Dietary and taxonomic controls on incorporation of microbial carbon and phosphorus by detritivorous caddisflies

Abstract

Heterotrophic microbes on detritus play critical roles in the nutrition of detritivorous animals, yet few studies have examined factors controlling the acquisition of microbial nutrients toward detritivore growth, which is termed “incorporation". Here, we assessed effects of detrital substrate identity (leaf type), background nutrients, and detritivore species identity on detritivore incorporation of microbial carbon (C) and phosphorus (P) in leaf litter diets. We fed oak and maple litter conditioned under two nutrient concentrations (50 or 500 µg P L(-1)) to the detritivorous caddisfly larvae Ironoquia spp., Lepidostoma spp., and Pycnopsyche lepida and used the radioisotopes 14C as glucose and 33P as phosphate to dually trace incorporation of microbial C and P by caddisflies. Incorporation efficiencies of microbial C (mean ± SE = 12.3 ± 1.3%) were one order of magnitude higher than gross growth efficiencies for bulk detrital C from recent studies (1.05 ± 0.08%). Litter type did not affect incorporation of microbial nutrients; however, caddisflies incorporated microbial P 11 % less efficiently when fed litter from the higher P concentration. Two lower body C:P species (Pycnopsyche and Ironoquia) exhibited 9.9 and 7.1% greater microbial C and 19.0 and 17.7% greater microbial P incorporation efficiencies, respectively, than the higher body C:P species (Lepidostoma). Our findings support ecological stoichiometry theory on post-ingestive regulation that animals fed lower C:P diets should reduce P incorporation efficiency due to excess diet P or alleviation of P-limited growth, and that lower C:P species must incorporate dietary C and P more efficiently to support fast growth of P-rich tissues.

Comparing the Ecological Stoichiometry in Green and Brown Food Webs – A Review and Meta-analysis of Freshwater Food Webs

“…A meta-analysis found that detritivores tended to have a lower C GGE than herbivores (Frost et al, 2006), but other element-specific GGEs and AEs were not commonly available across feeding guilds, and it remains unclear how efficiently detritivores assimilate and convert nutrients into new growth. However, recent estimates for aquatic detritivore element-specific AEs and GGEs (Halvorson et al, 2015b, 2016b) suggest that N- and P-specific AE and GGE are lower than those estimated for aquatic herbivores (DeMott et al, 1998; Ferrão-Filho et al, 2007). Therefore, detritivores will likely excrete elements at lower and egest at higher rates than taxa in other feeding guilds (McManamay et al, 2011).…”

“…Given the importance of microbial C in supporting detritivore growth (Chung and Suberkropp, 2009a; Halvorson et al, 2016b), it is difficult to determine whether positive growth effect sizes are driven by elevated dietary microbial biomass or increased N and P availability. However, one feeding study explicitly manipulated detrital P content without changing fungal biomass and still found strong P-limitation of growth, suggesting P can limit detritivore growth, independent of microbial biomass (Danger et al, 2013b).…”

“…Detritivores fed low-nutrient resources probably slow their feeding rates to increase gut residence time and maximize assimilation of limiting C and nutrients (Golladay et al, 1983). Indeed, assimilation probably imposes strong limits on detritivore growth, owing to the recalcitrance of detrital C and nutrients that set low maximum assimilation efficiencies (Halvorson et al, 2015b, 2016b). In contrast, herbivores fed low-nutrient resources may retain comparatively high assimilation efficiencies and improve growth by increasing intake rates (Fink and Von Elert, 2006; Liess, 2014).…”

“…Therefore, detritivores will likely excrete elements at lower and egest at higher rates than taxa in other feeding guilds (McManamay et al, 2011). This trend is likely to persist even with nutrient enrichment of food resources, because nutrient enrichment does not appear to improve detritivore AE or GGE, possibly because the recalcitrance of detrital C ultimately constrains detritivores’ ability to invest energy or resources toward acquisition of added nutrients (Halvorson et al, 2015b, 2016b). …”

Light and dissolved phosphorus interactively affect microbial metabolism, stoichiometry and decomposition of leaf litter

“…In streams, litter inputs are immediately colonised by microbes, resulting in net nutrient removal (hereafter uptake) from stream water (Mulholland, 2004). These processes of C and nutrient uptake and release often Correspondence: Halvor M. Halvorson, 601 Science Engineering Fayetteville, AR 72701, U.S.A. E-mail: halvorso@gmail.com regulate ecosystem elemental cycles in low-order forested streams (Mulholland, 2004) and form a link among detrital energy, dissolved nutrients and consumer growth (Cummins, 1973;B€ arlocher, 1985;Halvorson et al, 2016). These processes of C and nutrient uptake and release often Correspondence: Halvor M. Halvorson, 601 Science Engineering Fayetteville, AR 72701, U.S.A. E-mail: halvorso@gmail.com regulate ecosystem elemental cycles in low-order forested streams (Mulholland, 2004) and form a link among detrital energy, dissolved nutrients and consumer growth (Cummins, 1973;B€ arlocher, 1985;Halvorson et al, 2016).…”