Primary producers or consumers? Increasing phytoplankton bacterivory along a gradient of lake warming and browning

Abstract

Eukaryotic phytoplankton form the basis of aquatic food webs and play a key role in the global carbon cycle. Many of these evolutionarily diverse microalgae are also capable of feeding on other microbes, and hence simultaneously act both as primary producers and consumers. The net ecosystem impact of such mixotrophs depends on their nutritional strategy which is likely to alter with environmental change. Many temperate lakes are currently warming at unprecedented rates and are simultaneously increasing in water color (browning) due to increased run‐off of humic substances. We hypothesized that the resulting reduction in light intensity and increased bacterial abundances would favor mixotrophic phytoplankton over obligate autotrophs, while higher temperatures might boost their rates of bacterivory. We tested these hypotheses in a mesocosm experiment simulating a gradient of increasing temperature and water color in temperate shallow lakes as expected to occur over the coming century. Mixotrophs showed a faster increase in abundance under the climate change scenario during spring, when they dominated the phytoplankton community. Furthermore, both bacterial abundances and rates of phytoplankton bacterivory increased under future climate conditions. Bacterivory contributed significantly to phytoplankton resource acquisition under future climate conditions, while remaining negligible throughout most of the season in treatments resembling today's conditions. Hence, to our knowledge, we here provide the first evidence for an increasing importance of bacterivory by phytoplankton in future temperate shallow lakes. Such a change in phytoplankton nutritional strategies will likely impact biogeochemical cycles and highlights the need to conceptually integrate mixotrophy into current ecosystem models.

Browning reduces the availability—but not the transfer—of essential fatty acids in temperate lakes

“…changes in DOM quantity and quality, and thus light conditions and nutrient availability). Cyanobacteria have accessory pigments that allow them to photosynthesise under lower light conditions (Oliver & Ganf, 2000), some species can scavenge Fe from DOM-Fe complexes (Sorichetti et al, 2014(Sorichetti et al, , 2016, and some species can shift from autotrophy to mixotrophy to consume DOM (Poerschmann, Spijkerman, & Langer, 2004;Wilken et al, 2018) in nutrient-poor and dark lake waters. Cyanobacteria have accessory pigments that allow them to photosynthesise under lower light conditions (Oliver & Ganf, 2000), some species can scavenge Fe from DOM-Fe complexes (Sorichetti et al, 2014(Sorichetti et al, , 2016, and some species can shift from autotrophy to mixotrophy to consume DOM (Poerschmann, Spijkerman, & Langer, 2004;Wilken et al, 2018) in nutrient-poor and dark lake waters.…”

“…Cyanobacteria have been found to have competitive advantages in lakes with moderate concentrations of refractory DOM (Sorichetti et al, 2014). Cyanobacteria have accessory pigments that allow them to photosynthesise under lower light conditions (Oliver & Ganf, 2000), some species can scavenge Fe from DOM-Fe complexes (Sorichetti et al, 2014(Sorichetti et al, , 2016, and some species can shift from autotrophy to mixotrophy to consume DOM (Poerschmann, Spijkerman, & Langer, 2004;Wilken et al, 2018) in nutrient-poor and dark lake waters. Irrespective of the strategy, the increase in the cyanobacteria could drive declines in the content of PUFA of seston (Müller-Navarra et al, 2004).…”

Changes in food characteristics reveal indirect effects of lake browning on zooplankton performance

“…Cryptomonads are easily ingestible and digestible microalgae that contain large amounts of poly‐unsaturated fatty acids, which are important for Daphnia growth and especially reproduction (Ravet et al ; Sperfeld and Wacker ). Cryptomonads are mixotrophs that can ingest bacteria, a mode of resource acquisition that is predicted to increase under reduced light availability (Wilken et al ). Both bacterial abundances and rates of phytoplankton bacterivory have been shown to increase under browning scenarios (Wilken et al ), thus increasing the importance of heterotrophic bacteria and mixotrophic microalgae as food for zooplankton (Cole et al ; Hiltunen et al ; Tang et al ).…”

“…HF is a naturally occurring leonardite available as industrially processed, water‐soluble granulated sodium salt of humic acids that contains 43% organic carbon, 82% humic substances, 18% low‐molecular weight compounds, and no polysaccharides (Meinelt et al ). It has been previously used in aquatic mesocosm experiments to simulate browning resulting from tDOC inputs (e.g., Urrutia‐Cordero et al ; Wilken et al ) and in laboratory experiments to assess physiological responses of aquatic organisms (e.g., Meinelt et al ; Steinberg et al , b ; Saebelfeld et al ).…”

Hotspots of biotic compositional change in lakes along vast latitudinal transects in northern Canada

“…In boreal and arctic lakes, the combined effects of warmer temperatures, darker water and changes in nutrient content and quality (composition, bioavailability) linked to changes in terrestrial inputs will affect aquatic biodiversity and ecosystem functioning at various levels (Finstad et al, ; Hayden et al, ). With warming climates, these effects may include alterations in food webs and biogeochemical cycles, with loss of phytoplankton diversity (Urrutia‐Cordero et al, ), shifts to increased mixotrophy in eukaryotic phytoplankton (Wilken et al, ) and decreases in fish biomass production (Tanentzap et al, ; van Dorst et al, ). At the global scale, these changes are also likely to be observed at high altitudes (Moser et al, ).…”