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

Abstract

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.

Smaller species but larger stages: Warming effects on inter‐ and intraspecific community size structure

“…Additionally, the empirical results may be biased due to, for instance, seasonal patterns in zooplankton reproduction (as in Kang et al, 2006 ; Turner, 1982 ), or too short experimental durations allowing for only transient changes in stage abundances (as in Beisner et al, 1997 ; Garzke et al, 2015 ). Moreover, how warming affects natural plankton communities may also depend on interactive effects and feedbacks between resource abundance, nutrient availability, and consumer physiological and ecological strategies (Diehl et al, 2022 ; O'Gorman et al, 2017 ). We argue that to understand the response of community size structure to warming, concurrent intraspecific and interspecific size structure shifts need to be accounted for.…”

Experimental warming and browning influence autumnal pelagic and benthic invertebrate biomass and community structure

“…Hixson and Arts (2016) noted in a global analysis that for every 1°C increase in water temperature, the nutritional quality of phytoplankton was significantly reduced (Napolitano, 1999; Taipale et al, 2013). Thus, a mismatch between increased resource availability of likely reduced nutritional quality (Diehl et al, 2022; Hixson & Arts, 2016) and metabolic costs may have driven the negative responses in copepods and rotifers with warming. However, this mechanism is speculative as we did not collect data on nutritional quality and can be related to other mechanisms, such as warming‐induced increases in zooplankton parasitism and disease (Ozersky et al, 2020; Shocket et al, 2018).…”

Climate change creates nutritional phenological mismatches

“…A consumer may experience nutritional phenological mismatch (1F) if its demand for the nutrient (dark purple line) does not advance as rapidly as the higher nutrient resource advances, resulting in unsatisfied demand (light purple filled area) when it is no longer matched with nutrient availability (shaded gray area = sum of nutrients from both resources). The carbon to phosphorus ratio (C:P) of phytoplankton is a key determinant of food quality for zooplankton like Daphnia [7]. With earlier spring warming due to climate change, phytoplankton C:P ratios can quickly become higher than those of Daphnia (solid purple line).…”

“…Because food resources vary widely not only in their seasonal availability, but also in their nutritional composition throughout the year (Figure 1), there is high potential for phenological mismatches based upon nutritional content. For example, while the biomass of primary producers typically peaks later in the season, their nutritional quality for herbivores, in terms of protein and nitrogen content as well as the stoichiometric ratio (see Glossary) of carbon to phosphorus (C:P), is typically higher earlier in the season (e.g., 4,5,6,7). Importantly, the nutrient and energetic content of food resources may also respond to climate change at different rates.…”