The Nutrient Dynamics of Coral Reefs:
Part II, The Oceanic System


The first article addressed several topics, with the bulk of the discussion focusing on global patterns of material flow within the biosphere. The three elements we examined were carbon, nitrogen and phosphorus due to their importance in ecosystems, and because of the tendency for the growth and reproduction of living things to be limited by access to these resources. This month we will focus on factors critical to ecosystem function and conclude with a discussion of some of the patterns in the oceanic ecosystem.

An Ecosystem Is…

I've used the term ecosystem several times already, but I haven't really defined what an ecosystem is. An ecosystem is a particular assemblage of living organisms (called biotic factors) along with the non-living components (called abiotic factors) present in an environment that exert influence over each other. For example, the kelp forests off North America's west coast can be referred to as an ecosystem. Upwelling of deep oceanic water results in a high availability of nitrogen and phosphorus. These encourage phytoplanktonic growth as the base of a complex food web that eventually results in productive fisheries. This upwelling is controlled primarily by winds that blow parallel to the coast. Without the wind there would be no upwelling, without the upwelling there would be no abundance of nutrients, and without the growth of phytoplankton from the nutrients there would be no fisheries. In addition to the importance of abiotic factors such as wind, nutrient concentrations and currents, certain organisms live in this place and exert influence over one another as well. Kelp provides habitat for many of the fishes of economic interest. Sea urchins eat the kelp, but sea otters eat the urchins. Without the otters the urchins would multiply extensively and graze the kelp to their holdfasts, destroying the habitat for the fishes. Without the otters there would be too many urchins, and when there are too many urchins there is no kelp, and when there is no kelp the fisheries collapse. Both biotic and abiotic factors shape the structure of an ecosystem. An ecosystem needn't be large, either. A pool of water in a dead leaf on the forest floor is rightfully considered an ecosystem. Countless types of bacteria, fungi, flagellates and other microbes decompose organic matter in the water. Ciliates feed on these microbes and, in turn, are fed on by insect larvae. Temperature, pH, incident light, rainfall and many other factors contribute to the workings of this little living world. Additionally, ecosystems contain a variety of food chains forming a food web. A food chain is a graphic, linear representation describing which organisms feed on which other organisms. A food web is made up of many interconnecting food chains. These are discussed further below.

For an ecosystem to form in any environment, one fundamental requirement must be fulfilled: there must be a source of energy that is useable by living organisms and there must be organisms present that are able to utilize that energy.


In lay terms, if we say we've had a very productive day, we mean that we have accomplished many of our goals in a short period of time. An unproductive day means we have accomplished very few of our goals during that time. We use this term in everyday language to describe how fast we are accomplishing our tasks, and it is used in much the same way in ecology. In the plainest sense, the goal of every living thing is simply to stay alive, grow to maturity, and to reproduce. As such, the terms productivity, production or productive are used in ecology to signify the rate at which new materials are produced from their precursors by living things, whether they are new tissues within an organism, offspring or even carbohydrates that leak from a cell. The productivity of an organism or population is the rate at which it turns resources into more of itself. Productivity represents the flux of nutrients from the environment into living organisms.

Often we may want to know how fast not only a single species is growing and reproducing, but how fast all species are growing and reproducing within a given area. One might go to the far north and see the extensive boreal forests, full of countless and massive trees. One might also go to the equatorial region and see the extensive tropical rainforests there, full of countless and massive trees. In this way the two ecosystems appear rather similar. The trees in the boreal forest, however, experience a very short growing season, perhaps less than eight weeks. While the forests are vast and the trees gigantic, they grow rather slowly as an annual community average, as do the other plants in the forest. This environment shows relatively low productivity. In the tropical rainforest the growing season is year-round. Not only the trees, but especially the forest's other plants, grow at incredibly fast rates, much faster than those in the boreal forest. This environment shows relatively high productivity.

The rate of production in an ecosystem bears great importance on a variety of ecological questions. For instance, a grazing animal might need to eat some amount of plant material per day to be healthy and grow normally. In a highly productive habitat the organism won't have to travel far to get sufficient food. It can graze one area, move on to another, and then return to the original area in short order since the vegetation will have grown back in a short period of time. In a less productive habitat the grazer will have to wait a very long time before it can return to the original patch because that vegetation grows much more slowly. This means each of this species' grazers and any competitors for these resources must all have larger ranges and travel more to acquire sufficient food than they would if they lived in the more productive habitat. The result is that less food is available in areas with low productivity, and these habitats support fewer numbers of individuals (as well as lower species diversity often times, though not always) than habitats with relatively higher productivity. Another example, and one that's important to humans, involves natural food production. Sardines have very high rates of productivity and can, at least potentially, be harvested at high rates year after year. Most shark species, on the other hand, have very low rates of productivity, and even just a few years of intensive harvest can decimate a shark population for decades or more. In fact, this is exactly what has happened in most places today, though even the ultra-productive sardines have been overharvested in some places, even to the point of the collapse of the fishery.

Because the major source of energy for terrestrial and shallow, aquatic environments is sunlight, the presence of plants, algae and bacteria capable of capturing that energy is the critical element that allows the formation of the ecosystems with which we are most familiar. These organisms are the proximate source of energy and most nutrients for every other organism within the ecosystem. For this reason plants, algae and photosynthetic bacteria are termed primary producers, because they produce the organic material necessary to support the rest of the ecosystem. Herbivores that feed directly on primary producers are called secondary producers or, often times, primary consumers. They are the second link in a food chain, hence the secondary producers, but are the first group of organisms that consume already formed organic materials. Carnivores that eat these herbivores are usually called simply secondary consumers or, rarely, tertiary producers. Carnivores that eat these carnivores would be tertiary consumers. These links in the food chain are called trophic levels, with each being higher than the last (first, second, third, fourth, etc.). Terrestrial food chains rarely have more than four links, though exceptions certainly exist. An example of such a chain might be:

grasses grasshoppers songbirds falcons

Aquatic ecosystems' food chains tend to be slightly longer than those on land, with five to seven links, but are rarely longer. An example might be:

phytoplankton zooplankton larval fish small fish large fish

Some might be wondering why food chains tend to be limited to so few links. Why not have a "very large fish" that eats the "large fish" above, and then a "very, very large fish" to eat that one, and then a "very, very, very large fish" to eat that one? Certainly, the reason is not biological or physical limitations on what can be consumed. Many fish can certainly eat other fish only slightly smaller than themselves (or even larger, as some owners of Antennaris spp. can attest!). Why not have a 2 cm-long fish eat a 1 cm-long fish, and then a 4 cm-long fish eat the 2 cm-long fish, and then a 6-8 cm-long fish eat the 4 cm-long fish, and on up to the size of white sharks? Why not have hundreds of links in a food chain? Ahh, good question young student-of-life-as it turns out there is a very important reason this does not happen, and it is explained by the Second Law of Thermodynamics.

The Second Law of Thermodynamics

"The entropy of an isolated system will tend to increase over time approaching a maximum value."

…so what the heck does that mean? A simpler way to say this is that all natural systems tend to move from order (everything is arranged nicely) to disorder (everything is completely jumbled and homogenized) without the input of energy. Think of a nice, ordered playroom where all the toys are put away in bins, the paint is in the jars and the room is spick-and-span. Everything has its place and everything is in its place; there is order. What happens after releasing some children into the room for awhile? Disorder! The toys go everywhere, the paint inevitably ends up on the walls, and everything becomes thoroughly disorganized. No matter how long we wait, the toys will not go back into their bins by themselves, the paint will not clean itself off the walls, and the room will not become organized without an input of energy to make all of this happen. Undoubtedly, the input comes from some frustrated parents, but I digress. The important point to glean from this is as follows: everything in nature moves from order and organization to disorder and homogenization without the input of energy to prevent it from happening.

Another consequence of this law is that no transfer of energy is completely efficient. When wood is burned in a campfire to roast marshmallows, some of the energy is released as infrared radiation, which does the roasting, but a great deal is also lost into the environment as unused infrared radiation (i.e., infrared that does not directly roast the marshmallow), some is lost as light, some is lost as sound, etc. What this means is that every time the energy is converted from one form to another, some of it is lost to the environment (entropy is increased).

How does this help us to understand ecosystem ecology? First, living things are ordered structures in a sea of chaos. Almost everything about a living cell distinguishes it from its environment. Let us consider a human body. Mostly it is made of water, yet this water tends to quickly evaporate into the air in which we live. Our body contains salt, yet this salt is not leaked into the water if we swim in a lake, nor are we flooded by salt if we swim in the salty ocean. We maintain body temperatures at 37° C (98.6° F) even as the temperature around us rises above, and dips well below, that temperature. The proteins in our bodies maintain their shapes, even as chemical and physical laws work to break them apart. Maintaining this order, that is, being unique from the environment that surrounds us, requires a constant supply of, and a great deal of, energy. Much of the energy in the food we eat, however, is lost to our environment because no energy transformation from one form to another is ever 100% efficient. We lose a great deal of energy as radiant heat to our cooler environment, as sound while performing various tasks, as mechanical energy as we move objects, etc. We also lose some of the energy in our food as undigested material. For example, we and most organisms can't digest cellulose-fiber-and therefore gain no energy by eating this material, because it is not digested, though it took the original capture of a great deal of energy from the sun to produce that cellulose by whatever plant made it. With every step up a food chain there is less and less of the energy that was originally captured transferred to the next trophic level.

So, how much energy is transferred from one trophic level to the next? The true value depends on many factors, but for most organisms this value is about 10% of the energy they consume. In other words, to produce 1 lb. of cow you need about 10 lbs. of grass. In order to produce 1 lb. of salmon you need about 10 lbs. of small fish, about 100 lbs. of zooplankton to produce the small fish and about 1000 lbs. of phytoplankton to produce the zooplankton. Only five links require 10,000 lbs. of primary producer to produce 1 lb. of top predator, 100,000 lbs. with six links and 1,000,000 lbs. of primary producer to produce a single pound of top predator with a seven-link food chain! Now we can appreciate why food chains longer than this tend to be so rare. Usually, food chains longer than seven links (which do exist, especially in the ocean) are able to exist only because one or more of their links are far more efficient producers than those in the above examples, hence more energy is passed on than otherwise would be.

Oceanic Productivity

We understand now that productivity is a very important parameter influencing how an ecosystem functions. The logical question for all of us is how productive are the oceans, especially the tropical oceans where coral reefs grow? A multitude of factors influence precisely how to answer this question, but in general we can say, "not very," especially as compared to many other ecosystems. Typically when we discuss the productivity of an ecosystem we mean its net primary productivity, that is, the sum of all net production of all species of primary producer; in other words, how fast the plants, algae and photosynthetic bacteria in a given area are growing. Often this value is expressed as the dry weight of production in grams of carbon per square meter per year (g C m-1 yr-1), though it might also be expressed in some other set of units (e.g., grams of carbon per square meter per day) depending on the information being presented. Figure 1 shows the mean rates of primary production for a number of biomes. These are average values and some geographic variation is to be expected.

Notice that the open ocean is at the far left. It is one of the least productive of the world's major biomes over a given area (though it is by far the largest biome and therefore contributes a major portion to worldwide productivity, despite its own poor rate of productivity, because of its immense size). Why is the open ocean so relatively unproductive? Actually, the reasons are rather simple; so simple, in fact, that two boxes with a few lines drawn between them has proven to be a good model of what is happening in this complex system.

Figure 1. Mean net primary production in selected ecosystems.

A Bit of Oceanography

If a person swims in a lake in the temperate zone during the summer and dives into deeper water, he or she will probably notice that the surface water is very warm and abruptly becomes several degrees cooler as he or she descends, and then remains at this cooler temperature. In fact, during the summer this lake will become stratified such that a thin layer of warm water is floating on a thick layer of cold water. While water is obviously quite fluid and it seems as though the two layers should mix easily, just the opposite happens. A thin zone called a thermocline is established where the temperature changes abruptly. It is almost as if there are two separate water bodies, one over the other. Things that swim, sink or float can move between these two layers easily enough, but anything that moves with the water (such as dissolved substances like the nutrients necessary to fuel algal growth) can and does become trapped in whichever layer it happens to be in before the thermocline is established. During the Fall the top layer is not heated as much by the sun as it is during the summer, so the thermocline begins to break down and the water layers begin to mix. During the Winter there is no thermocline at all and the water becomes well mixed. During the Spring the thermocline begins to reestablish and the lake again begins to divide into two separate layers. This same general pattern is also observed in the ocean, though its large size allows this phenomenon to manifest in at least three different ways.

In the polar oceans the sun is strong enough to establish only a slight thermocline during the summer and no thermocline during the rest of the year, so the surface and deep water tend to stay well-mixed throughout the year and not to stratify. The temperate seas tend to follow seasonal stratification and mixing scenarios like those described above. In the tropics there tends to be a constant thermocline due to the perpetual heating by the sun, and thus the surface and deep waters tend to be constantly separated. This thermocline occurs rather deeply in the tropics, at approximately 100-200 m (330-660 ft.), in other words, deeper than any of the animals we might normally keep in a reef aquarium. I must point out that this oceanic thermocline is distinct from the transient thermoclines that sometimes become established in shallow water and might be felt by a diver as they descend on a reef. The two are very different. The oceanic thermocline could be approached only by a technical diver on a very deep and potentially dangerous dive. Additionally, there is relatively slow mixing between polar and temperate oceans and temperate and tropical ones on the surface. Because coral reefs are found only in shallow, tropical waters, the ocean around coral reefs can be treated as a semi-isolated water body with slow rates of mixing with the rest of the ocean, though certainly mixing does still occur.

Again, particles can move between these layers if they sink, float or can swim, but dissolved substances are essentially trapped. One of the hallmarks of the open ocean (often called the oligotrophic ocean) is the extreme scarcity of dissolved nitrogen and phosphorus sources that can be used by primary producers. Furthermore, the standing stock of primary producers is extremely low. Higher trophic levels are only very slightly more abundant than lower levels in terms of standing stock. The shallow, tropical ocean is devoid of neither life nor nutrients but, compared to many ecosystems (especially terrestrial ecosystems), it has a relatively low concentration of both inorganic and organic nutrients. On the contrary, deep oceanic water anywhere in the world, including in the tropics, tends to be quite rich in inorganic nitrogen and phosphorus that can be used by algae (though there is insufficient light at these depths for algae to grow). We might ask why there is a large supply of nutrients in the deep water and a short supply in the shallow water. It is for two reasons: 1) the lack of mixing between deep and shallow water as explained above, and 2) the biological pump.

The Biological Pump

When a phytoplankter takes up inorganic carbon, nitrogen and phosphorus from its environment (and any other nutrients or materials, for that matter), it reduces the pool of these dissolved nutrients in the water that surrounds it. These nutrients are used for the growth and maintenance of that algal cell and when the alga acquires enough nutrients, it splits into two daughter cells. Both of these daughter cells take up nutrients from their environment, further lowering the available supply in the water. They then grow and reproduce, splitting into four cells. Then these four cells continue their activities just as their parent cells did. Given the growth rate of most phytoplankton, it is easy to see that they will quickly draw down the inorganic nutrient supply in the water and fill the water instead with algal cells. While they are alive these phytoplankton tend to remain neutrally buoyant through various flotation mechanisms, but many are negatively buoyant without the expenditure of energy. Thus, when they die they begin to sink. The same is true of most other forms of life such as zooplankton and nekton such as fish and whales. Most of this production is decomposed in the water column and mineralized into inorganic components. How quickly a particle is decomposed (primarily by heterotrophic bacteria) depends primarily on its size and how labile it is. A tiny algal cell will be decomposed much more quickly than a Humpback whale, for example.

If either a phytoplankter or a whale die at the surface, they will begin to sink and bacteria will begin to decompose them. As they are decomposed the organic molecules they are made of will eventually be reduced to inorganic ions (nutrients) and released into the water, where they can be absorbed and reused to fuel the production of more phytoplankton. The algal cell will likely be completely or almost completely decomposed before it reaches the thermocline. There will have been a flux of nutrients from the water to the alga as it was born and grew, and then back to the water after it dies and decomposes, but there will be no net addition or loss of any nutrients from the surface waters. The whale, on the other hand, likely will not be totally decomposed before it reaches the thermocline, but will keep on sinking and decomposing until it is totally decomposed in the water column, or reaches the bottom and is fully decomposed. Either way, it will carry a great deal of nutrients from the surface below the thermocline in the form of a particle. The same happens if the phytoplankter dies nearer the thermocline-it sinks to the deep water layer, and takes all of its sequestered nutrients with it, before it is fully decomposed. These nutrients are mineralized into dissolved substances which do not freely move across the thermocline. In this way the surface waters lose nutrients to the deep ocean. It should also be noted that this allows carbon to be lost from the surface ocean and sequestered in the deep ocean. This mechanism is important to the global carbon cycle and future climate projections. An important point to stress, and one that is often misunderstood, is that particles do not have to reach the bottom of the ocean to remove nutrients from the surface layer; they simply have to sink below the thermocline. The shallow, tropical ocean is, therefore, constantly losing nutrients to the deep sea if these particles are able to sink below the thermocline. Because these layers mix very little, the dissolved, inorganic nutrient pool in shallow water is not recharged seasonally as it is in the temperate zone, or constantly as it is in the polar seas. Therefore, the tropical ocean tends to have perpetually low concentrations of dissolved inorganic nitrogen (DIN) and dissolved inorganic phosphorus (DIP), unless local conditions allow a temporary influx of these nutrients from land, the atmosphere or deep oceanic water (these sources will be discussed in upcoming segments). The productivity of the oligotrophic ocean, especially in the tropics, is therefore low due to nutrient limitation on the phytoplankton. But which nutrient is limiting them, and why?

Redfield's Ratio

Alfred C. Redfield was teaching physiology at Harvard Medical School when he was recruited by Henry Bigalow as a staffer for the newly formed Woods Hole Oceanographic Institute. He split his time, teaching at Harvard during the academic year and doing research at Woods Hole, for more than ten years, until 1942 when he took a one year leave of absence from Harvard (which actually lasted 14 years) to become the Associate Director at Woods Hole.

It was during his work at Woods Hole that he made an observation. The molar ratio of N:P in phytoplankton tends to be very similar to the molar ratio of DIN:DIP in deep oceanic water. He hypothesized, correctly, that it is not the availability of these nutrients that determines the make-up of phytoplankton, but rather the make-up of phytoplankton that creates this ratio in the water. The molar ratio he found for carbon, nitrogen and phosphorus is 106:16:1-106 atoms of carbon for 16 atoms of nitrogen for 1 atom of phosphorus in an average sampling of phytoplankters (Redfield, 1958). This is called a stoichiometric relationship.

You may recall the word "stoichiometry" from your high school chemistry class (or perhaps not, depending on how well you have blocked out those memories!). In chemistry, stoichiometry is often introduced when students are taught to balance chemical equations. Stoichiometry refers to the relative proportion of constituents in a material. Likewise, the stoichiometric relationship between car wheels and drivers is 4:1 whereas that of motorcycle wheels to drivers is just 2:1. Understanding the stoichiometry of living organisms and how this impacts their interactions with each other and with their environment is often referred to as ecological stoichiometry. To be clear, these are molar ratios, not mass ratios. The mass of a phosphorous atom is more than double the mass of a nitrogen atom. Thus, a molar ratio of 16:1 N:P becomes nearer 7:1 as a mass ratio. This is an important point to consider, as hobbyists usually measure dissolved nutrient concentrations in parts per million (ppm), which refers to mass, not moles.

Misunderstanding Redfield's Ratio

Unfortunately, all too often Redfield's ratio of 106:16:1 atoms of carbon, nitrogen and phosphorus has been interpreted not as the outcome of the interaction of thousands of species of phytoplankters over many generations' worth of time, but rather as the stoichiometric relationship to be expected in all phytoplankton (or worse yet, all algae) and all oceanic waters all of the time. Simply put, this is a gross misinterpretation. Some species of phytoplankton normally have N:P ratios of more than 45:1 (Klausmeier et al, 2004). Others might have N:P ratios as low as 8:1 (Klausmeier et al, 2004). It is the aggregate response of entire communities over many generations that produces the observed pattern. In fact, Atkinson and Smith (1983) found that benthic algae like those that grow on coral reefs or in our tanks tend to have a mean ratio of 550:30:1 atoms of C:N:P. Therefore, we should not expect the water in our tanks to always have molar N:P concentrations of 16:1, or even 30:1, or that variance from these ratios necessarily represents either nitrogen or phosphorus limitation of the algae in our systems. Not only do different species of algae grow with different N:P ratios, so do the same species, within a range of tolerance. I have seen hobbyists with slightly elevated DIN levels and barely detectable DIP levels dump significant amounts of various phosphate supplements into their tanks in an attempt to alleviate P-limitation and cause the algae to consume the nitrogen. They didn't drop their DIN concentrations, but they did cause significant damage to their corals and their tanks in general. There is no reason to think that our tanks should precisely reflect these ratios all of the time. In fact, N:P ratios of 10:1-20:1 for phytoplankton are often considered to represent cases of co-limitation, because most phytoplankton that can grow with a 16:1 ratio can easily grow in the range of 10:1-20:1 (Hamilton, pers. comm.). Addition of either N or P often stimulates growth of phytoplankton in such a situation…except in the Southern Ocean.

The Southern Ocean is both temperate and subpolar in parts. It contains plenty of available nitrogen and phosphorus to stimulate significant phytoplanktonic growth during the warmer months of the year, just like in the Northern Hemisphere, yet this is the least productive part of the ocean. As I mentioned last month, carbon, nitrogen and phosphorus are most frequently the limiting nutrients for organismal growth, but they're not the only nutrients that can limit growth. Nutrient limitation occurs when the supply of any required nutrient is low relative to how much is needed. If we extend Redfield's ratio to include iron, we find that phytoplankton tend to have a stoichiometric relationship of 106:16:1:0.005 atoms of C:N:P:Fe. The primary productivity of much of the Southern Ocean is limited by the availability of iron (Behrenfield and Falkowski, 1999; De Baar et al, 1990; Martin et al, 1991).

If nothing else, this must remind us as reef aquarists that not every interaction involving algae or nutrients in our tanks is simple or necessarily obvious, and that nitrogen and phosphorus, while very important pieces of the puzzle, are still just two pieces of a large and complex whole. Idiosyncratic interactions in ecosystems as diverse as a coral reef are commonplace, and if we are to appreciate these interactions and how we can better maintain our tanks, we must consider them.

Where do we go next?

My goal in the rest of this series is to bring to light not only the simple and well established interactions between nutrients, algae and higher organisms on a coral reef, but also to draw out many of the complex or little-known influences that each has on the other, and to make this information accessible to average reef hobbyists in ways that will improve how they design and maintain their own reef aquariums on a day-to-day basis.

Some may have noticed in Figure 1 that, while the mean net primary productivity in the oligotrophic ocean surrounding coral reefs is fairly low, the mean net primary productivity of a coral reef is much, much higher-an order of magnitude higher, in fact! How can that be? Why are coral reefs so productive over a given area, when the ocean around them is so unproductive? How do they maintain such large and complex food webs? Next month we will begin to answer these questions and to better understand how and why our aquariums function.

If you have any questions about this article, please visit my author forum on Reef Central.


Atkinson, MJ and SV Smith. 1983. C:N:P ratios of benthic marine plants. Limnol. and Oceanogr. 28(3): 568-574.

Behrenfield, M J and PG Falkowski. 1999. Widespread Fe limitation of phytoplankton in the South Pacific Ocean. Science 283: 840-843.

De Baar, HJW, AGJ Buma, RF Nolting, and GC Cadee. 1990. On Fe limitation of the Southern Ocean: Experimental observations in the Weddell and Scotia Seas. Mar. Ecol. Prog. Ser. 65: 105-122.

Hamilton, SK. 2005. Personal communications.

Klausmeier, CA, E. Litchman, T Daufresne, and SA Levin. 2004. Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature 429: 179-174.

Martin, JH et al. 1994. Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature 371: 123-129.

Redfield, AC. 1958. The biological control of chemical factors in the environment. Am. Sci. 46: 205-221.

Suggested Reading

Nybakken, James W. Marine Biology: An Ecological Approach, 5th edition. San Francisco: Benjamin Cummings. 2001.

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The Nutrient Dynamics of Coral Reefs: Part II, The Oceanic System by Chris Jury -