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

Abstract

Animals can have pervasive effects on ecosystems as they modify their biogeochemical and physical environments. In particular, when animals occur in high densities these effects can result in dramatic changes in the physical environment and biogeochemical hotspots or hot moments. While most research to date has focused on the direct role of animals in biogeochemical cycles, few have examined how animals indirectly influence biogeochemical cycles across scales. Freshwater mussels occur as spatially heterogeneous, dense and species‐rich aggregations in many river ecosystems world‐wide. Here we examined how mussel communities (a) directly influence the flux of particulate and dissolved nutrients and (b) indirectly effect the flux of N2 production, via denitrification, across a gradient of mussel biomass and differences in community composition at the patch‐ (0.25 m2) and stream reach‐scales (60–80 m). We combined measurements of ammonia (N) and soluble reactive phosphorous (P) excretion and C, N and P biodeposition rates for 10 species with biomass and distribution estimates for seven mixed‐species aggregations to quantify direct mussel contributions to biogeochemical cycling and the spatial heterogeneity of their impact. Additionally, we sampled sediments at a fine spatial scale to determine how mussel biomass and richness influence potential denitrification (indirect flux) rates at the patch‐ and reach‐scales. We predicted that increasing mussel biomass would lead to greater direct and indirect fluxes of nutrients, manifesting in heterogeneous nutrient redistribution within and among stream reaches. We also predicted that variation in community composition would result in differential nutrient excretion and egestion stoichiometries. Our results indicate that mussel aggregations directly influence soluble and particulate nutrient fluxes with community composition, particularly phylogenetic tribe composition, controlling the stoichiometry. Mussel aggregations also indirectly influenced nutrient fluxes as greater mussel biomass and species richness resulted in higher denitrification rates as mediated by their interactions with the sediments and enhancement of nutrient availability. Our results underscore the importance of patchy communities in acting as biogeochemical control points. A free Plain Language Summary can be found within the Supporting Information of this article.

Long‐term monitoring shows that drought sensitivity and riparian land use change coincide with freshwater mussel declines

“…Here, it has been shown that analysing temporal changes in both the species and functional composition of mussel beds yields further insights into the potential adverse effects of anthropogenic change on mussels. Mussel declines threaten both biodiversity and the roles that mussels play in driving ecosystem functioning and generating ecosystem services (Atkinson, Julian & Vaughn, 2014; Vaughn, 2018; DuBose et al, 2019; Atkinson & Forshay, 2022). Even remote natural catchments are vulnerable to human changes, but repeated sampling at appropriate time scales and functional classifications can provide additional biological insights that may help decision‐makers prioritize freshwater mussel conservation.…”

Identifying potential drivers of distribution patterns of invasive Corbicula fluminea relative to native freshwater mussels (Unionidae) across spatial scales

“…Sediment organic matter produced by mussels via biodeposition may be an important factor influencing the distribution of Corbicula , because OM can be an alternative food source that is accessed through pedal feeding (Hakenkamp & Palmer, 1999; Hakenkamp et al, 2001) and may provide them with beneficial gut microbiota (Chiarello et al, 2022). It seems likely high densities of Corbicula may be supported in habitats with high organic matter content, such as mussel beds (Atkinson & Forshay, 2022; Vaughn & Hakenkamp, 2001). Thus, Corbicula invading into mussel bed habitats may not be limited by habitat parameters in these rivers and begs the question of whether OM biodeposition may facilitate Corbicula invasion into mussel beds.…”

“…Mussel beds exist in river channels that experience significant sediment mobility, but beds can persist in the same stream sites and have similar abundance and species composition for decades (Sansom et al, 2018). Mussels are also heterogeneous within beds, with individual mussels aggregating in dense patches separated by areas with few or no mussels (Atkinson & Forshay, 2022; Vaughn & Spooner, 2006b). Mussels are crucial for ecosystem function as they filter particles from the water column and excrete and egest nutrients that are important to green (Vaughn et al, 2008) and brown food webs (Atkinson et al, 2021; Hopper et al, 2021).…”

Assessing the potential for restoring freshwater mussels to urban streams

“…A number of studies have shown that the presence of mussel beds may enhance stream capacity to support biodiverse communities, and create biogeochemical hotspots for N removal and sequestration (e.g. Gardner et al, 2001; Benelli et al, 2017; Hoellein et al, 2017; Nickerson, Mortazavi & Atkinson, 2019; Atkinson & Forshay, 2022). In regions like Chesapeake Bay, where stream restoration projects are implemented with a goal towards improving ecosystem services, such as sediment and nutrient retention, there is a need to document the potential for mussel stocking to enhance the provisioning of these services (Wood et al, 2021).…”