Maternal effects in zooplankton consumers are not only mediated by direct but also by indirect effects of phosphorus limitation

Abstract

Nutrient limitation of primary producers has repeatedly been shown to negatively affect consumers, directly through stoichiometric mismatch and indirectly via alterations in the producer's biochemical quality or palatability. In this study, we assessed whether direct and indirect impacts of phosphorus‐limitation on a planktonic consumer are transferred to the next generation via maternal effects and whether these effects reflect an anticipatory adaptive strategy. For this, we subjected cultures of the algivorous monogonont rotifer Brachionus calyciflorus to three food quality treatments, i.e. P‐limited (LP), P‐replete (HP) and P‐enriched LP algae (i.e. algae with an LP‐growth history but with molar C:P ratios equal to those of HP‐algae). After two generations, we subjected offspring of these cultures to each of the three food quality treatments and monitored life history traits. In addition, we tested starvation resistance. Our results showed very strong negative maternal effects of low P food on offspring performance. These negative effects prevailed irrespective of contemporary diets, suggesting transmissive and selfish maternal effects rather than anticipatory adaptive effects. The relative strength of direct and indirect maternal P‐limitation effects varied among different traits. Adult body size was predominantly determined by direct effects of P‐shortage in maternal as well as contemporary food (LP < LP + P and LP + P = HP). In contrast, whereas egg size was negatively affected by direct effects of P‐limitation in the maternal diet, a contemporary diet of LP and LP + P algae resulted in larger eggs than HP algae. Animals born from such larger eggs showed no higher growth rates, but they were more resistant to starvation, likely as the result of higher maternal allocation of energy rich molecules to the eggs. The present study shows that maternal food conditions represent an important factor that should be taken into account in studies of stoichiometric mismatch between producers and consumers.

A critical assessment of the stoichiometric knife-edge: no evidence for artifacts caused by the experimental P-supplementation of algae

“…Irrespective of the molar C:P ratio of the food, rotifer populations fed P-supplemented algae with a growth history under P-limiting conditions (i.e., MP LP?P and HP LP?P ) systematically underperformed compared to rotifers that had been fed algae grown under intermediate or high P levels (MP chem and HP chem ). This observation is consistent with other studies (Rothhaupt 1995;Zhou et al 2018;Zhou and Declerck 2020) that observed and explained such growth rate reductions by indirect non-stoichiometric changes in algal traits associated with P-limited growth, e.g., biochemical composition (Spijkerman and Wacker 2011;Challagulla et al 2015) or morphology (van Donk and Hessen 1995;van Donk et al 1997). Alternatively, such effect of growth history could be interpreted as the result of adverse effects of the P-supplementation treatment, but then one would expect that the magnitude of such effect should increase with increasing amounts of supplemented P. However, we found no empirical support for this expectation given the absence of a statistical interaction between food P content and growth history.…”

“…P-supplementation to algae has been applied for two major aims. In one type of studies, the method has been used to compare the relative impact of direct with indirect, non-stoichiometric impacts of P-limitation (Rothhaupt 1995;Zhou et al 2018;Zhou and Declerck 2020). Typically, two types of algal cultures are set up under P-sufficient (HP) and P-limited (LP food) conditions.…”

The Growth Rate Hypothesis as a predictive framework for microevolutionary adaptation to selection for high population growth: an experimental test under phosphorus rich and phosphorus poor conditions

“…We counted the remaining animals to estimate PGR and preserved them in 4% formalin 132 solution. Data from the first five days were omitted from the calculations to avoid maternal effects from 133 previous culturing conditions (Zhou & Declerck 2020). To determine the fraction of sexual females for 134 each replicate, we examined all preserved individuals and determined the number and type of eggs they 135 carried (Appendix S1).…”

A unified framework for herbivore-to-producer biomass ratio reveals the relative influence of four ecological factors

“…A theory of ecological stoichiometry suggests that the carbon content of primary producers relative to their nutrient content such as nitrogen or phosphorus is an important property affecting growth efficiency in herbivores 4 . Supporting the theory, a number of studies have shown that growth rate in terms of carbon accumulation relative to ingestion rate strongly depends on the carbon contents of the food relative to nutrients [26][27][28][29] . Thus, k can be expressed as:…”

“…As our traps often contained no fish, we used θ ¼ CPUE þ 1. For α nut , we focused on phosphorus since freshwater limnetic ecosystems are primarily phosphorus limited 17,18 and as growth of zooplankton is affected by relative phosphorus in algae [26][27][28][29] . Specifically, we used the carbon to phosphorus ratio of seston as a surrogate for α nut because this ratio has been generally used in consideration of ecological stoichiometry in freshwater 4 .…”