Algal-Mediated Priming Effects on the Ecological Stoichiometry of Leaf Litter Decomposition: A Meta-Analysis

Abstract

In aquatic settings, periphytic algae exude labile carbon (C) that can significantly suppress or stimulate heterotrophic decomposition of recalcitrant C via priming effects. The magnitude and direction of priming effects may depend on the availability and stoichiometry of nutrients like nitrogen (N) and phosphorus (P), which can constrain algal and heterotrophic activity; in turn, priming may affect heterotrophic acquisition not only of recalcitrant C, but also N and P. In this study, we conducted a meta-analysis of algal-mediated priming across leaf litter decomposition experiments to investigate (1) bottom-up controls on priming intensity by dissolved N and P concentrations, and (2) effects of algal-mediated priming on the fate of litter-periphyton N and P during decomposition. Across a total of nine datasets, we quantified priming intensity and tested algal effects on litter-periphyton C:N, C:P, and N-and P-specific mass loss rates. Algal effect sizes did not significantly differ from zero, indicating weak or inconsistent algal effects on litter-periphyton stoichiometry and nutrient loss. These findings were likely due to wide variation in algal priming intensity across a limited number of experiments, ranging from strongly negative (410% reduced decomposition) to strongly positive (104% increased decomposition). Correlation and response surface analyses showed that priming intensity switched from negative to positive with increasing dissolved inorganic N:P across datasets. Algal effects on litter-periphyton stoichiometry and nutrient loss further co-varied with dissolved N:P across datasets, suggesting algae most strongly influence the stoichiometry of decomposition under imbalanced N:P, when priming is most intense. Our findings from this limited meta-analysis support the need for additional tests of aquatic priming effects, especially across gradients of N and P availability, with consideration of coupled C and nutrient dynamics during priming of organic matter decomposition.

Temporal and stoichiometric patterns of algal stimulation of litter‐associated heterotrophic microbial activity

“…Exploration of the factors contributing to 3 such litter-specific responses could be of considerable interest. 4 Alteration of litter stoichiometry affected extracellular enzyme activity in ways broadly 6 congruent with predictions based upon litter stoichiometry and the resulting relative scarcity of 7 C, N and P within litter. Nutrient-enhanced Schoenoplectus litter displayed elevated Gase and 8 LAMPase activity, consistent with expectations of how the activities of these enzymes would 9 change under conditions in which the relative abundance of P was increased.…”

“…In contrast, photosynthesis can also reduce litter decomposition rates via negative priming effects (Halvorson et al, 2019a), possibly as a result of fungal decomposers shifting C acquisition from litter to photosynthetically-derived labile organic C. It is possible that identity of the nutrient in shortest supply might regulate the direction of the priming effect. For example, a recent meta-analysis found that increased DIN:SRP ratios were associated with a switch from negative to positive priming of litter decomposition (Halvorson, Francoeur, Findlay, & Kuehn, 2019b).…”

“…All rights reserved resources (e.g., photosynthetic provision of labile C; e.g., Wyatt, Stevenson, & Turetsky, 2010;Wyatt, Tellez, Woodke, Bidner, & Davison, 2014) could result in differential up-or downregulation of enzymatic synthesis. Furthermore, relative scarcity of N or P might interact with C supply to influence microbial capacity to produce extracellular enzymes (see Halvorson et al, 2019b). Individual optima of extracellular enzymes with respect to environmental conditions (e.g., pH, Espeland & Wetzel, 2001;Francoeur & Wetzel, 2003), coupled to photosyntheticallymediated shifts in these environmental conditions (e.g., Jones, Eaton, & Hardwick, 2000;Espeland & Wetzel, 2001) could add another layer of complexity to enzymatic responses to photosynthesis.…”

Aggregated filter‐feeders govern the flux and stoichiometry of locally available energy and nutrients in rivers

“…However, nearly half of aggregate excretion in our study exceeded microbial TER C:P (ln( E v C:P) = 5.00 ± 0.60), but none exceeded C:N (ln( E v C:N) = 1.18 ± 0.38), suggesting there is a great potential for animal‐mediated nutrient cycling to link green and brown food webs under high C and low‐nutrient conditions. Although microbial priming can be significant, the ecological stoichiometry of priming effects is understudied (Halvorson et al., 2019), especially by aquatic animals (Halvorson et al., 2020). We suggest biogeochemical hotspots associated with animal aggregations with opposing stoichiometric trait abundances may influence priming intensity or switch it from negative to positive depending on nutrient context.…”

Substratum‐associated microbiota

“…Work by Francoeur, Neely, Underwood, and Kuehn (2020) supported the hypothesis that benthic algal photosynthesis strongly influences heterotrophic microbial activity on macrophyte leaf litter, especially that of fungi, throughout microbial community development, but how much algal photosynthesis stimulates heterotrophs may not depend on differences in litter nutrient content according to leaf litter stoichiometry. Halvorson, Francoeur, Francoeur, Findlay, and Kuehn (2019) conducted a meta‐analysis across leaf litter decomposition experiments to investigate the influence and fate of dissolved N and P in algal‐mediated priming. Analysis across datasets produced insights about how priming intensity can switch from negative to positive as dissolved N:P increases, as well as the conditions when algae most strongly influence the stoichiometry of decomposition (when N:P is very low or very high).…”