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Light and Nutrients Alter Detritivore Assimilation of Microbial Nutrients from Leaf Litter

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Light and Nutrients Alter Detritivore Assimilation of Microbial Nutrients from Leaf Litter The University of Southern Mississippi The Aquila Digital Community Faculty Publications 6-1-2021 Brown Meets Green: Light and Nutrients Alter Detritivore Assimilation of Microbial Nutrients From Leaf Litter Taylor L. Price University of Southern Mississippi Jennifer Harper Eastern Michigan University Steven N. Francoeur Eastern Michigan University Halvor M. Halvorson University of Southern Mississippi Kevin A. Kuehn University of Southern Mississippi, [email protected] Follow this and additional works at: https://aquila.usm.edu/fac_pubs Part of the Ecology and Evolutionary Biology Commons Recommended Citation Price, T., Harper, J., Francoeur, S., Halvorson, H., Kuehn, K. (2021). Brown Meets Green: Light and Nutrients Alter Detritivore Assimilation of Microbial Nutrients From Leaf Litter. Ecology, 102(6). Available at: https://aquila.usm.edu/fac_pubs/18837 This Article is brought to you for free and open access by The Aquila Digital Community. It has been accepted for inclusion in Faculty Publications by an authorized administrator of The Aquila Digital Community. For more information, please contact [email protected]. Report Ecology, 102(6), 2021, e03358 © 2021 by the Ecological Society of America Brown meets green: light and nutrients alter detritivore assimilation of microbial nutrients from leaf litter 1,2 3,4 3 1,5 TAYLOR L. PRICE , JENNIFER HARPER, STEVEN N. FRANCOEUR , HALVOR M. HALVORSON , AND 1,6 KEVIN A. KUEHN 1School of Biological, Environmental, and Earth Sciences, University of Southern Mississippi, Hattiesburg, Mississippi 39406 USA 2Department of Plant and Microbial Biology, University of Minnesota, Saint Paul, Minnesota 55108 USA 3Department of Biology, Eastern Michigan University, Ypsilanti, Michigan 48197 USA 4Department of Biological Sciences, Bowling Green State University, Bowling Green, Ohio 43403 USA 5Department of Biology, University of Central Arkansas, Conway, Arkansas 72035 USA Citation: Price, T. L., J. Harper, S. N. Francoeur, H. M. Halvorson, and K. A. Kuehn. 2021. Brown meets green: light and nutrients alter detritivore assimilation of microbial nutrients from leaf litter. Ecology 102 (6):e03358. 10.1002/ecy.3358 Abstract. In aquatic detrital-based food webs, research suggests that autotroph-hetero- troph microbial interactions exert bottom-up controls on energy and nutrient transfer. To address this emerging topic, we investigated microbial responses to nutrient and light treat- ments during Liriodendron tulipifera litter decomposition and fed litter to the caddisfly larvae Pycnopsyche sp. We measured litter-associated algal, fungal, and bacterial biomass and pro- duction. Microbes were also labeled with 14C and 33P to trace distinct microbial carbon (C) and phosphorus (P) supporting Pycnopsyche assimilation and incorporation (growth). Litter- associated algal and fungal production rates additively increased with higher nutrient and light availability. Incorporation of microbial P did not differ across diets, except for higher incorpo- ration efficiency of slower-turnover P on low-nutrient, shaded litter. On average, Pycnopsyche assimilated fungal C more efficiently than bacterial or algal C, and Pycnopsyche incorporated bacterial C more efficiently than algal or fungal C. Due to high litter fungal biomass, fungi supported 89.6–93.1% of Pycnopsyche C growth, compared to 0.2% to 3.6% supported by bac- teria or algae. Overall, Pycnopsyche incorporated the most C in high nutrient and shaded litter. Our findings affirm others’ regarding autotroph-heterotroph microbial interactions and extend into the trophic transfer of microbial energy and nutrients through detrital food webs. Key words: algae; bacteria; carbon; ecological stoichiometry; fungi; phosphorus; Pycnopsyche. levels (Sterner et al. 1997). While green and brown food INTRODUCTION webs differ in their energy basis, they are both limited by Classic approaches to trophic ecology have focused on the availability of nutrients (e.g., nitrogen and phospho- delineating energy and material flow between “brown” rus (P)) and play major roles in ecosystem-level energy and “green” food webs (Lindeman 1942, Brett et al. flow and nutrient cycling (Zou et al. 2016, Evans-White 2017). Brown food webs are driven by inputs of detrital and Halvorson 2017). subsidies and subsequent assimilation and mineraliza- In brown food webs, detritivores derive nutrition tion by microbial decomposers (i.e., fungi and bacteria) from both detritus and microbial biomass (Marks that are key to detritivore nutrition (Marks 2019). In 2019). The detrital-microbial matrix consists of diverse turn, green food webs are directly influenced by light microbes, predominantly heterotrophic fungi and bacte- availability, which regulates autotroph biomass and ria, which may differ in nutritional importance for nutrient content, and therefore influences upper trophic detritivores (Findlay et al. 2002). Detritivores assimilate most of their nutrition from microbial biomass com- pared to the detritus itself, due to the higher nutritional Manuscript received 22 September 2020; revised 27 January value of microbial biomass; for example, fungi colonize 2021; accepted 15 March 2021. Corresponding Editor: Helmut Hillebrand. and assimilate detrital organic carbon (C) and nutrients 6 E-mail: [email protected] into a form more palatable for detritivores to ingest Article e03358; page 1 Article e03358; page 2 TAYLOR L. PRICE ET AL. Ecology, Vol. 102, No. 6 and assimilate (Chung and Suberkropp 2009). The Pycnopsyche growth, based on experiments established detrital substrate is one source of nutrients supporting in previous feeding studies (Chung and Suberkropp microbial biomass, but microbes can also assimilate dis- 2009). On 8 January 2018 leaf discs were mounted on solved inorganic nutrients, which allows microbes to acrylic plates and conditioned for seven weeks in eight increase biomass, growth rates, and nutrient contents outdoor flume mesocosms at Lake Thoreau Environ- with increased inorganic nutrient availability (Manning mental Center using stream water from Big Creek, a sec- et al. 2015). ond-order forested stream in De Soto National Forest, To date, most research within detrital-based food webs Mississippi, USA. Four low-nutrient flumes received no has emphasized the nutritional importance of hetero- nutrient amendments while four high-nutrient flumes trophic bacteria and fungi to detritivores (e.g., Chung received nutrient amendments of NaNO3 and Na2HPO4 and Suberkropp 2009, Halvorson et al. 2016); however, to raise concentrations by 400 µg/L N-NO3 and 60 µg/L roles of detrital-associated autotrophic microbes (i.e., P-PO4, with new amendments during each water change. algae) remain poorly known. This is due to the assump- Flumes from a given nutrient level shared an aerated tion that autotrophs play minimal roles in detrital-based recirculating cattle trough, containing 150 L stream food webs, especially in ecosystems of low light availabil- water of which one-third was replaced every 5 d and set ity and low algal biomass, such as headwater streams. to flow rates of 10 mL/s in each flume. All flumes were Yet, increasing research suggests that algae can play key shaded by mesh canopy to reduce solar heating; each of roles in brown food webs by stimulating heterotrophic the eight flumes was divided into half receiving ambient activity (Danger et al. 2013, Kuehn et al. 2014, Demars sunlight (light treatment; 51% and 23% of ambient pho- et al. 2020). Moreover, food web data suggest that detri- tosynthetically active radiation (PAR) and UV, respec- tivores partly rely on green energy pathways, suggesting tively) and half shaded with opaque barrier (shade that autotrophs play greater roles in detrital food webs treatment; PAR and UV below detection). HOBO Onset than is classically assumed (Wolkovich et al. 2014). Loggers (Onset Computer Corporation, Bourne, Mas- Algae support animal growth across many aquatic sys- sachusetts, USA) monitored temperatures, and after tems, likely due to the high nutritional quality of algal each nutrient amendment, we collected, froze, and amino and fatty acids (Brett et al. 2017). Anthropogenic thawed and filtered water to measure concentrations of deforestation and nutrient enrichment have also likely P-PO4, N-NH4, and N-[NO3] using a SEAL Autoana- magnified these algal roles in aquatic food webs by lyzer 3 (SEAL Analytical, Mequon, Wisconsin, USA). removing growth constraints on algae, further motivat- See Appendix S1: Table S1 for flume water physico- ing research of algal influences on brown food webs chemistry. eport (Danger et al. 2013, Kaylor et al. 2016). After conditioning, replicate leaf discs were collected Our objective was to determine the effects of light and to characterize elemental content, microbial biomass, nutrient availability on the detrital-microbial matrix and and production rates in the laboratory (Appendix S2: R subsequent trophic transfer of microbial energy and Table S2). Briefly, litter fungal biomass and production nutrients to detritivores. We used 14C and 33P as tracers were estimated using the concentration of ergosterol and of assimilation and incorporation of detrital microbial C incorporation of 14C-acetate into ergosterol, respectively. and P by the detritivorous caddisfly larvae Pycnopsyche The algal taxa, Oedogonium, found in our study, produce sp. We hypothesized that (1) given the comparatively ergosterol; however, prior experiments have shown litter- high quality of algal nutrients (Brett et al. 2017), larvae
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