An evidence-based framework for predicting the impact of differing autotroph-heterotroph thermal sensitivities on consumer–prey dynamics

Abstract

Increased temperature accelerates vital rates, influencing microbial population and wider ecosystem dynamics, for example, the predicted increases in cyanobacterial blooms associated with global warming. However, heterotrophic and mixotrophic protists, which are dominant grazers of microalgae, may be more thermally sensitive than autotrophs, and thus prey could be suppressed as temperature rises. Theoretical and meta-analyses have begun to address this issue, but an appropriate framework linking experimental data with theory is lacking. Using ecophysiological data to develop a novel model structure, we provide the first validation of this thermal sensitivity hypothesis: increased temperature improves the consumer's ability to control the autotrophic prey. Specifically, the model accounts for temperature effects on auto- and mixotrophs and ingestion, growth and mortality rates, using an ecologically and economically important system (cyanobacteria grazed by a mixotrophic flagellate). Once established, we show the model to be a good predictor of temperature impacts on consumer–prey dynamics by comparing simulations with microcosm observations. Then, through simulations, we indicate our conclusions remain valid, even with large changes in bottom-up factors (prey growth and carrying capacity). In conclusion, we show that rising temperature could, counterintuitively, reduce the propensity for microalgal blooms to occur and, critically, provide a novel model framework for needed, continued assessment.

Predicting temperature impacts on aquatic productivity: Questioning the metabolic theory of ecology's “canonical” activation energies

“…Most studies, including this one, that have assessed thermal responses for implementation in population models have focused on resource‐replete measurements (i.e., maximal rates), though nutrient and light limitation is more likely the rule in natural ecosystems. There is strong evidence for interaction between resources and temperature on both phytoplankton and protozoa (e.g., Edwards et al ; Yang et al ; Thomas et al ; Marañón et al ), and there are good indications that RUBISCO is not a rate‐limiting enzyme under low light or nutrient levels (Raines ; Flynn and Raven ). Ultimately, we encourage the integration of such interactions into large‐scale models, as currently there are insufficient data to provide appropriate general responses.…”

“…To fully appreciate the impact of these protozoan‐algal interactions, at local and ecosystem levels, models must then incorporate predator‐prey dynamics, rather than relying on average community responses. For instance, to assess the impact of temperature on discrete patch‐ and bloom‐dynamics, studies have embedded taxon‐specific thermal responses into predator‐prey models (e.g., Montagnes et al ; Yang et al ). Moreover, to better approximate community and ecosystem processes, predator‐prey dynamics are now being incorporated into large‐scale models; i.e., complex network‐models include predator‐prey functions, relying on taxon‐specific responses, rather than the cross‐community response used in older model structures (e.g., Pawar et al ; Posch et al ; D'Alelio et al ).…”

“…Within these waters, it has long been recognized that protozoan growth rates tend to match those of their algal prey (e.g., Banse ). This coupling allows rapid exploitation of prey populations, drives food web dynamics, may prevent algal blooms through top‐down control, and potentially reduces harmful algal blooms ( see “Predator‐prey dynamics” section, Rose and Caron ; Montagnes et al ; Sherr and Sherr ; Yang et al ).…”

Temperature sensitivities of microbial plankton net growth rates are seasonally coherent and linked to nutrient availability

“…Disentangling the factors controlling the dynamics of planktonic microorganisms biomass and productivity is a central topic in marine microbial ecology (Ducklow, ; Kirchman, ). Regulation by resource availability (bottom‐up), mortality including predation and viral lysis (top‐down) and temperature explain most of the variability of the standing stocks and activity of phytoplankton, heterotrophic prokaryotes and protistan grazers (Yang et al, ). These three types of control operate simultaneously with varying contributions to the observed variability, but some general patterns have been recently suggested (Morán et al, ).…”

Simulating Effects of Variable Stoichiometry and Temperature on Mixotrophy in the Harmful Dinoflagellate Karlodinium veneficum

“…These wetter spring conditions, with more nutrients may lead to more N-rich and/or P-deplete prey that may further support the development of these HABs. As mixotrophs may be more temperature sensitive than their autotrophic prey, the increased temperatures could enhance their ingestion capabilities and effectively control the growth of autotrophic prey (e.g., Yang et al, 2016). The modeled biomass of K. veneficum as a mixotroph was found to achieve the highest biomass when they consumed prey under high N:P conditions (Figure 5).…”