptake by various organisms, is that the dissolved organics tend to form films at water/air interfaces and also form colloidal aggregates (particles between 1nm and 1µm in diameter) in the water column, often by association with iron or other metal compounds and "turning into" particulate material. The colloids, finely divided particles (a few millionths of a millimeter) dispersed within a continuous medium in a manner that prevents them from being filtered easily or settled rapidly, can also attract various inorganic molecules, including trace metals, leading to a somewhat complex situation. In one sense, it may allow larger colloids to be included in the fraction of particulate organic matter (while, conversely, some particulate matter may be colloids of dissolved materials). This also makes it difficult to assess the true nature of uptake, and whether or not the uptake is a generalized process or if specific components are targeted, utilized, required, or even toxic and incidental components of otherwise desirable materials. Generally speaking, "dissolved" organic material is defined as fractions that pass through a 0.45µm filter. Furthermore, dissolved material may be adsorbed from water onto carbonates, clays, and particulate material that is not only present in seawater, but also may be a significant reservoir of both organic and inorganic constituents. True organic material in solution and not in the colloidal state is generally less than 0.1µm in size. As an example of the plethora of materials in the difficult to assess size class, many bacteria are between 0.25 and 1µm in size, and the common phytoplankton, Nannochloropsis oculata is 2-3µm in size. Thus, bacteria, and a partially consumed or degraded phytoplankton particles, clearly not dissolved organic material, may be included in this category simply by virtue of size and methods that screen DOM by filtration. To further complicate the matter, bacteria generally mediate the events. For example, dissolved organic carbon initiates bacterially mediated aggregation of detrital (particulate) material. The bacteria, using the material as a food source may form films, or they may cement the material together (Figure 1).

Microbial use of dissolved organic material adsorbed onto carbonate sand is responsible for the not infrequent "cementing" of sand beds in aquaria. Other organic aggregates may occur with the absorption of materials onto the surface of air bubbles (the general principle behind protein skimming, whereby dissolved proteins are removed by adherence to foam produced by the skimmer). As a side note, it is often said that the foam produced by wave action acts like "natural skimming." This is frequently countered by those saying this analogy has never been proven. Well, it has been proven - often (see references at the end of this article). A final important mode or organic aggregation, and perhaps most applicable to coral reefs, occurs through the production of mucus by many organisms. Mucus consists of mainly sugars and glycoproteins - soluble materials in and of themselves. However, the formation of mucus and its release in a matrix of chains of these materials, may result in a particulate material. This material is both utilized directly by many organisms, and also forms the basis for a predominant fraction of the particulate "marine snow" on reefs. In the latter situation, it is utilized and loosely adhered together by microbes and subsequently ensnares other particulate material, forming even larger accumulations that are clearly no longer "dissolved' by any means (Figure 2).

The Levels and Production of Dissolved Nutrients

Nutrients are brought to the reef via numerous pathways. First, they are brought with oceanic water; either by thermohaline upwellings or currents and waves driven by wind and tides. Groundwater may be another important nutrient source. Land based nutrients are also produced and washed seaward to reefs from rains, and river and coastal discharges. More recently, enhanced nutrient levels from anthropogenic land-based (sewage discharge, coastal development, land clearing and agriculture), and marine-based sources (ships, etc.) have produced a somewhat disturbing pattern of eutrophication.

Nutrients are also formed allocthonously (produced by the reef) by the excess secretions and excretions of the organisms (feces, mucus, etc.). Dissolved nutrients "leak" from algae, plankton, and other organisms, as well. All dead and decomposing matter eventually makes its way back into the nutrient broth of seawater as a product of microbial degradation, and nitrogen is also "fixed" by certain classes of bacteria and blue-green algae (cyanobacteria). These processes occur throughout the reef, from aerobic surfaces to deep anoxic sediments. It is primarily the sediments that form the "action areas" of decomposition and remineralization or organic materials. Moreover, adjacent communities, such as mangroves, estuaries, and seagrass areas provide large areas of enriched production and nutrient export to coral reefs.

Still, the abundance of life on coral reefs, living in clear tropical waters relatively devoid of dissolved nutrients, could not be sustained by this resource alone (Table 1).

As such, there is a tight recycling of nutrients within the reef community that includes the well-known symbioses between photosynthetic organisms (like zooxanthellae) and animal hosts (clams, sponges, corals, etc.) The dynamics of inorganic nutrient cycling on coral reefs have been studied extensively, and yet are still unknown in many aspects. They are, however, beyond the scope of this article, and I confine any further discussion to the set of tables and figures below.

Dissolved organic material on reefs is much less studied (despite the plethora of references at the end of this article) and is probably underestimated. The low levels in oceanic waters are boosted primarily by phytoplankton excretion and then again from the products of benthic algae and corals. In fact, reef waters are 30-40% higher in DOM than oceanic waters, and this makes sense since 5-40% of the photosynthetic production of phytoplankton, algae, and corals is lost primarily as glycine, amino acids, sugars, vitamins, fatty acids, and phenols.

The Uptake of Dissolved Materials

Given the introduction above, it may not be surprising that deciphering reports and studies on the uptake of dissolved materials by reef organisms includes assessing whether the reported "use" also includes other forms, such as bacteria and particulate materials. Both of these are well known to be removed and use as sources of heterotrophic nutrition that should be considered separate from the use of dissolved materials. In fact, many early studies simply lumped bacteria into the DOM fraction and ignored particulates within the "dissolved" size fraction, and instead dealt with particulates above a certain size class.

In general, the use of dissolved material requires a means of uptake. For the larger size classes, including some of the colloids, phagocytosis is probably utilized. In this method, material is encircled by the cell membrane of an organism's cells and is "pinched off," and is then located in a membrane-surrounded compartment called a vacuole. The vacuole will fuse with other compartments containing enzymes, and the material is digested into components able to be used by the cell. Smaller dissolved material probably enters the cell by pinocytosis that doesn't usually involve the formation of a vacuole, though the basic uptake processes are similar.

In terms of determining the degree to which organisms may use dissolved material as significant source of nutrition, one may examine the surface area of the outer cell membranes exposed to such materials. In general, the larger the absorptive area, the more likely organisms are to depend on absorption. Some cell surfaces are covered with many finger-like processes called microvilli that greatly increase the surface area of the membrane. Furthermore, the presence of cilia is often a good indicator of absorptive surfaces. Perhaps not surprisingly, corals have extensive microvilli and cilia.

Dissolved "Nutrients"

What are nutrients? They are substances that are required or produced for use in the normal metabolic functioning of an organism or cell. Depending on the organism, they may include unusual substances, such as vanadium or yttrium. However, basic organic constituents are typically far less exotic. Thus, the term dissolved "nutrients" typically refers to common metabolic building blocks such as carbon, nitrogen, and phosphorus. Despite the heavy uptake of elements such as calcium by calcifying organisms, calcium is not normally considered a major "nutrient." However, trace amounts of calcium are used in cell function and metabolism of most organisms. It may be notable, though, that dissolved organic material, and inorganic ions such as magnesium, may interfere significantly with the precipitation of calcium carbonate (Chave and Suess 1970; Meyers and Quinn 1971).

Because this is a column that focuses on corals, I will constrain the remainder of this article to the use of dissolved major nutrients by corals. It is not my intent to discuss every case where a species might have unusual requirements (for example, iodine in some gorgonians), nor will I address the many theoretical considerations that will likely plague some minds after reading the remainder of this column. Rather, I confine the topic to information that is available and reasonably well document with an emphasis on practical considerations that are part of maintaining corals in aquaria.

Uptake of Dissolved Material by Corals

Phosphorus

Early studies of phosphorus flux across coral reefs showed little net uptake or loss by coral and algae, but mostly a change in the form of phosphorus (Pilson and Betzer 1973). However, Atkinson (1987) later found that the reef flat community, mainly algae and corals, were taking up phosphorus as fast as they were known to be able to do, and the main limitation to the rate of uptake was the low availability of phosphorus in the environment (Table 2).

Corals are known to take up phosphorus in solution. However, this process is thought to be mainly a function of zooxanthellae uptake rather than the coral polyp, since only zooxanthellate corals uptake phosphorus, and this activity only takes place during the day (Yonge and Nichols 1931; d'Elia 1977). It was proposed that phosphatases found in tridacnid clams were involved in digesting zooxanthellae by the animal (Fitt and Trench 1983), but more recent work suggests that it is likely that their presence is a zooxanthellae response to phosphate limitation by the host polyp with phosphorus uptake (as well as other nutrients) controlled by the algal membrane (Jackson et al. 1989, Rand et al. 1993). Still, phosphorus is present in very low amounts in the reef environment (Figure 3), and recycling of phosphorus between host and algae, even if ultimately controlled by the alga, is likely a necessary requirement for the survival of both partners of the symbiosis in order to acquire adequate phosphorus from the environment (D'Elia 1977).

Corals have been previously found to "prefer" particulate sources of phosphorus over dissolved forms (Sorokin 1973). Much of the dissolved fraction of phosphorus on reefs may be adsorbed onto calcareous substrates such as sand and the reef material, and can be liberated by dissolution.

Nitrogen

Despite the view above that phosphorus may indeed be a limiting nutrient source on coral reefs, far more study and far more attention has been paid to the role of nitrogen on coral reefs and the role of dissolved forms of nitrogen to reef coral (Figure 4).

Figure 4. Dissolved inorganic nitrogen levels from various reefs in micromoles/liter (from D'Elia and Wiebe 1990). Click for larger image.

It has also been widely stated and often accepted the nitrogen may be the primary limiting nutrient to reef organisms, although the view that phosphorus truly limits corals has been well-made (Miller and Yellowlees 1989). It is also interesting that despite the lack of dissolved nitrogen on coral reefs, reefs are generally sources of net export of nitrogenous compounds to oceanic waters!

As with phosphorus, nitrogen appears to be highly recycled within the reef community; such recycling occurs both between the organisms in the community and within each of the corals through recycling between host polyp and algal symbiont (Rahav et al. 1989). On reefs, the most abundant form of dissolved nitrogen is ammonium, and not nitrate as is the case in aquaria. Also similar to the case with phosphorus, azooxanthellate corals appear to have a net export of nitrogen whereas zooxanthellate coral appears to have a net uptake of dissolved nitrogen. Nitrogen fixation and denitrification also occurs, and this is thought to be result of bacterially and cyanobacterially mediated events that take place not only on the surface of corals (Wafar et al. 1990), but throughout the microbially productive surfaces and sediments on and surrounding coral reefs (Webb et al. 1975). Because sediments are enriched with organic material, there is generally a net efflux of dissolved nitrogen from sediments and other pore waters (coral skeletons, live rock) into the water column. This may also lead to locally higher levels in areas with lower water circulation. Nitrogen fixation is thought to be the most important source of dissolved nitrogen to coral reefs, while denitrification is thought to be the major source of nitrogen loss. A tremendous description of the complete nitrogen cycle on coral reefs is found in D'Elia and Wiebe (1990). Most aquarists are only familiar with the limited process of nitrification and denitrification, but this chapter describes all aspects of the nitrogen cycle in detail (Table 4).

Corals are able to take up various forms of both organic and inorganic dissolved nitrogen. As with phosphorus, the zooxanthellae appear to be nutrient limited by their host, and here it extends to nitrogen. Particulate material or zooplankton captured by the coral are available first to the coral whereas the animal has little control over the availability of dissolved intracellular nitrogen. Again, as with phosphorus, the algae are able to control the amount of nitrogen that they take up, provided it is made available (as in enriched conditions). However, unlike phosphorus, availability of dissolved nitrogen to zooxanthellae has a number of important effects: First, nitrogen made available to the zooxanthellae is taken up and used to produce proteins and increase the rate of mitosis. Even slightly elevated nitrogen levels can quickly result in rapid increases in the density of zooxanthellae as they use it to fuel their own reproduction. Second, there is a subsequent drop in the amount of carbon and nitrogen translocated by the algae to the host. With increased densities, the zooxanthellae begin to translocate less carbon to their host, as apparently they need it themselves (Muscatine et al 1989). It is also somewhat equivocal that corals are able to utilize nitrate (which exists nearly totally in its ionic state at physiological pH) at all, and an inability to find nitrate reductase in many studies makes the ultimate importance of this dissolved nitrogen source to corals (and anemones) rather tenuous. However, it is unambiguously true that ammonium is a sought-after nitrogen source by both coral host and algal partner.

Carbon

Carbon is rarely discussed in terms of its limitation on coral reefs. Inorganic carbon is usually abundant in seawater either as carbon dioxide or as a form of carbonate. Additionally, dissolved inorganic carbon can be found, as well as making up components of the many other sources of dissolved organic material. Furthermore, and at least for corals living in shallow water environments, the productivity of the zooxanthellae in providing reduced carbon compounds often exceeds the needs of both symbiotic partners. Primary production via photosynthesis, at least in relatively shallow areas, also tends to have a photosynthesis to respiration (P:R) rate of greater than 1, meaning that more carbon is being produced than is being respired. Thus, carbon is the least of the worries for reef organisms, corals, and us (as aquarists). The situation may be somewhat different in deeper water, but algal remains, particulates, and other organic material usually prevents any shortage of carbon even outside the photic zone.

Silicon

The role of silicon is much less studied than other nutrients, however it is considered to play an important role in the requirements of many coral reefs organisms such as sponges and diatoms. Their role on corals reefs, especially since reefs are mostly calcareous based and not siliceous, is less than other marine environments. The principle source of silica is likely from terrestrial runoff, and its principle form, silicic acid, is found in a dissolved form in seawater.

Humic (refractory) compounds

I will only briefly mention humic compounds because of their interest to aquarists. These yellowing compounds are typically found at relatively high levels in aquaria, and they are removed with protein skimming and activated carbon. Humic materials have been thought to be relatively inert and unavailable for use as a nutrient source. However, studies have shown that organisms from bacteria to brine shrimp (Artemia salina) can utilize humic substances as a source of nutrients. It does, however, appear that they are less preferentially utilized than other dissolved organic and inorganic sources. Bingman has treated humic substances extensively in the aquarium literature (Bingman, 1996).

Summary

Dissolved organic and inorganic nutrients, and their role to coral reefs (and corals) is still dramatically unknown. The complications arising from methodological problems and poor studies have only compounded the confusion. In terms of corals reefs, the amounts of most dissolved nutrients, except carbon in most cases, are very low. Depending on the location, the reef area, and the organism, various nutrients can limit the growth of the entity. An example well known to many is the nutrient limitation of algae. The recycling nature of the coral-zooxanthellae symbiosis has given a competitive edge to corals in low nutrient environments, despite the abundance of highly grazed turfs, unicellular microalgae, and crustose coralline algae on reefs. However, and as we saw from the results of excess nitrogen available to zooxanthellae, the algae are eager to take advantage of increased dissolved nutrients. Such inputs can lead to algal dominance in the lack of sufficient grazing.

To aquarists, this means that a "high nutrient" tank may have algae problems in the lack of adequate grazing. Put another way, if a tank currently has a given level of herbivory and a low nutrient content, increasing dissolved nutrients may allow algae to increase and become problematic without a subsequent increase in herbivores. Even so, the higher nutrient levels may cause corals and other symbiotic partnerships to decline as the partner algae preferentially utilize the increased nutrient sources to the expense of the host.

Without question, corals and many reef organisms are able to utilize dissolved nutrients to help meet their energy requirements and to use in tissue growth. However, of all the nutrient sources available, and discussed in the previous articles in this series, these may be the least desirable to provide - both in aquariums and to wild reef communities.

This concludes my series on the "food of reefs." I do hope it has been enlightening and provides readers and aquarists with a more complete view of how the organisms in our tanks acquire the materials they need in order to grow and thrive in our aquaria. If nothing else, I hope it serves to emphasize the importance of adequate nutrition not only for corals, but for our miniature reef tank ecosystems. I conclude with a quote by Kenneth Sebens that I have used often in my writings, postings, and presentations to underscore a very simple point that has, for far too long, been an inappropriate assumption by too many reefkeepers:

"Corals Are Not Plants."

Links to Part 1, Part 2, Part 3, Part 4, Part 5, Part 6

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