Control of microbial communities by the macrofauna: a sensitive interaction in the context of extreme summer temperatures?

Abstract

Climate models predict an increasing frequency of extremely hot summer events in the northern hemisphere for the near future. We hypothesised that microbial grazing by the metazoan macrofauna is an interaction that becomes unbalanced at high temperatures due to the different development of the grazing rates of the metazoans and the growth rates of the microbial community with increasing temperature. In order to test this hypothesis, we performed grazing experiments in which we measured the impact of increasing temperatures on the development of the grazing rates of riverine mussels in relation to the growth rates of a unicellular prey community (a natural heterotrophic flagellate community from a large river). In a first experimental series using Corbicula fluminea as a grazer and under the addition of a carbon source (yeast extract), the increase of the prey's growth rates was considerably stronger than that of the predator's grazing rates when temperatures were increased from 19 to over 25 degrees C. This was also the outcome when the mussels had been acclimatized to warm temperatures. Hereafter, specific experiments with natural river water at temperatures of 25 and 30 degrees C were performed. Again, a strong decrease of the mussels' grazing rates in relation to the flagellate growth rates with increasing temperature occurred for two mussel species (C. fluminea and Dreissena polymorpha). When performing the same experiment using a benthic microbial predator community (biofilms dominated by ciliates) instead of the benthic mussels, an increase of the grazing rates relative to the growth rates with temperature could be observed. Our data suggest that predator-prey interactions (between metazoans and microbes) that are balanced at moderate temperatures could become unbalanced at high temperatures. This could have significant effects on the structure and function of microbial communities in light of the predicted increasing frequency of summer heat waves.

Effects of temperature increase on the grazing of planktonic bacteria by biofilm-dwelling consumers

“…Feeding rate in particular usually shows exponential or rectilinear dependencies on temperature in metazoans (e.g. Viergutz et al 2007). In this study, we recorded linear relationships between temperature and community grazing rates.…”

“…Gillooly et al 2001, Savage et al 2004, growth rate (e.g. Müller & Geller 1993 and feeding rate (Montagnes et al 2001, Viergutz et al 2007). An increase in temperature generally has a stimulating effect on biological rates within a species-specific optimal temperature range.…”

“…Sanford 1999). Recent studies have identified benthopelagic coupling as a leverage point through which temperature changes can generate rapid changes in the composition of planktonic communities due to differential development of the grazing rates of benthic macrograzers (such as bivalves) and differential growth of planktonic communities due to differential development between the grazing rates of benthic macrograzers (such as bivalves) and the growth rates of their planktonic prey (Viergutz et al 2007, Weitere et al 2008. However, it is still unknown whether or not community grazing rates of biofilm-dwelling grazers respond in a similar manner to warming as macrofaunal grazing rates.…”

“…It seems likely that microbial biofilm communities can respond more quickly to changing temperatures because they contain a large pool of grazers with different thermal optima and can thus rapidly shift in their relative importance (due to their short generation times and high densities) with changes in abiotic and/or biotic conditions. Such community shifts might also enable biofilm communities to keep high grazing rates at high temperatures (> 25°C) at which macrofaunal grazing rates are negatively affected (Viergutz et al 2007). …”

The response of temperate aquatic ecosystems to global warming: novel insights from a multidisciplinary project

“…Mesocosm experiments by Viergutz et al (2007) showed that summer heat waves enhance nanoplankton (\20 lm) abundances due to differential temperature responses of the plankton growth rates and the grazing rates by filter feeders. The increased abundance of nanoplankton leads to an increased grazing pressure on bacteria (usually \2 lm) and thus to shifts in plankton size structure (Weitere et al 2008).…”