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

Abstract

Biogeochemical cycling has often been characterized by physical and microbial processes, yet animals can be essential mediators of energy and nutrients in ecosystems. Excretion by aggregated animals can be an important local source of inorganic nutrients in green food webs; however, whether animals are a source of dissolved energy that can support brown food webs is understudied. We tested whether animal aggregations are a substantial flux of bioavailable dissolved organic matter (DOM) by studying spatially stable, biogeochemical hotspots formed by filter‐feeding freshwater mussels. We used parallel‐factor analysis to quantify DOM fluorescent components composition of mussel excretion and expected digestive breakdown of particulate food sources would lead to excretion of labile DOM. Next, we combined measured excretion rates of DOM, ammonium (NH4+, N) and phosphorous (SRP; P) for 22 species with biomass estimates for 14 aggregations to quantify contributions of DOM, N and P to local availability. Because mussels occupy distinct stoichiometric niches, we anticipated that differences in species biomass and assemblage structure would elicit different flux and stoichiometries of aggregate excretion. Aggregate dissolved organic carbon (DOC) excretion was minor (1%–11%) compared to N (12%–2,860%) and P (1%–97%), yet generalities across assemblages emerged regarding organic matter transformation by mussels towards labile protein‐like compounds compared to abundant aromatic, humic compounds in ambient water. Aggregate excretion of labile DOM was a substantial pool of bioavailable energy, contributing 2%–114% of local labile DOM. Spatial differences in assemblage structure led to strong differences in aggregate flux and stoichiometry driven by biomass and stoichiometric trait expression of species with contrasting dominance patterns. Under the nutrient conditions of our study (high C:nutrient), biogeochemical hotspots associated with low‐trophic position animal biomass may indirectly control energy flow to the brown food web by shifting C:nutrient stoichiometry available to microbes or directly by increasing the flux of microbially available DOM. Collectively, our results highlight a potentially substantial flux of labile energy and nutrients to microbial communities through the transformation of ingested organic matter by aggregations of animals and emphasize that shared functional trait classification may not translate into shared ecological function. A free Plain Language Summary can be found within the Supporting Information of this article.

Community patch dynamics governs direct and indirect nutrient recycling by aggregated animals across spatial scales

“…Mussel aggregations had direct effects on CND as their patches contribute directly to reconstituting particulate‐bound nutrients into highly available soluble nutrients, dissolved organic matter and translocate suspended particulates as biodeposits into the benthic sediments (Hopper et al., 2021; Vaughn & Hoellein, 2018). Consequently, mussels indirectly enhance denitrification due to their interaction with the stream sediments as they bury and translocate nutrients and organic‐rich materials facilitating microbial activity in the stream sediments.…”

“…As such, community composition and subsequent functional traits impact community tissue stoichiometry and consequential excretion stoichiometry (Atkinson, van Ee, et al., 2020). While recent work has increased awareness of the direct impacts of mussels on biogeochemical cycles (Atkinson & Vaughn, 2015; Hopper et al., 2021), their indirect effects on ecosystem‐level biogeochemical processes, such as denitrification rates, are still relatively understudied (but see, Hoellein et al., 2017; Nickerson et al., 2019; Trentman et al., 2018).…”

Associations among elements in freshwater mussel shells (Unionidae) and their relation to morphology and life history

“…By constructing novel nutrient balances in addition to two balances based on traditional ecological stoichiometry, we provide empirical evidence of species-specific elemental relationships that illustrate associations among elements required for shell biomineralisation and growth. Overall, we highlight a useful approach to quantifying elements beyond C, N, and P for studying biological sources of elemental diversity in animal biomass and add to the growing knowledge of elemental diversity among animals (Allgeier et al, 2015(Allgeier et al, , 2020, and more specifically unionid mussels (Atkinson et al, 2020;Hopper et al, 2021;Vaughn, 2010).…”

“…To explore differences between elements in water and shells we collected water samples ( n = 6) in 2019 and 2020 from near where shells were collected. We used previously published dissolved organic C measurements (Hopper et al., 2021) and measured NH 4 –N, NO 3 –N, NO 2 –N, and soluble reactive phosphorus (PO 4 –P) on a SEAL AQ300 Discrete Analyzer (SEAL Analytics, WI, U.S.A.). We combined these parameters as a measure of total inorganic N from water samples collected during 2020.…”

“…To explore differences between elements in water and shells we collected water samples (n = 6) in 2019 and 2020 from near where shells were collected. We used previously published dissolved organic C measurements (Hopper et al, 2021) We combined these parameters as a measure of total inorganic N from water samples collected during 2020. Analyses for all other elements were run at Waters Agricultural Laboratories Inc. as for shells.…”