Warming shifts top-down and bottom-up control of pond food web structure and function

Abstract

The effects of global and local environmental changes are transmitted through networks of interacting organisms to shape the structure of communities and the dynamics of ecosystems. We tested the impact of elevated temperature on the top-down and bottom-up forces structuring experimental freshwater pond food webs in western Canada over 16 months. Experimental warming was crossed with treatments manipulating the presence of planktivorous fish and eutrophication through enhanced nutrient supply. We found that higher temperatures produced top-heavy food webs with lower biomass of benthic and pelagic producers, equivalent biomass of zooplankton, zoobenthos and pelagic bacteria, and more pelagic viruses. Eutrophication increased the biomass of all organisms studied, while fish had cascading positive effects on periphyton, phytoplankton and bacteria, and reduced biomass of invertebrates. Surprisingly, virus biomass was reduced in the presence of fish, suggesting the possibility for complex mechanisms of top-down control of the lytic cycle. Warming reduced the effects of eutrophication on periphyton, and magnified the already strong effects of fish on phytoplankton and bacteria. Warming, fish and nutrients all increased whole-system rates of net production despite their distinct impacts on the distribution of biomass between producers and consumers, plankton and benthos, and microbes and macrobes. Our results indicate that warming exerts a host of indirect effects on aquatic food webs mediated through shifts in the magnitudes of top-down and bottom-up forcing.

Figure 1.

Effects of the treatments on the six functional groups sampled. Each point indicates the parameter estimate (±1 s.e.) for the treatment or interaction term in the linear mixed effects model. A positive value indicates that biomass of that group increased in a particular treatment and a negative value indicates the opposite. Each model is based on the log_e-transformed biomass (in g C m⁻³ for pelagic organisms and g C m⁻² for benthos), with individual mesocosm treated as a random effect. The treatments are: W, warming; N, nutrients; F, fish predation. The symbols show the significance of the parameter estimates as follows: *p < 0.05, **p < 0.01 and ***p < 0.001.

Figure 2.

The biomass of the six food web components studied in our experiment under (a) fish predation, (b) warming and (c) nutrient treatments. Each of the four pelagic groups is measured in log_e g C m⁻³ and the benthic invertebrates and periphyton in log_e g C m⁻². We plotted the average biomass for two time periods when all groups of organisms were sampled within the same four-week period. Solid black lines are the average biomass for each of the two treatment levels representing the main effects and the coloured bars are±1 s.e.

Figure 3.

Food web diagrams showing the interaction between the fish and warming treatments, and the stronger effects of fish in pelagic than benthic habitats. The solid arrows represent direct effects of fish on zooplankton and benthic invertebrates, the dashed arrows indirect effects on primary producers and micro-organisms. The black arrows show measured direct or indirect effects, whereas the grey arrows represent unmeasured interactions. ‘Detritus’ is the decomposition of leaf litter in the tanks as reported in Greig et al. [33]. Arrow thickness is proportional to the magnitude of biomass change. The values shown indicate the log_e of the ratio of biomass in the tanks with and without fish, averaged across sampling dates (with 1 s.e. in parentheses), and asterisks indicate values that were significantly affected by warming (the interactions shown in figure 1). Phytoplankton responded more strongly to fish than periphyton or leaf litter decomposition, even though the direct effect of fish on zooplankton was similar to that on benthic invertebrates. (a) Unwarmed and (b) warmed food webs.

Figure 4.

Effects of the main treatments on net ecosystem production (NEP). The y-axis shows the parameter estimates (±1 s.e.) from a linear mixed effects model with time as a random effect nested within tank. The summary ANOVA table is shown in table 1. (a) Also shows the mean daily air temperature throughout the experiment. (a) Warming, (b) nutrients and (c) fish.