Life on the stoichiometric knife-edge: effects of high and low food C:P ratio on growth, feeding, and respiration in three Daphnia species

Abstract

Recently, data have emerged indicating that not only high food carbon:phosphorus (C:P) ratio but also low food C:P (P-rich food) can have negative effects on the growth of consumers. The shape of this "stoichiometric knife edge," however, is not yet well-documented, and the mechanisms underpinning it are not understood. Here we report the results of experiments using 3 species of Daphnia (D. magna, D. pulicaria, D. pulex) consuming the green alga Scenedesmus acutus with widely varying C:P ratios (from <50 to >1500 by atoms). The experiments were designed to (1) characterize the potential stoichiometric knife edge for each species, and (2) evaluate potential changes in feeding and respiration rates that may underpin the unimodal response to food C:P. All 3 Daphnia species grew more slowly when food C:P (atomic) exceeded ~250-300 but also when C:P was <120. Both high and low C:P foods were associated with increased respiration rates, indicating that the negative effects of food C:P imbalance at least partially involve increased metabolic costs of dealing with stoichiometrically imbalanced food. Feeding rate experiments indicated that, in contrast with limited previous data, animals generally increased their feeding rate on P-rich food. Overall, the "lower threshold elemental ratio" we identify here (~120) is surprisingly high, in an ecologically meaningful range, suggesting that negative effects of excessive food P content may play an under-recognized role in affecting Daphnia performance in P-rich lakes with low seston C:P ratio. Such effects also need to be incorporated into stoichiometrically explicit models of planktonic trophic interactions.

Herbivore consumers face different challenges along opposite sides of the stoichiometric knife‐edge

“…Indirect negative effects of eutrophication on primary zooplankton consumers, for example, via the promotion of toxic or inedible cyanobacterial blooms (Carpenter ; Schindler et al ) or the enhancement of planktivorous fish stocks (Sereda et al ) are quite well understood. Remarkably, much less attention has been given to the potential detrimental direct effects of stoichiometric mismatch caused by high levels of nutrient supply (Boersma & Elser ; Elser et al ). The results of our study support the idea that the high P content in food seston itself may be an underappreciated factor that may not only contribute to the reduction of primary consumer performance in eutrophied systems (Elser et al ) but that may also affect ecosystem functions, for example, by altering mass‐specific rates of grazing and P excretion.…”

“…Remarkably, much less attention has been given to the potential detrimental direct effects of stoichiometric mismatch caused by high levels of nutrient supply (Boersma & Elser ; Elser et al ). The results of our study support the idea that the high P content in food seston itself may be an underappreciated factor that may not only contribute to the reduction of primary consumer performance in eutrophied systems (Elser et al ) but that may also affect ecosystem functions, for example, by altering mass‐specific rates of grazing and P excretion.…”

Optimal metabolic regulation along resource stoichiometry gradients

“…Moreover, when food C‐to‐nutrient (especially C:P) ratios are low, growth rates can be inhibited, but due to excessive rather than limiting nutrients (Boersma & Elser ; Elser et al . ) and C starvation that results in lowered CUE (del Giorgio & Cole ; Apple & del Giorgio ). The theory presented here neglects these effects and thus cannot predict CUE trends in these C‐poor conditions.…”

“…In the three datasets where CUE increased, the animals were either P-limited or co-limited by N and P ( N : P ð Þ B \ N : P ð Þ S ), and in the two P-limited animals, CUE was consistently low (Fuller et al 2015;Halvorson et al 2015), suggesting that other constraints might have masked a CUE-food C:P relation. Moreover, when food C-to-nutrient (especially C:P) ratios are low, growth rates can be inhibited, but due to excessive rather than limiting nutrients (Boersma & Elser 2006;Elser et al 2016) and C starvation that results in lowered CUE (del Giorgio & Cole 1998;Apple & del Giorgio 2007). The theory presented here neglects these effects and thus cannot predict CUE trends in these C-poor conditions.…”

Functional shifts in lake zooplankton communities with hypereutrophication

“…However, zooplankton can also experience bottom‐up growth limitation from imbalances in nutrient supply relative to their stoichiometric demand (Urabe, Clasen, & Sterner, ). Hypereutrophic lakes may function differently than oligotrophic lakes because the ratio of N:P supplied to lakes can still be above the threshold where primary production is P‐limited while high P loading could shift zooplankton consumers below the threshold elemental ratio where excess P limits growth (Collins et al., ; Elser et al., ; Filstrup et al., ). Further, increased reliance on heterotrophic microbes in hypereutrophic systems may buffer taxa with flexible diets from these impacts (Christoffersen, Riemann, Hansen, Klysner, & Sørensen, ).…”