Interplay between Energy Limitation and Nutritional Deficiency: Empirical Data and Food Web Models

Abstract

Food quality may play an important role in consumer population dynamics. The frequently large differences in elemental and biochemical composition observed between autotrophs and their grazers suggest that food quality may be of particular importance for herbivores. Under nutrient-depleted conditions the carbon-to-nutrient ratios of autotrophs can increase to such an extent that consumers become nutrient rather than energy limited. Estimating the importance of this effect in situ in pelagic food webs is complicated by the omnivory of many consumers and by rapid nutrient recycling. Isolated predator–prey studies inadequately represent this interaction; instead, an ecosystem perspective is required. We used seven years of data from large, deep Lake Constance to develop seasonally resolved flux models of the pelagic food web and analyzed the balance between energy and nutrient constraints. The carbon (C) and phosphorus (P) flows were simultaneously quantified and balanced. C represented food quantity/energy. P was taken as a surrogate of food quality, because algal C:P ratios exceeded the threshold above which P limitation of herbivores is predicted by stoichiometric theory throughout summer and autumn. Primary production exceeded bacterial C production by a factor of 3, but autotrophs and bacteria took up approximately equal amounts of P during summer and autumn. As a consequence, the C and P supplies of suspension-feeding zooplankton were decoupled: Consumer C demands were largely met by phytoplankton whereas P was mostly obtained from bacteria and their protist predators. The degree of consumer P deficiency varied according to supplementation of their algal diet with P-enriched bacteria or bacterivores. This favored the occurrence of omnivores, i.e., organisms that minimized P deficiencies at the cost of enhanced energy limitation. In contrast with previous perceptions, P remineralization during P-depleted summer conditions was dominated by bacterivorous flagellates, carnivorous crustaceans, and fish, which fed on prey with an elemental composition similar to their own, whereas herbivores contributed only 30% of P cycling despite their large biomass and C production. Our results suggested a co-limitation of predominantly herbivorous consumers by C and P and a mutual dependence of the two types of deficiency at the individual and system level. This pattern is not specific to pelagic systems but appears to be applicable across ecosystem types.