Rationalizing Elemental Ratios in Unicellular Algae

In 1934, the year Harold Urey was awarded a Nobel prize in chemistry for the discovery of deuterium, Alfred Redfield (Fig. 1), a 44-year-old animal physiologist at Harvard University, proposed that marine plankton have relatively constrained elemental ratios (Redfield 1934). The so-called Redfield ratios of 106 C: 16 N: 1 P (by atoms) were subsequently embraced by many biological oceanographers and geochemists as canonical values, comparable to such physical constants as Avogadro’s number or the speed of light in a vacuum. Although the wholesale adoption of a simple chemical analysis by a large group of otherwise highly self-critical scientists was certainly not Redfield’s intention, his fundamental interpretation of the causes and consequences of constant elemental ratios in the ocean has become a key foundation for biogeochemistry. Nonetheless, despite the passage of almost 70 years since his landmark paper, there is no biological understanding of elemental ratios. Although Redfield ratios per se have become an accepted empirical observation, their deeper meaning remains obscure. Here I examine how Redfield and his famous elemental ratios evolved, and present some analyses about their meaning. Redfield’s interest in elemental ratios was stimulated by the earlier work of the British marine chemist, H. W. Harvey (Harvey 1926). Redfield noted that the ratio of dissolved fixed inorganic nitrogen (nitrate) to phosphate in seawater was remarkably constant regardless of the absolute concentration of the molecules, and was similar (but not exactly equal) to the bulk N/P ratio of what he referred to simply as plankton. The original seawater analyses of Redfield were not corrected for salt; this was rectified in an article by Cooper in 1938. In 1958, Redfield used the chemical analyses for the (average) plankton provided by Richard Fleming in an obscure (and unreviewed) publication from 1940 (Fleming 1940) to (re)derive the famous ratio (Redfield 1958). The term plankton was originally used by Fleming in the broadest context, and included both phytoplankton 3 and zooplankton (but not bacteria or picoplankton, which at the time were not sampled). As time went on, more and more chemical analyses of seawater and both marine and lacustrine plankton (mostly phytoplankton were obtained) (Vinogradov 1953, Haug and Myklestad 1973, Copin-Montegut and CopinMontegut 1983, Hecky et al. 1993), and the basic premise that (autotrophic) organisms utilize nitrogen and phosphorus in the proportion in which they are found in seawater, and return these elements back to seawater upon their death and decomposition, was largely embraced by geochemists (Sverdrup et al. 1942, Broecker and Peng 1982, Anderson and Sarmiento 1994). The elemental composition of seawater was therefore thought to represent the steady-state ratio of the remineralized (i.e. oxidized) organic matter. A summary of the results of chemical analyses, replicated by several workers, is provided (Table 1). The concept of a constant elemental composition for plankton and seawater is extremely convenient for modeling ocean biogeochemistry and marine planktonic processes (Broecker and Peng 1982, Pahlow and Riebesell 2000), but the conceptual understanding of the biological basis for variability in elemental ratios is lacking. Hence, there are numerous papers in the literature showing that the bulk elemental composition and/or nutrient assimilation of various phytoplankton assemblages differ from the Redfield ratio (e.g. Menzel and Ryther 1964, Sambrotto et al. 1993). Variability in the elemental composition of plankton was certainly recognized by Fleming, who wrote (as a coauthor of The Oceans , Sverdrup et al. 1942), “The ratios given above hold very well for the nitrate and phosphate in ocean waters, but since they represent the net effect of biological activity, marked deviations from the ratios may be found in individual types of organisms.” Redfield’s fundamental insight into the chemistry of aquatic ecosystems was not dependent on a specific elemental ratio per se, but rather was related to the coupling between the chemical composition of plankton (specifically the N/P ratio) and that of seawater. Key index words: Gaia hypothesis, iron, nitrogen fixation, oceanic productivity, Redfield ratio