Colimitation of a freshwater herbivore by sterols and polyunsaturated fatty acids

Abstract

Empirical data providing evidence for a colimitation of an herbivore by two or more essential nutrients are scarce, particularly in regard to biochemical resources. Here, a graphical model is presented, which describes the growth of an herbivore in a system with two potentially limiting resources. To verify this model, life-history experiments were conducted with the herbivore Daphnia magna feeding on the picocyanobacterium Synechococcus elongatus, which was supplemented with increasing amounts of cholesterol either in the presence or the absence of saturating amounts of eicosapentaenoic acid (EPA). For comparison, D. magna was raised on diets containing different proportions of S. elongatus and the cholesterol- and EPA-rich eukaryotic alga Nannochloropsis limnetica. Somatic and population growth of D. magna on a sterol- and EPA-deficient diet was initially constrained by the absence of sterols. With increased sterol availability, a colimitation by EPA became apparent and when the sterol requirements were met, the growth-limiting factor was shifted from a limitation by sterols to a limitation by EPA. These data imply that herbivores are frequently limited by two or more essential nutrients simultaneously. Hence, the concept of colimitation has to be incorporated into models assessing nutrient-limited growth kinetics of herbivores to accurately predict demographic changes and population dynamics.

Figure 1

Hypothesized resource-dependent fitness in a system with two essential dietary resources (a and b) expressed as Monod curves. Fitness is improved with increasing concentrations of resource a in the diet following a saturation curve. If the concentration of resource a in the diet is increased from point 1 to 2, fitness is improved by a (y-axis) in the absence of resource b and by a(b) in the presence of resource b. At a given supply of resource a, e.g. at concentration 1 or 2 on the x-axis, fitness is improved by b₁ or b₂, respectively, when resource b is added to the diet. Thus, fitness is improved by the addition of both resources a and b, which indicates colimitation by these two essential resources (see text for more details).

Figure 2

Growth kinetics of D. magna in response to the dietary sterol content. Somatic and population growth rates on cholesterol- and/or EPA-supplemented S. elongatus are shown in (a) and (b), respectively (filled circles, cholesterol; open circles, cholesterol+EPA). Somatic and population growth rates obtained using different mixtures of S. elongatus and the cholesterol- and EPA-rich N. limnetica are shown in (c) and (d), respectively (plotted against the total dietary sterol content; diamonds, Synechococcus/Nannochloropsis). The regression lines were calculated using a modified Monod model. Data are means of three replicates per treatment; error bars indicate standard deviation (s.d.).

Figure 3

Number of viable offspring produced by D. magna within three reproduction cycles. Animals were fed with S. elongatus supplemented with increasing amounts of cholesterol-containing liposomes either in (a) the absence or (b) in the presence of EPA and with (c) different mixtures of S. elongatus and N. limnetica. Data are means of three replicates per treatment; error bars indicate s.d. Maximum values are indicated by upper case letters; bars labelled with the same letters are not significantly different (Tukey's HSD test, p<0.05 following ANOVA).