Animal‐mediated organic matter transformation: Aquatic insects as a source of microbially bioavailable organic nutrients and energy

Abstract

Animal communities are essential drivers of energy and elemental flow in ecosystems. However, few studies have investigated the functional role of animals as sources of dissolved organic matter (DOM) and the subsequent utilization of that DOM by the microbial community. In a small forested headwater stream, we tested the effects of taxonomy, feeding traits, and body size on the quality and quantity of dissolved organic carbon (DOC) and dissolved organic nitrogen (DON) excreted by aquatic insects. In addition, we conducted steady‐state solute additions to estimate instream demand for labile C and compared it to the C excreted by invertebrates. Individual excretion rates and excretion composition varied with body size, taxonomy and feeding guild. The estimated average community excretion rate was 1.31 μg DOC· per mg insect dry weight (DW)−1 hr−1 and 0.33 μg DON·mg DW−1 hr‐1, and individuals excreted DON at nearly twice the rate of NH4+. This DOM was 2–5 times more bioavailable to microbial heterotrophs than ambient stream water DOM. We estimated that the insect community, conservatively, excreted 1.62 mg of bioavailable DOC·m−2 hr−1 and through steady‐state additions measured an ambient labile C demand as 3.97 ± 0.67 mg C m−2 hr−1. This suggests that insect‐mediated transformation and excretion of labile DOC could satisfy a significant fraction (40 ± 7%) of labile C demand in this small stream. Collectively, our results suggest that animal excretion plays an essential functional role in transforming organic matter into microbially bioavailable forms and may satisfy a variable but significant portion of microbial demand for labile C and N. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13242/suppinfo is available for this article.

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

“…Importantly, aggregate nutrient and DOM excretion rates were driven by body size and taxonomy of individuals within assemblages, highlighting the fundamental control of animal metabolism and stoichiometry on biogeochemical cycling (Vanni & McIntyre, 2016). Additionally, we revealed functional diversity of organic matter and nutrient cycling traits within a functional group (filter‐feeders) that scale to the ecosystem, expanding previous work demonstrating such diversity among functional groups (Hopper et al., 2018; Parr et al., 2019). Overall, we provided evidence that biogeochemical hotspots associated with animal biomass and stoichiometric traits may constitute a large source of microbially available dissolved nutrient and energy subsidies.…”

“…Body size mediated excretion rates of DOM, N, and P. Although variable, increasing DOM excretion rates with increasing body size parallels those for inorganic nutrients excreted by mussels in our study and previous studies of animal‐mediated nutrient cycling (Vanni & McIntyre, 2016). This result highlights the influence of metabolism, driven by body size, on animal‐mediated DOM transformation (Meyer & O'Hop, 1983; Parr et al., 2019). Body size is the strongest predictor of nutrient excretion rates across vertebrate and invertebrate taxa because allometric metabolic scaling leads to higher per capita, but lower mass‐specific excretion rates in large animals (Vanni & McIntyre, 2016).…”

“…Additionally, we identified functional diversity within a functional‐feeding group (filter‐feeders) by quantifying DOM fluorescent signatures of excreta for species occurring across environmental gradients. In previous work, DOM fluorescent signatures highlighted among functional‐feeding group differences in organic matter transformation, showing that predatory insects had distinct DOM fluorescent signatures compared with insects feeding at lower trophic positions (Parr et al., 2019). Although mussels are filter‐feeders, their diets span a continuum from phytoplankton in lentic systems to bacteria and algae in lotic systems that vary in quality that might affect excreted DOM (Nichols & Garling, 2000; Vander Zanden & Rasmussen, 1999).…”

“…While the terrestrial literature is rich in work illustrating the importance of animal nutrient release in mediating biogeochemical cycling across brown and green food webs (Bohlen et al., 2004; Sitters et al., 2020; Zimmer et al., 2005), animal‐driven nutrient cycling studies in aquatic systems have primarily focused on inorganic N and P influences in green food webs (Atkinson et al., 2017). Therefore, gaps remain in our understanding of aquatic animals as sources of dissolved organic matter (DOM) that may positively influence brown food webs via enhancing microbial production (but see Meyer & O'Hop, 1983; Parr et al., 2019).…”

Ecosystem engineering in the streambed: Net‐spinning caddisflies influence hydraulic properties

“…First, biodeposited caddisfly faecal pellets likely leach dissolved organic matter (DOM) into the hyporheic zone. Previous studies have demonstrated that bioavailable carbon can control biogeochemical activity in the streambed and the leeching of DOM from animal faecal pellets makes up a substantial proportion of available DOM for heterotrophic organisms (Jumars, Penry, Baross, Perry, & Frost, 1989; Parr, Capps, Inamdar, & Metcalf, 2019; Reeder et al, 2018; Urban‐Rich, 1999). Second, caddisfly nets directly increase the surface area available for heterotrophic biofilm colonization in the interstitia.…”