Introduction

Let's start by reiterating a little bit of what we know about nutrients, algae and the functioning of coral reefs. First, living things' rate of production is often limited by the availability of essential nutrients, as explored in the first article in this series. Second, primary production in the oligotrophic ocean is low primarily due to the scarcity of certain essential plant nutrients (usually nitrogen and phosphorus, but iron and even silicate also play a role) as explored in the second article in this series. Third, the primary production over a given area on a coral reef is much higher-an order of magnitude higher-than the production over a similar area of ocean even though reef water may have very little more in the way of dissolved nutrients. So what gives? If the primary production in the ocean is limited to a low level because of the scarcity of nutrients in the water, how can the production on a reef be higher when water with a similar nutrient concentration is washing over it? In order to support and maintain this level of production it seems that nutrients would have to be coming from somewhere and fueling the algae on the reef. Indeed they are, and one of the important sources of nutrients such as nitrogen, phosphorus and iron is the terra firma located very close to most of the world's coral reefs.

Comparing Earth and Ocean

The dry weight of rich, agricultural soil might be composed of as much as 0.5% nitrogen in the upper layer where plants root themselves and extract nutrients for growth. In a unit more familiar to aquarists, that is 5000 ppm. Let us compare this nutrient concentration to some reported values for seawater over typical coral reefs (see Table 1).

As the table shows, the concentration of nitrogen and phosphorus in oceanic water is much lower than it is on land, but why? When something dies in the ocean it begins to sink and decompose, forming the biological pump as described last month. The nutrients that make up its body are mineralized and eventually mix or diffuse as widely throughout the water column as physical forces allow. If something suspended dies on land it, too, sinks, but through the air. Because air is not particularly buoyant compared to water, we tend to call this falling. Without a doubt, any organism of substantial mass will sink rapidly to the ground and long before it can fully decompose. It is interesting to wonder how long microscopic organisms linger in the air after they die, as they often are as buoyant in the air as many organisms are in the water. Decomposition of organisms on land, therefore, happens on and within solid surfaces. As this mineralization of dead tissue occurs, some nitrogen is lost to the atmosphere as gaseous ammonia, but much of the nitrogen and phosphorus are put into the soil or humus where plants can gain access to them (Bashkin and Howarth, 2003; Schlesinger, 1997). Soil tends to be shallow compared to the ocean, however. In many places the soil that receives essentially all of the nutrients from the mineralization of organic matter may be only a meter or two deep (or even less sometimes). By comparison, the average depth of the ocean is 3000 m and varies from zero to more than 7000 m (Nybakken, 2001). If we compare oceanic water and terrestrial soil in terms of the sum of their nutrient content over the range of their depth (perhaps a few meters for soil and 3000 m on average for the ocean), we find that they are not so drastically different after all. The major differences are that the nutrients required for primary production on land are very concentrated, close to the sunlight, and can be accessed easily by the primary producers. The nutrients necessary for primary production in the ocean are much more diluted due to the larger volume of oceanic water compared to terrestrial soil, and most of these nutrients are far away from the photic zone. This coupling on land of a concentrated source of nutrients directly adjacent to sunlight allows many terrestrial ecosystems to support higher levels of productivity over a given area than the ocean. Land and sea do eventually meet, though. We must ask, what happens when it rains?

In a Van, Down by the River…

…, especially if the river is large, we see that during a heavy storm the water initially remains mostly clear and the level does not rise. As time passes after the storm the water rises and possibly becomes more turbid. It eventually peaks and then begins to fall nearer to the pre-storm level and degree of turbidity. Exactly when this storm pulse passes through a floodplain depends on the rate at which the water goes through headwater streams and tributaries before reaching that section of river. For example, the Pantanal floodplain in Brazil floods every year due to rains that begin almost six months prior to its flooding (Hamilton et al, 1996)!

As we learned in the movie Finding Nemo, "All drains lead to the ocean." Unfortunately for Nemo, they usually lead to turbines first… This statement is factual, however, to the extent that any substance that makes its way into the earth, air or a drainage system on land will eventually make its way into groundwater or runoff and into the ocean. Many factors affect how fast and how much of any substance reaches the ocean, though. Significant amounts of nitrate and, to a lesser extent, phosphate (orthophosphate has very low solubility in freshwater), can and do leach from the soil into headwater streams, into rivers and eventually are flushed into the ocean. Additionally, depending on land use practices, variable amounts of sediment may enter a river from its watershed (Furnas, 2003; Hamilton and Gehrke, 2005). The more rapidly a river flows, the greater its load and the larger the size of the particles it can transport. Because many terrigenous sediments tend to be such concentrated sources of nitrogen and phosphorus compared to oceanic water, the addition of these sediments to coastal waters can significantly increase the availability of nitrogen and phosphorus in such systems. Therefore, the outwelling of inorganic nitrogen and phosphorus, primarily as nitrate and orthophosphate, and of organic material from rivers and land-based runoff, is a critically important source in the nutrient balance of every coral reef located near land (Furnas, 2003; Furnas and Mitchell, 1997; Furnas et al, 1995). The closer a reef is to the terrestrial environment, the greater the influence that land-based runoff has on that reef. This influence extends not only hundreds of meters from shore but, depending on the magnitude of the input, can influence reef development and nutrient budgets tens and even hundreds of kilometers away. However, the degree of influence drops as the distance from land increases. Oceanic atolls and banks obviously cannot derive nutrient input from land to the same degree that fringing reefs do, because the atolls are not located near land. They represent interesting cases of reef development and will be examined in future installments. They also comprise only a small portion of the world's total reef development. Additionally, groundwater enriched with inorganic nutrients may seep from land through porous frameworks and onto coral reefs (Lapointe and Matzie, 1996; Shinn et al, 1994). This pathway's prevalence and importance, however, is equivocal.

In short, the outwelling of nutrients from land to the coastal ocean, where most coral reefs are located, is a major factor in allowing coral reefs to maintain high rates of primary productivity, as well as large and complex food webs based on this productivity.

Too Much of a Good Thing

Unfortunately, as is the case with any natural system, the input of nutrients to coral reefs from land-based sources, and the balance of these inputs with rates of sequestration and loss can be, and have been, perturbed. In the last several decades the amount of combined nitrogen in the biosphere has doubled due to human activities (Galloway et al, 1995; Galloway et al, 2003). Leibig's research on nutrient limitation and others' research on the processes necessary to fix atmospheric nitrogen into combined forms led to the development of chemical fertilizers. This accounts for approximately 57% of anthropogenic sources of combined nitrogen. The cultivation of N-fixing crops, such as soybeans and alfalfa to increase soil-N and thus soil fertility, accounts for about 29% of this increase. The combustion of fossil fuels accounts for the remaining 14% (Galloway et al, 1995; Galloway et al, 2003). Phosphorus is mined from mineral deposits and usually is added along with nitrogen to agricultural fields and urban landscapes such as lawns and golf courses. It has been estimated that approximately 25% of anthropogenically fixed nitrogen is exported to the ocean in riverine water (Howarth et al, 1996; Conley, 1999). Because of this, most rivers in areas where fertilization for agriculture and other purposes takes place have experienced a 2-20-fold increase in the amount of nitrogen they conduct, and a similar or higher increase in the amount of phosphorus (Caracao and Cole, 1999; Conley, 1999). This has been the root of dramatic problems in many areas in the developed world, and has caused significant eutrophication of coastal waters in some places.

Perhaps the most dramatic example of nutrient over-enrichment's effects on a marine ecosystem is the development and expansion of the "dead zone" in the Gulf of Mexico near the mouth of the Mississippi River. The Mississippi River watershed encompasses a significant portion of the United States, especially its major agricultural region. Fertilization of these agricultural lands to satisfy world grain markets, which demand high quantities for low prices, has led to a dramatic increase in the export of N and P from the watersheds to tributaries of the Mississippi, eventually to the Mississippi itself and finally to the ocean. When these nutrients reach the Gulf of Mexico they support high rates of primary productivity where the rate of production had previously been lower. The phytoplankton in such areas, having been alleviated of a normal state of nutrient-limited production, bloom massively. They, like any organism, die and contribute to the workings of the biological pump. However, the decomposition of organic material by bacteria requires oxygen. Under a scheme of low productivity in the Gulf's surface waters, the biological oxygen demand (BOD) is low, and the water remains oxygenated due to low rates of oxygen consumption by bacteria. As production rises the amount of organic material decomposing rises and so does the BOD.

Every year as farmers throughout the Mississippi River watershed fertilize their fields and as suburbanites fertilize their lawns and support the fertilization of golf courses and other attractions, the amount of nitrate and phosphate flowing into the Gulf increases. As it increases, the rate of production climbs, the BOD follows right behind and an area of hypoxic water unable to support most marine life (e.g., shrimp, fish, crabs and bivalves - all of economic and social importance) grows and grows. This dead zone covers more than 7,000 square miles-an area the size of New Jersey. This is not the only hypoxic area in the ocean caused by cultural eutrophication (indeed, hundreds have been documented), but it is perhaps the most daunting.

Nutrient-loading on Reefs

Similar eutrophication has occurred on some coral reefs. The reefs of Kaneohe Bay off Oahu, Hawaii were severely damaged and nearly destroyed when the outflows of two major sewage pipes were placed within the bay. Within a few years the coverage of live stony corals plummeted while the abundance of macroalgae and certain suspension feeding and bioeroding organisms increased dramatically. This problem was worse near the outflows and least noticeable further away. The cause of the decline in reef health was realized, and the sewage outflows were moved far offshore into deep water. Slowly, over the course of years, the reefs began to recover and are returning to a healthy state.

Uncontrolled release of sewage also severely damaged the reefs around Jamaica. Again, live coral coverage fell dramatically and algal cover and abundance increased. While some of Jamaica's reefs are returning to coral-dominated systems many show no evidence of recovery to their original state, even after many years. In fact, it does not appear that some of the reefs in Jamaica will move in the direction we would consider recovery any time soon, and instead are remaining in what may be considered an alternative stable state for this ecosystem.

A major influence on coastal ecosystems that has allowed the development of many of today's coral reefs is the buffer provided by mangroves and seagrass beds between land and the reef. Mangroves and seagrass beds serve as areas of regeneration for organic material from land, from the reef and from material produced within each system. They utilize inorganic nutrients from land in the production of organic material as well. Additionally, they serve as a source of organic food production for reefs. Perhaps most importantly they trap fine sediments that stress reef animals and can lead to reef decline. Unfortunately, most of these systems have been destroyed throughout the world. We will examine the importance of mangroves and seagrass beds in terms of nutrient cycling in a future article in this series.

Alternatively, other reefs such as those off Western Australia continue substantial growth and development though they experience significant nutrient enrichment from land-based sources. In fact, the nutrient concentrations within the water column on these reefs are often much higher than what has been suggested as a threshold for algal dominance over corals (Lapointe, 1997; Szmant, 2002). Additionally, the Great Barrier Reef (hereinafter, GBR) has developed entirely under a case of increased nutrient input from land due to human activities (Furnas, 2003). The GBR, before the end of the last ice age, was merely a thin fringing reef off the Australian continent. As sea levels rose, the shore moved further west, and the small fringing reef continued to grow into what it is now. During this period, however, aboriginal Australians used fire to clear land in the catchments leading to the GBR lagoon, and in so doing increased the amount of nutrients and sediment transported to the GBR lagoon. With the arrival of Europeans it appears that the transport of sediment to the GBR lagoon has increased, and as the Northern Territory is developed for agriculture the export of nutrients to the GBR lagoon is increasing dramatically (Furnas, 2003). This has caused some concern about the negative impacts on the GBR of such increased nutrient abundance and sedimentation. While some corals seem exceedingly adaptive when it comes to differing regimes of turbidity and the utilization of autotrophy vs. heterotrophy, others seem much less tolerant of increasing turbidity, even if the sediment has the potential to provide the coral with necessary nutrients (Anthony, 2000; Anthony and Fabricius, 2000). On the other hand, Anthony (2006) has just recently published strong evidence suggesting that living offshore in clear water without the potential stress associated with sedimentation may prove to be a trade-off for some corals, compared to living inshore where sedimentation stress is more likely but where nutrients necessary for growth and reproduction may be more easily accessed.

Conclusion

Land represents a major source of the nutrients necessary to fuel coastal marine ecosystems, including coral reefs. We've seen that reefs can both benefit from and be destroyed by land-based runoff. Thus, nutrient enrichment from terrestrial sources cannot be called either beneficial or deleterious without context. The outwelling of nutrients can certainly benefit a reef by allowing it to maintain high levels of primary productivity and the communities that rely on that productivity, but if the magnitude of this outwelling is too great or is combined with other factors (several of which are understood and will be explored in later segments), these nutrients can also cause the eutrophication and destruction of that coral reef and, as in Jamaica, may represent semi-permanent or permanent changes to the ecosystem. Unfortunately, we have no historical basis on which to determine which alternate stable state will persist. Coral reefs use nutrients, though, and they need them in order to function. The land is one place from which reefs acquire the nutrients they need, but it certainly is not the only source that is available or that they utilize. Next month we will explore other sources of the nutrients that coral reefs require to continue functioning as they have for millennia.

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