Some thoughts on the concept of colimitation: Three definitions and the importance of bioavailability

We discuss the concept of colimitation of primary productivity in aquatic environments, with an emphasis on reconciling this concept with recent advances in marine bioinorganic chemistry. Colimitations are divided into three categories on the basis of their mathematical formulations and visualizations: type I, independent nutrient colimitation (e.g., N and P); type II, biochemical substitution colimitation (e.g., Co and Zn); and type III, biochemically dependent colimitation (e.g., Zn and C), where the ability to acquire one nutrient is dependent upon sufficient supply of another. The potential for colimitation occurring in the marine environment and the critical importance of understanding nutrient bioavailability are discussed. The notion of simultaneous limitation by multiple elements, or colimitation, is an important yet often misunderstood concept. Our aim in this manuscript is to clarify and define the types of colimitation, review and discuss their mathematical descriptions, and present threedimensional examples to promote a visual understanding. There is a particular emphasis on the role of trace metals in colimitation, as well as the potential importance of organic complexation to nutrient bioavailability and colimitation in marine waters. These discussions are necessitated in part by the recent advances in marine bioinorganic chemistry, where it is now believed that limitation by certain trace metals could reverberate through coupled biogeochemical systems by hindering the biosynthesis of key metalloenzymes (Morel et al. 2003). The water column of the marine environment contains micronutrients and macronutrients that nourish the growth of autotrophic life. Much has been written about the nutrition of oceanic primary production (e.g., Redfield et al. 1963; Droop 1973; Moore et al. 2004). A useful recurring theme in the marine literature is Liebig’s law of the minimum (de Baar 1994). This law was the 33rd of 50 principles of agricultural chemistry: ‘‘When a given piece of land contains a certain amount of all the mineral constituents in equal quantity in an available form, it becomes barren for any one kind of plant when, by a series of crops, one only of these constituents—as for example soluble silica—has been so far removed, that the remaining quantity is no longer sufficient for a crop.’’ (Liebig 1855 as cited in de Baar 1994). While Liebig’s law exerts itself on biological systems by controlling the overall yield of biomass, an alternate concept of limitation is rate limitation (also known as Blackman limitation) where growth rate is reduced rather than yield. These can be interrelated concepts; for example, both types of limitation have been clearly observed in the metal limitation experiments (e.g., Saito and Goepfert 2008), where the gradual replenishment of free metals in solution from the metalbuffered media operates as a chemical chemostat, inducing growth rate limitation. Once significant biomass is achieved in the culture relative to the amount of cobalt and zinc needed for nutrition, yield is limited and the buffer is effectively ‘‘blown’’ (either by kinetics of the back reaction of the metal–buffer complexes, or by actual depletion of the total metal). Liebig’s law implies that there is a single limiting nutrient. But the concept of limitation (either Liebig or Blackman) is frequently expanded to more than one nutrient, often by invoking the term ‘‘colimitation.’’ The surface oceans are particularly prone to colimitation because of the simultaneous scarcity of many nutrients. In particular, improvements in trace metal analytical methods that occurred at the end of the last century have allowed researchers to demonstrate the potential for 1 Corresponding author ([email protected]).