Stoichiometric mismatch causes a warming-induced regime shift in experimental plankton communities

In many ecosystems, consumers respond to warming differently than their resources, sometimes leading to temporal mismatches between seasonal maxima in consumer demand and resource availability. A potentially equally pervasive, but less acknowledged threat to the temporal coherence of consumer-resource interactions is mismatch in food quality. Many plant and algal communities respond to warming with shifts toward more carbon-rich species and growth forms, thereby diluting essential elements in their biomass and intensifying the stoichiometric mismatch with herbivore nutrient requirements. Here we report on a mesocosm experiment on the spring succession of an assembled plankton community in which we manipulated temperature (ambient vs. +3.6°C) and presence versus absence of two types of grazers (ciliates and Daphnia), and where warming caused a dramatic regime shift that coincided with extreme stoichiometric mismatch. At ambient temperatures, a typical spring succession developed, where a moderate bloom of nutritionally adequate phytoplankton was grazed down to a clear-water phase by a developing Daphnia population. While warming accelerated initial Daphnia population growth, it speeded up algal growth rates even more, triggering a massive phytoplankton bloom of poor food quality. Consistent with the predictions of a stoichiometric producer-grazer model, accelerated phytoplankton growth promoted the emergence of an alternative system attractor, where the extremely low phosphorus content of the abundant algal food eventually drove Daphnia to extinction. Where present, ciliates slowed down the phytoplankton bloom and the deterioration of its nutritional value, but this only delayed the regime shift. Eventually, phytoplankton also grew out of grazer control in the presence of ciliates, and the Daphnia population crashed. To our knowledge, the experiment is the first empirical demonstration of the "paradox of energy enrichment" (grazer starvation in an abundance of energy-rich but nutritionally imbalanced food) in a multispecies phytoplankton community. More generally, our results support the notion that warming can exacerbate the stoichiometric mismatch at the plant-herbivore interface and limit energy transfer to higher trophic levels.