The biogeochemical cycling of phosphorus in marine systems
Introduction
Phosphorus (P) is an essential nutrient utilized by all organisms for energy transport and growth. Yet, little is known about the role P plays in the production and distribution of plankton in the world's ocean. One of the major reasons for this relative lack of understanding is the dominant, but slowly changing view that P only limits production over geologically long time scales in marine systems (>1000 years, Hecky and Kilham, 1988, Codispoti, 1989). The theory behind this P limitation is relatively simple. Over prolonged time scales, phytoplankton N requirements can be met through the process of N2-fixation McCarthy and Carpenter, 1983, Tyrell, 1999. This hypothesis assumes that the standing stock of N2-fixing organisms will increase as the N:P ratio in the ocean decreases. Since the reservoir of N2 in the atmosphere is so large, N2-fixing organisms would eventually be limited by other nutrients. Given the long residence time of P in the ocean compared to other potentially bio-limiting nutrients and trace elements, such as silica and iron, P is often regarded as the ‘ultimate’ limiting nutrient over long time scales Redfield, 1958, Van Cappellen and Ingall, 1994, Van Cappellen and Ingall, 1996, Tyrell, 1999.
Unfortunately, this common perception has resulted in the study of P to be focused on the identification and balance of oceanic P sources and sinks Froelich et al., 1982, Ruttenberg, 1993, Howarth et al., 1995, Follmi, 1996, Delaney, 1998. The intermediate steps, i.e. the transformation processes of P within the water column, have been relatively ignored. The idea that P is unimportant in limiting marine phytoplankton growth over short time scales stems from the work of Redfield et al. (1963). In their study, Redfield et al. (1963) noted that the ratio of C:N:P within particulate organic matter is ubiquitous at 106:16:1. Hence, they hypothesized that phytoplankton required these elements in the above ratios for balanced growth. Since then, the Redfield ratio has been used to evaluate nutrient limitation in various oceanic regimes Ryther and Dunstan, 1971, Boynton et al., 1982, Downing, 1997. Global oceanic surveys of dissolved inorganic nutrients (GEOSECS, TTO) discovered that when plotting inorganic N versus inorganic P, N concentrations tended to decrease to zero first, leaving a small, but detectable residual P concentration (e.g. Fig. 1). These results led others to suggest that over short time scales, N was the most important nutrient in limiting phytoplankton growth in the open ocean Thomas, 1966, Ryther and Dunstan, 1971, Goldman et al., 1979, Codispoti, 1989.
Unfortunately, this presumption of a single limiting nutrient, i.e. N, has many inherent weaknesses. Perhaps the most obvious is related to the plots of inorganic N and P concentrations, which completely ignores the potential role of organic nutrients and trace metals in plankton production. Although inorganic N and P are the most readily available forms of nutrients to plankton, several studies have shown that organic nutrients can be utilized by phytoplankton as well Chu, 1946, Kuentzler, 1965, Cembella et al., 1984a, Berman et al., 1991, Van Boekel, 1991, Bronk et al., 1994. Jackson and Williams (1985) plotted total dissolved P (TDP) versus total dissolved N (TDN) in the North Pacific and found that TDP is exhausted just prior to TDN (e.g. Fig. 2). They suggested, using the above assumptions, that P may limit phytoplankton production. However, this could only be inferred as neither nutrient actually decreases to zero concentrations. Nonetheless, that the nutrient depleted surface waters have a TDN to TDP ratio similar to that of Redfield, implies that both DOP and DON are important sources of N and P in the upper water column. Since then, evidence that P, rather than N, may limit community production has been found in regimes ranging from restricted Smith and Atkinson, 1984, Granéli et al., 1990, Krom et al., 1991 and shallow-marine areas Fourqurean et al., 1992, MacRae et al., 1994 to the open ocean, oligotrophic sites of the North Atlantic and North Pacific Cotner et al., 1997, Karl et al., 1997.
Another discrepancy that is often overlooked when discussing nutrient limitation is the difference between standing stocks of specific nutrients and the flux of nutrients between various dissolved and particulate pools. Depending on the pool size, nutrients which have long turnover times suggest either a lack of bioavailability or need. Short turnover times, on the other hand, suggest that a particular nutrient is both bioavailable and necessary for growth and production. This information, coupled with new molecular methods for evaluating the in situ nutrient status of plankton can provide important insight into the controls of nutrient limitation (Scanlan and Wilson, 1999). Regardless, measuring the concentration of a nutrient alone, does not provide any insight into these processes.
In recent years, the debate of N versus P limitation has also come to include the role of trace elements, such as iron, and other nutrients, such as silica Howarth et al., 1988a, Howarth et al., 1988b, Martin et al., 1994, Hutchins and Bruland, 1998, Dugdale and Wilkerson, 1998, Cavender-Bares et al., 1998. Many studies have shown the potential growth limiting effects of these other elements in various environments. In fact, Fe may limit the rate of N2-fixation and the growth of N2-fixing organisms Falkowski, 1997, Karl et al., 1997. If true, this would have long standing implications for the ‘ultimate’ control of phytoplankton growth over long time scales.
Nonetheless, understanding the water column biogeochemical cycling of all nutrients and trace metals is essential for elucidating the current and future effects of both natural and anthropogenically induced changes in nutrient composition on the plankton productivity and speciation of the world's oceans. Areas which would most likely suffer the greatest impact of man's activities are along the cost, simply due to its proximity to the Earth's major population centers. A recent controversial study by Tyrell (1999) suggests that because P limits production over long time scales, it is not necessary to restrict the inputs of other nutrients, such as N, into coastal ecosystems. This view is too simplistic and does not take into account the wide variety of organisms with different strengths and weaknesses that exist in the marine realm. In fact, increased and/or changing nutrient input ratios have been clearly shown to reduce food web diversity, alter phytoplankton composition and even increase in the intensity and frequency of toxic dinoflagellate blooms, or red tides (e.g., Nixon, 1993).
The open ocean is also not immune from man's activities due to large-scale atmospheric transport and deposition of anthropogenic emissions. For example, inorganic N and P surface ocean concentrations were examined in detail by Fanning (1989). He found that inorganic N concentrations were below detection (<0.2 to 0.37 μM) and inorganic P at or above detection (>0.015 μM) in most areas of the world's oceans. However, he also found that the reverse circumstance occurred in surface waters of the North Pacific and North Atlantic, areas downwind of the most populated and urbanized regions of eastern Asia and North America. Paerl (1993) has further confirmed the potentially large source of N to marine environments via acid rain. More recently, Migon and Sandroni (1999) determined that atmospheric anthropogenic P inputs slightly increased the annual new production within the western Mediterranean basin. Given that N has a much larger natural and anthropogenic atmospheric source than P, an increase in inputs could lead to phosphorus limitation of surface waters over time Fanning, 1989, Paerl, 1993, Carpenter and Romans, 1991, Karl et al., 1997. In this study, a much needed review of the oceanic P cycle is given. Special consideration is given to the processes that effect the distribution and cycling of P within the upper ocean. Only brief synopses of P sources and sinks are discussed.
Section snippets
The history of phosphorus
P is the eleventh most abundant element in the Earth's crust. It was first discovered in 1669 by the German alchemist, Hennig Brand, who noted that a white solid could be obtained that not only glowed in the dark, but also spontaneously ignited in air. Hence, its name P, literally means ‘light bearing’ and is derived from the Greek words ‘Phos’ (light) and ‘Phorus’ (bearing). The importance of P as a nutrient was not realized until the mid-1800s. Shortly thereafter, a technique was developed
Riverine
Phosphorus enters the oceans predominantly through rivers (Fig. 3). Continental weathering of crustal materials, which contain on average 0.1% P2O4, is the major source of riverine P. It is difficult to determine the natural riverine flux of P due to the temporal variability in riverine water mass fluxes and anthropogenic effects due to deforestation and the use of fertilizers. Attempts to estimate these inputs have been mostly based on water flux and concentration measurements from areas which
Methods of measurement
Before one can discuss the cycling of P within the oceans, it is first necessary to understand the methodologies by which P concentrations are measured. Currently, the distribution of P in aquatic systems is most often defined analytically. This is one of the biggest hurdles in elucidating P composition and cycling in marine systems.
Conclusions and future outlook
It is clear that elucidating the cycling of all nutrients in marine systems is extremely important if we are to understand current controls on primary production and particulate carbon export in the world's oceans. The intensity of upper ocean P cycling, in particular, can have a direct impact on the magnitude of particulate matter exported from the euphotic zone to underlying sediments. Hence, long-term changes in P cycling will effect the residence time of P over geological time scales.
The
Acknowledgements
I wish to thank Drs. Karin Björkman, Dave Karl, and Bryan Benitez-Nelson for their helpful comments pertaining to the manuscript. This work was supported by the SOEST Young Investigator Award and NOAA/UCAR Postdoctoral Fellow in Global Change. SOEST Contribution number 5246.
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