Nature: Synergies between large-scale environmental changes, such as climate change1 and increased humic content (brownification)2, will have a considerable impact on future aquatic ecosystems. On the basis of modelling, monitoring and experimental data, we demonstrate that community responses to global change are determined by food-chain length and that the top trophic level, and every second level below, will benefit from climate change, whereas the levels in between will suffer.
Photo: Time-series development (means±1 s.d.) in the control (C, present climate scenario), temperature (T) and brownification (B) treatments, as well as the combined treatment (TB; future scenario) of phytoplankton (μg l−1), zooplankton (No. l−1)…
Hence, phytoplankton, and thereby algal blooms, will benefit from climate change in three-, but not in two-trophic-level systems. Moreover, we show that both phytoplankton (resource) and zooplankton (consumer) advance their spring peak abundances similarly in response to a 3 °C temperature increase; that is, there is no support for a consumer/resource mismatch in a future climate scenario. However, in contrast to other taxa, cyanobacteria—known as toxin-producing nuisance phytoplankton3—benefit from a higher temperature and humic content irrespective of the food-chain composition. Our results are mirrored in natural ecosystems. By mechanistically merging present food-chain theory with large-scale environmental and climate changes, we provide a powerful framework for predicting and understanding future aquatic ecosystems and their provision of ecosystem services and water resources.
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An overwhelming body of scientific evidence of a warming climate leaves little doubt that temperatures will increase by between 2 and 5 °C in many parts of the world during the lifetime of the coming generation1. Such rapid, large-scale changes will probably result in profound effects on ecosystem functioning, as well as food-chain length and interactions in aquatic systems4, 5. However, predicted increases in temperature will not act in isolation, but will interact with trophic dynamics such as food-web structure, as well as with other expressions of environmental change. For example, in recent years there has been a significant increase in the amount of humic substances reaching fresh and coastal marine waters, even though the mechanism behind this brownification is still intensively debated2. Monitoring data show that humic substances have more than doubled during the past 25 years in many systems (Supplementary Fig. S1), which may have important consequences for both ecosystem function6 and the quality of our water resources. Yet despite the recognition that the predicted increases in temperature and humic substances will occur simultaneously, and probably not independently, there is still negligible knowledge on how synergistic effects of these environmental changes will affect aquatic ecosystems. Thus, the present vague understanding of synergism between environmental processes restricts our ability to predict scenarios that may meet the coming generation7.
To understand how our future aquatic ecosystems will function, and what changes we should expect, it is critical to combine expected scenarios and study synergies between them. Modelling studies may here provide some insights and testable hypotheses, especially when the predictions they generate are combined with available monitoring data. Here we use such predictions to create an experimental scenario to quantify the synergistic effects of predicted higher temperatures and brownification. Our experiment followed the natural phenology from winter to the development of phytoplankton and zooplankton in spring, the hatching of fish larvae in late spring and the growth of the juvenile fish in summer.
We predicted that increased temperature and brownification should strongly affect organisms and their interactions, and that, in accordance with the hypothesis of a mismatch between the consumer and resource at elevated temperatures8, zooplankton may be unable to track the predicted earlier peak in phytoplankton food. Moreover, some taxa, such as cyanobacteria, are predicted to benefit more than others from a warmer climate9, but also from reduced light penetration, such as will be the case in systems undergoing brownification. We also reasoned that fish would grow faster in elevated temperature treatments than in ambient controls10, and thereby feed more vigorously on zooplankton. Moreover, higher trophic levels may benefit from the subsidy of terrestrially derived carbon6, suggesting a faster growth of, for example, fish as brownification proceeds. We used 400 l polyethylene containers as experimental enclosures. Five of these were used to mimic today’s situation (controls; C treatment), whereas in another treatment we increased the temperature with 3 °C (ref. 1) above ambient (T treatment). In the brownification (B) treatment we extrapolated the monitoring data from natural systems (Supplementary Fig. S1) by doubling the humic content compared with the controls. The final treatment combined the T and B treatments to represent a likely future scenario of simultaneous climate change and brownification, that is, to mimic a situation predicted to occur at similar nutrient levels within a timescale of about 25–75 yr. Moreover, we aimed at tracking the succession pattern from spring to summer by including the effects of fish hatching and ontogeny. The temperature was controlled by a computerized system measuring the average temperature in the control treatment using temperature sensors that adjusted the temperature in the heated treatment 3 °C above the controls. Each treatment was replicated five times and the nutrient levels, as well as fish abundances, were identical among treatments throughout the study. Samples were taken for zooplankton and phytoplankton analysis from 3 March to 28 July 2009. We used a randomized-block analysis of variance (ANOVA) design normalized for ambient (control) conditions to assess the expected direction and level of change in phytoplankton, cyanobacteria (Microcystis spp.), zooplankton and fish development.
Our future scenario for aquatic systems, with an elevated temperature of 3 °C and a doubling of the humic content, revealed considerable effects on several key variables, showing that they were strongly influenced by food-chain length, that is, context dependent (Fig. 1). During the period before the fish hatched (before 26 May), our systems contained only two trophic levels, phyto- and zooplankton. During this period, the elevated temperature imposed a positive effect on zooplankton abundances, whereas brownification alone (B) had a weak negative effect (Fig. 1). On the contrary, the phytoplankton biomass was negatively affected when compared with the controls in all treatments, suggesting that zooplankton may have reduced their food resource before the fish hatched (Fig. 1). Fish hatching, that is, the introduction of a third trophic level, strongly affected the systems by even shifting the sign of the treatment effects; that is, the phytoplankton biomass was, compared with the controls, positively affected by temperature and brownification in the presence of fish, whereas zooplankton instead experienced a negative effect as fish entered the systems (F>30; p<0.001; Table 1 and Fig. 1). This notion is in line with previous observations that mass-hatching of fish in spring strongly affects zooplankton abundances and community composition11. With respect to zooplankton, the treatment×trophic level interaction term was significant (Table 1), reflecting higher zooplankton abundances before than after fish addition in treatments T and TB, but not in B (Fig. 1). The size of the fish was also positively affected by both temperature and brownification; that is, adding another trophic level shifted the direction (±) of the effect imposed by the treatments throughout the food chain. Hence, we show here that the top trophic level will benefit from predicted future large-scale environmental changes, whereas the level below will suffer. This means that although predicted changes in climate and humic content will have strong effects on our freshwater systems, the direction of the effects is altered by the food-web composition of the specific system. This also suggests that in functionally three-trophic-level systems, phytoplankton and planktivorous fish (every second level) will benefit from climate change, that is, the same taxa that also benefit from eutrophication, further reinforcing a problematic situation with respect to ecosystem services and water quality3.
