Autotrophic biomass is generally controlled by factors regulating from the bottom up (resources) and from the top down (herbivory). The long-standing debate over which type of factors prevail has been replaced by the view that they interact (Leibold et al. 1997). Recent meta-analyses have shown that both resource supply and grazing significantly affect plant biomass in a range of ecosystems including terrestrial grasslands (Hawkes & Sullivan 2001), phytoplankton (Brett & Goldman 1997) and periphyton (Hillebrand 2002).
Most investigations have used nutrients as the basal resource (Brett & Goldman 1997; Hillebrand 2002), and light has received much less attention in this context (Harley 2002). Light is the only energy source for all photoautotrophic organisms and therefore light limitation may be as important as nutrient limitation for primary production (Hill 1996). Light limitation can be particularly strong for periphyton, the dominant photoautotroph community in streams and lake littorals, due to the absorption of light by the water column, the asymmetric competition for light with phytoplankton and the shading by terrestrial vegetation along the stream or the shoreline.
Therefore, many experimental studies found an increase in periphyton biomass with increasing light supply (Hill 1996), mediated by an increase in photosynthesis and carbon fixation. The relationships between light and both photosynthesis and growth are non-linear. The typical photosynthesis-irradiance (P-I) curve is characterized by increase, saturation and inhibition phases (Fig. 1) although for periphyton, photo-inhibition seems to be rare (Hill 1996). In the absence of other growth constraints, higher photosynthesis will increase plant biomass, which can best be described by a saturation function (Fig. 1). It can therefore be presumed that at high light conditions more algal biomass is available to herbivores (Fig. 1).
Light also affects relative nutrient content and the representation of different growth forms in the community (Fig. 1). High light conditions often relate to high C : nutrient ratios in the algae, which then represent poorer food for the herbivores (Urabe et al. 2002; Hillebrand et al. 2004). This lowered nutritional quality can be expressed as changes within species (increased cellular C : nutrient ratios) as well as by changes in species composition, because growth forms favoured at high light contain more structural carbon (Fig. 1). Light effects on species composition are often related to different growth forms (Steinman et al. 1992), as, with increasing algal biomass, small and prostrate algal species are heavily shaded, whereas erect growth forms are superior competitors for light. The filamentous and chain-forming algal species that therefore tend to dominate at high light are often more prone to grazing (Steinman et al. 1992; Hillebrand et al. 2000), as the dominant herbivores (snails, insect larvae) are large compared with their algal prey and tend to graze preferentially on the upper layers of the periphyton community (Steinman 1996). However, single algal species may grow into a size refuge (Hart 1992), which can reduce grazer effectiveness at greatest prey height. If such inedible prey gains dominance in the plant assemblage, grazer effects decrease at greatest plant height (see non-linear response in Fig. 1).
From a consumer perspective, increasing light thus results in more algal biomass, which, moreover, is dominated by easily ingestible growth forms, although these have poor nutritional quality. By contrast, nutrient enrichment tends to increase plant biomass and quality and there are therefore strongly contrasting ways in which nutrient and light effects can be propagated to the consumer level. The effects of changes in nutritional quality may also depend on the ability of the grazers to choose food. High light may result in less algal biomass consumed if grazers selectively avoid food of lower quality, or in more biomass consumed if grazers increase their intake to compensate for the low quality (Cruz-Rivera & Hay 2000).
Patterns described for grazer–periphyton interactions may also be relevant in other plant–herbivore interactions. Grasslands grazed by large mammals such as ungulates reveal a similar size ratio between consumer and prey. Consequently, grazer presence also affects plant biomass and plant size structure in these ecosystems (McNaughton 1984). Despite several differences in community functioning between periphyton and grasslands (e.g. the importance of below-ground processes in terrestrial communities), results on light vs. consumer control of algal biomass may be important beyond the community analysed.
To test for the relative effects of light and consumer presence on algal biomass, I conducted a meta-analysis of experiments that manipulated light supply and grazer presence in a factorial design and monitored the effect on periphyton biomass. This study therefore represents a general test for significant interactions between light supply and grazer presence in determining algal biomass. Comparison with a previous analysis of nutrient vs. grazer control (Hillebrand 2002), further enables evaluation of the relative importance of light and nutrients as basal resources and the identification of abiotic and biotic factors regulating the relative role of light and consumer effects on periphyton biomass.
Following the recommendations of Lajeunesse & Forbes (2003), two different types of effect sizes were analysed. First, a recently proposed factorial meta-analysis (Gurevitch et al. 2000) on the standardized difference (measured as Hedges’d) between the manipulated factor and the control was used to compare the overall effect sizes of light enhancement and grazer removal and to test for significant interactions. Secondly, the proportional effects (measured as log response ratio, LR) of light enhancement and grazer removal were calculated for either level of the other variable. These analyses were used to test the following hypotheses.
- 1Grazer removal and light enhancement both have significant positive effects on algal biomass.
- 2The interaction between grazer and light manipulation is significant, i.e. light enhancement increases grazer effect size, whereas grazer presence reduces light effects.
- 3The interaction between grazer and light is stronger than that previously determined (Hillebrand 2002) for the interaction between grazer and nutrient manipulations.
- 4Light effects are stronger in situations of high nutrient supply or high algal biomass.
- 5Grazing effects are stronger at high algal biomass and/or high grazer biomass.
- 6The effect sizes depend on characteristics of the experimental design such as (a) experiment type, (b) degree of light enhancement, (c) manipulated grazer group, and (d) duration of the experiment.