Differential grazer-mediated effects of high summer temperatures on pico- and nanoplankton communities

We investigated the role of a macrograzer (the filter feeding mussel Dreissena polymorpha) in mediating effects of high summer temperatures on the dominant components of natural river plankton (i.e., bacteria, algae, and heterotrophic flagellates) in flow channel experiments. Effects of adaptation (by comparing mussels from a southern and a northern population) and thermal acclimation of the mussels were considered. Both heterotrophic flagellates and algae are released from grazing pressure and increase in abundance at temperatures above 20uC. Bacterial abundance, however, decreased with increasing temperature, suggesting a trophic cascade (mussel–flagellates–bacteria) that is altered by the temperature response of the mussel ingestion rate. Warm acclimation of the mussels did not change the outcome of the experiments. The dreissenids from the southern population showed a significantly higher ingestion rate than those from the northern population only in July. The general pattern (i.e., decreasing ingestion rates at high temperatures) was found in both populations. Microbial communities controlled by macrofauna can experience substantial changes in warm summers because of differential development of direct and indirect grazing effects with increasing temperature. Currently we are facing a temperature increase caused by anthropogenic emission of greenhouse gases. In the most probable scenarios, the average global surface temperature is projected to increase by between 1.7uC and 4.0uC during the 21st century (IPCC 2007). Temperature changes can even be greater on a local or temporal scale. Examples are European summer heat waves, which are predicted to occur in high frequencies in the near future (Schär et al. 2004). The temperature increase already affects organisms and ecosystems on different levels, e.g., by influencing the feeding rates of organisms and the strength of species interactions (e.g., Sanford 1999) or by leading to shifts in the geographic ranges of organisms (for review see Parmesan 2006). It is important that ecologists are able to understand and predict the ecological consequences of temperature increases. To do so, it is essential to identify processes that (1) contribute significantly to ecosystem functioning and (2) are sensitive toward small temperature changes (cf. Sanford 1999). The grazing of plankton by benthic filter-feeders, particularly mussels, in rivers, shallow lakes, and coastal areas is such an interaction. It can have a considerable influence on ecosystem functions since it has a strong effect on the composition of the plankton and acts as a link through which a large part of primary and secondary plankton production is imported into the benthos (Welker and Walz 1998; Jack and Thorp 2000; Weitere and Arndt 2002). Both the grazing rates (Walz 1978; Aldridge et al. 1995; Lei et al. 1996) as well as the growth rates of the planktonic organisms (e.g., Montagnes et al. 2003) depend strongly upon temperature. However, the two rates can show different responses toward warming. We have recently shown that the grazing rate of the invasive freshwater mussel Corbicula fluminea on planktonic heterotrophic flagellates (HF) decreases with high summer temperatures relative to the growth rate of its prey, leading to a rapid increase in HF abundance at high temperatures due to the grazing release (Viergutz et al. 2007). The differential development of the macrofaunal grazing rates and the growth rates of unicellular organisms is therefore one way through which temperature changes can alter the structure of microbial communities. Benthic filter-feeding communities among the macrofauna are often dominated by relatively few species; this is especially the case when they are dominated by invasive species and when the increase of the invaders’ abundance is correlated with dramatic decreases in the abundance of native competitors, as has been demonstrated for the zebra mussel Dreissena polymorpha (Pallas, 1771) (Ricciardi et al. 1998; Schloesser et al. 2006). Indigenous to the PontoCaspian area, this dominant and efficient benthic filterfeeder has invaded large parts of Europe and North America, where it is now widespread in various freshand brackish water environments (Reid and Orlova 2002). It has been shown that the invasion of D. polymorpha can lead to a strong restructuring of aquatic communities (Caraco et al. 1997; Findlay et al. 1998; Caraco et al. 2006). The success of many invasive species such as D. polymorpha is at least partly attributed to environmental changes (Dukes and Mooney 1999; Stachowicz et al. 2002). However, the secondary effect of environmental warming on communities dominated by the invader is as yet poorly explored. Here we analyzed the consequences of temperaturedriven changes in the grazing pressure of D. polymorpha on the major components of the riverine planktonic food web, i.e., bacteria, algae, and HF. These three groups dominate 1 Corresponding author ([email protected]). Acknowledgments We thank Jost Borcherding for sampling Dreissena polymorpha from the Rhine and Frederic Bartlett for helpful comments. This study is part of the priority program ‘‘Impact of climate variability on aquatic ecosystems (AQUASHIFT)’’ funded by the German Research Foundation (DFG). Limnol. Oceanogr., 53(2), 2008, 477–486 E 2008, by the American Society of Limnology and Oceanography, Inc.