12.6: Primary Production and Nutrients

Phototrophic organisms require many elements for growth. Carbon, hydrogen, and oxygen are obtained from dissolved carbon dioxide and water. Because carbon dioxide is abundant in seawater (Chap. 5), carbon is plentiful in the ocean. Several other elements are required, each in different amounts. Some, such as magnesium and sulfur, are present in high concentrations in seawater. As with carbon dioxide and water, they are always available in plentiful amounts. Other elements, such as nitrogen, phosphorus, iron, zinc, cobalt, and, for some species, silicon, are needed sometimes in substantial quantities but are present in low concentrations in seawater. In some areas, uptake by organisms or by processes such as adsorption on lithogenous particles can remove enough of these elements from solution that the remaining concentrations are too low to meet the needs of some species of autotrophs. Growth of phytoplankton, marine algae, and other species can be limited by the unavailability of a single essential element. In this condition, the system is said to be nutrient-limited.

Where growth is slowed or prevented because the concentration of a particular element is too low, that element is called a limiting nutrient. The most important limiting nutrients are nitrogen as dissolved inorganic ions nitrate (NO^3–), nitrite (NO^2–), and ammonia (ammonium ion NH⁴⁺ and NH³⁺); phosphorus (phosphate ion, (PO₄)^3-), iron; and silica (probably present in seawater as silicic acid: H₂SiO₄). When inorganic nitrogen and phosphorus ions are at very low concentrations, phytoplankton will often use organic nitrogen and/or phosphorus compounds. Although other nutrient elements, such as cobalt and zinc, are present only as trace elements, biological requirements for trace elements are so small that these elements generally do not limit phototrophic growth. Some marine species that are otherwise autotrophs may need certain organic compounds that they are unable to synthesize for themselves. In certain circumstances, including some newly upwelled water in coastal upwelling zones (Chap. 15), primary productivity may be limited by lack of such organic nutrients.

Nutrient Uptake

Phytoplankton and other autotrophs obtain nutrients from seawater through their outer membrane, relying on the random movements of nutrient ions to that membrane. At lower nutrient concentrations the nutrient ions are farther apart and the probability that an ion can diffuse to the cell outer membrane is lower. More nutrient ions will be in contact with a cell that has a larger surface area. Hence, autotrophs improve their chances of capturing low concentrations of nutrient ions if they have a large surface area. Because phytoplankton and other autotrophs are composed of similar organic compounds, their nutrient needs are approximately proportional to their volume. Recall that, the ratio of surface area to volume generally is greater for smaller than for larger organisms. Thus, phytoplankton compete more effectively for nutrients at low concentrations if they are small (their surface area is large in relation to their volume). This is one reason that most marine autotrophs are small, particularly where nutrient concentrations are low.

Small size is not the only adaptation that allows phytoplankton to compete for a limited supply of nutrients. When phytoplankton grow in seawater with relatively high nutrient concentrations, they take up more nutrients than are immediately needed. The excess nutrients are stored and can be used as a reserve to support growth and reproduction after nutrients have been depleted to concentrations that would otherwise limit growth. If concentrations remain growth-limiting for more than a few days, even the stored nutrients will be used up and primary productivity will slow. However, phototrophy is not completely halted, because some nutrients are continuously made available by recycling (Fig. 12-3).

Nutrient Recycling

Nutrients are recycled to solution when organic matter is decomposed during animal and decomposer respiration. Animals excrete nutrients in fecal material and in dissolved form, either in the equivalent of urine or by diffusion losses through external membranes. Bacteria and other decomposers act as recyclers and release nutrients as they extract energy from dead organisms, fecal material, and dissolved organic compounds. The four most important limiting nutrients are recycled at different rates: phosphorus is recycled very rapidly, nitrogen more slowly, and iron and silica more slowly yet.

Phosphorus

Phosphorus recycling is relatively simple (Fig. 12-6). Phosphate is returned to solution rapidly after the death of any organism by the action of enzymes within the organisms that break phosphorus away from organic molecules with which it is combined. Phosphorus is converted directly to phosphate and released to solution. Enzyme-mediated release of phosphate also occurs within living zooplankton and other animals as they digest their food. Certain zooplankton species are known to excrete as much as 60% of the phosphorus taken in with their food. More than half of what remains is disposed of in fecal pellets, from which it is rapidly released by continued enzyme activity as the fecal material is attacked by decomposers. While much phosphorus is recycled in the water, some sinks to the seafloor sediments. Once released to solution, this phosphorus can migrate into the water column through sediment pore water movements or hydrothermal vents where water movements can eventually bring it back to the surface where it can fuel new life.

Figure 12-6. Simplified representation of the phosphorus cycle in the oceans. The boxes represent compartments (CC10) or components of the system among which the phosphorus is distributed. The ovals represent processes that transport or convert the phosphorus between these compartments. Thicker arrows show more important pathways. Phosphorus is recycled rapidly between solution and organisms in the photic zone. Thus, although some phosphorus is progressively transported below the thermocline, the low concentrations present in some ocean surface waters are still usually sufficient to support phytoplankton growth.

Because it is recycled rapidly, phosphorus is usually not a limiting nutrient in the oceans. In contrast, phosphorus is often the limiting nutrient in lakes. As a result, phosphate-free detergents are required by law in many areas, primarily to prevent eutrophication in lakes and rivers.

Nitrogen

Nitrogen, which occurs in living tissue mainly in amino acids, is released during the decomposition of organic matter, primarily as the ammonium ion (Fig. 12-7). Animals also release nitrogen in their liquid excretions as soluble organic compounds, such as urea and uric acid, which are broken down by decomposers to the ammonium ion. Decomposition of particulate organic matter to release ammonium is much slower than processes that release phosphorus. Consequently, nitrogen often becomes the limiting nutrient in the marine environment.

Figure 12-7. Simplified representation of the nitrogen cycle in the oceans. The boxes represent compartments (CC10) or components of the system among which the nitrogen is distributed. The ovals represent processes that transport the nitrogen or convert its chemical form between these compartments. Thicker arrows show more important pathways. Unlike phosphorus, nitrogen is not recycled rapidly in the photic zone, and it tends to be transported below the thermocline. Thus, nitrogen is often the limiting nutrient. Nitrogen can be recycled from shallow seafloor sediments (as depicted for phosphorus in Figure 12-6), but these pathways have been omitted in this figure to reduce its complexity.

The ammonium ion is used as a source of energy by specialized bacteria and, as discovered more recently, vast numbers of archaea that oxidize ammonium to nitrite. In turn, nitrite is oxidized to nitrate by another group of bacteria. Conversions from ammonium to nitrite and nitrate take place relatively slowly. Nevertheless, in waters below the photic zone this process can be completed, and nitrate is the principal form of dissolved nitrogen other than molecular nitrogen in the aphotic zone. Although the ammonium ion is the preferred source because it requires less energy to capture and use, it is taken up so rapidly that the more abundant nitrate is often the primary nitrogen source, even in the photic zone. Conversion to nitrate may also be completed in temperate latitudes during winter, when reduced light availability limits primary productivity. Such seasonal variations are discussed in Chapter 13. 

Because nitrogen may be predominantly ammonium, nitrite, or nitrate ions at different times and locations, primary producers are generally able to utilize nitrogen in each of these forms. Nitrogen and phosphorus are both supplied to the oceans by river flow, erosion, and weathering from the land, and, in small amounts, in rain and dust (Figs. 12-6, 12-7). The biogeochemical cycle (Chap. 5) is balanced in each case by the removal of equivalent amounts of nitrogen and phosphorus to the ocean sediment in detritus particles. This balance has been disturbed by human activities, particularly through the use of agricultural fertilizers and the discharge of sewage (Chaps. 13, 16). The supply to and removal from the oceans of biologically available nitrogen are complicated by the exchange of molecular nitrogen gas between the atmosphere and ocean waters. Molecular nitrogen dissolved in ocean waters is biologically available only to nitrogen-fixing bacteria and archaea that are able to convert molecular nitrogen to nitrate. Other types of bacteria and archaea, called “denitrifying,” can convert nitrate to molecular nitrogen. Although nitrogen fixation and denitrification are very limited, nitrogen fixation in particular is thought to be extremely important in some nutrient-poor environments, such as coral reefs and the centers of subtropical gyres. Phosphorus does not usually become the limiting nutrient because it is readily released from detritus back into solution in the photic zone and, as a result, only a small fraction of the phosphorus remains in the detritus that sinks below the photic zone. However, if the supply of nitrogen through nitrogen fixation is continuous, even if very slow, phosphorus can eventually be depleted and become the limiting nutrient.

Silicon

Silicon is essential for the construction of hard parts (the shells or skeletons) of a variety of marine organisms, of which diatoms (Fig. 6-7) are the most important. Diatoms are larger than many other types of phytoplankton and are covered by an external silica (SiO₂) frustule.

Silica is not soluble, so organisms must create their hard parts from silicate ions ((SiO₄)^4-) which are soluble. Silica is not utilized or released to solution by decomposers, so silica hard parts must dissolve chemically in seawater before silicate ions are again biologically available. Silica dissolves very slowly (Fig. 6-10). Consequently, once silicate is depleted in the photic zone, silicate limitation inhibits the growth and reproduction of organisms with silica hard parts. Because phytoplankton that do not have silica hard parts are not affected, silicate depletion can lead to a change in the dominant species, but it does not limit primary productivity. Silicate is supplied to the oceans in large quantities by rivers and is slowly dissolved from ocean sediment. Therefore, silicate limitation is generally only a temporary situation that develops in locations where diatoms undergo an explosive population growth called a bloom.

Iron

Iron is essential to certain reactions within the process of photosynthesis. Iron is supplied to the surface waters of the oceans from the land, primarily in runoff, but also through the transport and deposition of airborne dust. Iron is also continuously transported below the photic zone in detritus. As a result, iron can become the limiting nutrient in areas of the oceans where inputs from the continents are too small to replace the iron that is lost from the surface layers by sinking of detritus. 

Iron is now thought to be the primary nutrient that limits primary production in large areas of the open oceans where river and dust inputs of iron are low.

High Nutrient Low Chlorophyll (HNLC) Areas

In approximately one third of the area of the oceans there is always sufficient biologically available nitrogen (and phosphorus) but chlorophyll concentrations are very low. These are known as high nutrient, low-chlorophyll (HNLC) areas. Chlorophyll concentration and primary production are closely related so chlorophyll is a proxy measurement of primary production. HNLC areas have plentiful nitrogen and phosphorus but low chlorophyll concentrations indicating low primary productivity so some factor other than nitrogen and phosphorus must limit primary production in these regions.

There are at least three different possible reasons for the low primary productivity of HNLC areas. 

• In some areas, wind mixing can be strong enough to transport phytoplankton well below the depth of the photic zone. Phytoplankton cells can then spend too large a percentage of their time without sufficient light for phototrophy. This mechanism appears to be important in limited areas and only during strong wind events but it is likely to apply in some areas, including parts of the Southern Ocean.
• Phytoplankton biomass is kept extremely low due to very high rates of predation by zooplankton. High rates of predation can reduce the average length of time during which each phytoplankton cell lives and can photosynthesize. There is strong evidence for the effect of this mechanism in parts of the subarctic North Pacific Ocean and of the eastern equatorial Pacific Ocean.
• Phytoplankton growth is limited by the lack of availability of nutrients other than nitrogen and phosphorus such as iron or zinc.

Although a lack of other nutrients such as zinc may be possible in some areas, a lack of available iron is now thought to be the primary mechanism limiting productivity in most of the world’s HNLC areas. Iron is supplied to the oceans primarily from rivers and wind blown dust and it is highly insoluble in oxygenated sea water. HNLC areas are, therefore, in the open ocean far from the continental shelf and river inputs, and in areas that do not receive large inputs of iron containing wind blown dust. These areas include the sub-Arctic Pacific Ocean, large areas of the equatorial Pacific Ocean, and much of the Southern Ocean.

Nutrient Transport and Supply

Substantial quantities of nutrients are supplied to the oceans by rivers, and smaller quantities are supplied in rainfall (and for some elements wind blown dust). In the open ocean remote from river influences, nutrients in the photic zone are depleted rapidly by growing phytoplankton and other autotrophs. Therefore, if primary production is to continue, nutrients must be resupplied. Some nutrients are continuously recycled and resupplied directly to the photic zone by decomposition. However, there must also be nutrient resupply by upwelling from below the photic zone because a proportion of the nutrients taken up by primary producers is released back to solution in waters below this zone.

Nutrients are transported from the photic zone to the aphotic zone by two major mechanisms. Almost all phytoplankton are eaten by grazers (herbivores or omnivores). Although these grazers are mainly small zooplankton, most are much larger than phytoplankton. Much of these animals’ undigested waste material is excreted as fecal pellets. Fecal pellets from even the smallest zooplankton are packages of partially digested remains of numerous phytoplankton cells. Consequently, fecal pellets are larger than phytoplankton and sink much faster (CC4). As they sink, fecal pellets provide food for other heterotrophs, bacteria, and fungi and are progressively decomposed with some or all of the nutrient elements being released to solution. Much of the decomposition and release of nutrients occurs below the photic zone, including on the ocean floor.

The second major mechanism of nutrient removal from the photic zone is the vertical migration of zooplankton and other animals. Phytoplankton generally remain in the photic zone unless carried out of it by turbulence or downwelling. However, many species of zooplankton and other animals migrate vertically between the photic and aphotic zones each day, rising into the photic zone at night to feed, and then sinking or swimming down to waters below the photic zone during the day. This diel vertical migration is probably a defensive mechanism that prevents many potential predators from feeding on the zooplankton when it is light enough to see them easily, while also allowing phytoplankton communities to recover and multiply during the day, ensuring a sustainable food supply for zooplankton when they return to the surface layer to feed. Zooplankton and other animals that practice diel vertical migration continue to digest food and excrete fecal pellets and liquid wastes during the day when they are below the photic zone. Consequently, much of the organic matter that they consume is transported below the photic zone, where it is released, with its nutrients, to the decomposer community.

Vertical Distribution of Nutrients 

The photic zone is usually less than 100 m deep in the open oceans and normally restricted to water above the permanent thermocline (Chap. 8). Phytoplankton and nutrients are distributed throughout the mixed layer, above the thermocline, by turbulent motions of wind and wave mixing (Chap. 8). Where light is sufficient to support primary production in the open oceans away from terrestrial sources of supply, nutrients are continuously transported below the thermocline by the mechanisms already described. Below the thermocline, these nutrients are released by decomposers, but the water into which they are released does not mix with the mixed-layer or photic-zone water above, because vertical mixing is inhibited by the density difference across the thermocline. Consequently, the mixed layer becomes nutrient-depleted, while deeper water becomes more nutrient-rich (Fig. 12-8).

Figure 12-8. General representation of the vertical profiles of water density, nitrate, phosphate, silicate, and dissolved oxygen concentrations in the center of the Atlantic Ocean basin. Dissolved oxygen concentration is high above the thermocline, reaches a minimum just under the thermocline, and then increases to somewhat higher levels in the deep water masses formed by cooling of surface water at high latitudes. Nutrients (nitrate, phosphate, silicate) are generally depleted in the photic zone, increase rapidly in concentration until they reach a maximum at about the same depth as the dissolved oxygen minimum, then remain at relatively constant high levels in the deep water masses.

Organic matter is decomposed continuously at all depths in the oceans, although the rate of decomposition varies with depth. Hence, water that leaves the surface to form deep water masses progressively accumulates recycled dissolved nutrients. Nutrient concentrations are usually highest in water immediately below the thermocline layer. The primary reason for this nutrient maximum is that this is the “oldest” deep water because it is formed by slow upward mixing of bottom waters that were formed near the poles (Chap. 8). The effect of water-mass “age” in determining nutrient concentrations is illustrated by the nutrient concentration differences between the deep waters of the Atlantic Ocean and the much older deep waters of the Pacific Ocean (Fig. 12-9).

Figure 12-9. The vertical profiles of nitrate nitrogen and dissolved oxygen in the North Atlantic (south of Greenland), South Atlantic, and North Pacific Oceans are very different. In the North Atlantic, where cooled surface water is sinking to form North Atlantic Deep Water (NADW), the concentrations vary little with depth. During its passage southward to the South Atlantic, this water mass loses oxygen and gains dissolved nitrate as respiration by animals and decomposers uses oxygen and releases dissolved nitrate. This process continues as the water mass moves around Antarctica and northward into the deep water of the Pacific Ocean. Thus, the ratio of nitrate concentration to oxygen concentration is an indication of the “age” of the water mass since it left the surface layer. Higher ratios indicate “older” water. The “oldest” water has too little oxygen for animal life to survive in and areas with this low level of oxygen are called oxygen minimum zones (OMZs).

Several additional factors cause concentrations of nutrients to be higher in waters just below the bottom of the thermocline than in bottom waters. First, bacterial decomposition processes are slowed at the low temperatures and high pressures near the deep-ocean floor. Second, the most easily oxidizable organic matter is decomposed long before it reaches the ocean floor. Third, animals that migrate vertically generally do not descend far below the permanent thermocline. However, these influences on the vertical distribution of nutrients, even taken together, are less important than the age of the water and the length of time during which recycled dissolved nutrients have accumulated in it.

The permanent thermocline is a persistent and widely distributed feature. Primary productivity above the thermocline is nutrient-limited except in areas where nutrients are transported into the mixed-layer waters by inputs from the continents or by upwelling of nutrient-rich water from below the thermocline. Major zones of high primary productivity and highly productive fisheries are found in coastal upwelling regions, off the mouths of rivers (which discharge nutrients), and in shallow areas where nutrients in sediments are returned to solution by decomposition and then released directly into the photic zone.