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1. Stable isotope fingerprinting traces essential amino acid assimilation and multichannel feeding in a vertebrate consumer

   https://doi.org/10.1111/2041-210X.13903  

   Manlick, Philip J.; Newsome, Seth D. (June 2022, Methods in Ecology and Evolution)

   Abstract Animals often consume resources from multiple energy channels, thereby connecting food webs and driving trophic structure. Such ‘multichannel feeding’ can dictate ecosystem function and stability, but tools to quantify this process are lacking. Stable isotope ‘fingerprints’ are unique patterns in essential amino acid (EAA) δ¹³C values that vary consistently between energy channels like primary production and detritus, and they have emerged as a tool to trace energy flow in wild systems. Because animals cannot synthesize EAAs de novo and must acquire them from dietary proteins, ecologists often assume δ¹³C fingerprints travel through food webs unaltered. Numerous studies have used this approach to quantify energy flow and multichannel feeding in animals, but δ¹³C fingerprinting has never been experimentally tested in a vertebrate consumer.We tested the efficacy of δ¹³C fingerprinting using captive deer micePeromyscus maniculatusraised on diets containing bacterial, fungal and plant protein, as well as a combination of all three sources. We measured the transfer of δ¹³C fingerprints from diet to consumer liver, muscle and bone collagen, and we used linear discriminant analysis (LDA) and isotopic mixing models to estimate dietary proportions compared to known contributions. Lastly, we tested the use of published δ¹³C source fingerprints previously used to estimate energy flow and multichannel feeding by consumers.We found that EAA δ¹³C values exhibit significant isotopic (i.e. trophic) fractionation between consumer tissues and diets. Nevertheless, LDA revealed that δ¹³C fingerprints are consistently routed and assimilated into consumer tissues, regardless of isotopic incorporation rate. Isotopic mixing models accurately estimated the proportional diets of consumers, but all models overestimated plant‐based protein contributions, likely due to the digestive efficiencies of protein sources. Lastly, we found that δ¹³C source fingerprints from published literature can lead to erroneous diet reconstruction.We show that δ¹³C fingerprints accurately measure energy flow to vertebrate consumers across tissues with different isotopic incorporation rates, thereby enabling the estimation of multichannel feeding at various temporal scales. Our findings illustrate the power of δ¹³C fingerprinting for quantifying food web dynamics, but also reveal that careful selection of dietary source data is critical to the accuracy of this emerging technique. 

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2. The coupling of green and brown food webs regulates trophic position in a montane mammal guild

   https://doi.org/10.1002/ecy.3949  

   Manlick, Philip_J; Cook, Joseph_A; Newsome, Seth_D (January 2023, Ecology)

   Abstract Food web ecology has revolutionized our understanding of ecological processes, but the drivers of food web properties like trophic position (TP) and food chain length are notoriously enigmatic. In terrestrial ecosystems, above‐ and belowground systems were historically compartmentalized into “green” and “brown” food webs, but the coupling of these systems by animal consumers is increasingly recognized, with potential consequences for trophic structure. We used stable isotope analysis (δ¹³C, δ¹⁵N) of individual amino acids to trace the flow of essential biomolecules and jointly measure multichannel feeding, food web coupling, and TP in a guild of small mammals. We then tested the hypothesis that brown energy fluxes to aboveground consumers increase terrestrial food chain length via cryptic trophic transfers during microbial decomposition. We found that the average small mammal consumer acquired nearly 70% of their essential amino acids (69.0% ± 7.6%) from brown food webs, leading to significant increases in TP across species and functional groups. Fungi were the primary conduit of brown energy to aboveground consumers, providing nearly half the amino acid budget for small mammals on average (44.3% ± 12.0%). These findings illustrate the tightly coupled nature of green and brown food webs and show that microbially mediated energy flow ultimately regulates food web structure in aboveground consumers. Consequently, we propose that the integration of green and brown energy channels is a cryptic driver of food chain length in terrestrial ecosystems. 

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3. Amino acid carbon isotope fingerprints are unique among eukaryotic microalgal taxonomic groups

   https://doi.org/10.1002/lno.12350  

   Stahl, Angela R.; Rynearson, Tatiana A.; McMahon, Kelton W. (April 2023, Limnology and Oceanography)

   Abstract Eukaryotic microalgae play critical roles in the structure and function of marine food webs. The contribution of microalgae to food webs can be tracked using compound‐specific isotope analysis of amino acids (CSIA‐AA). Previous CSIA‐AA studies have defined eukaryotic microalgae as a single functional group in food web mixing models, despite their vast taxonomic and ecological diversity. Using controlled cultures, this work characterizes the amino acidδ¹³C (δ¹³C_AA) fingerprints—a multivariate metric of amino acid carbon isotope values—of four major groups of eukaryotic microalgae: diatoms, dinoflagellates, raphidophytes, and prasinophytes. We found excellent separation of essential amino acidδ¹³C (δ¹³C_EAA) fingerprints among four microalgal groups (mean posterior probability reclassification of 99.2 ± 2.9%). We also quantified temperature effects, a primary driver of microalgal bulk carbon isotope variability, on the fidelity ofδ¹³C_AAfingerprints. A 10°C range in temperature conditions did not have significant impacts on variance inδ¹³C_AAvalues or the diagnostic microalgalδ¹³C_EAAfingerprints. Theseδ¹³C_EAAfingerprints were used to identify primary producers at the base of food webs supporting consumers in two contrasting systems: (1) penguins feeding in a diatom‐based food web and (2) mixotrophic corals receiving amino acids directly from autotrophic endosymbiotic dinoflagellates and indirectly from water column diatoms, prasinophytes, and cyanobacteria, likely via heterotrophic feeding on zooplankton. The increased taxonomic specificity of CSIA‐AA fingerprints developed here will greatly improve future efforts to reconstruct the contribution of diverse eukaryotic microalgae to the sources and cycling of organic matter in food web dynamics and biogeochemical cycling studies. 

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4. Preservation of stable isotope signatures of amino acids in diagenetically altered Middle to Late Holocene archaeological mollusc shells

   https://doi.org/10.1016/j.gca.2023.05.005  

   Vokhshoori, N.L.; Rick, T.C.; Braje, T.J.; McCarthy, M.D. (July 2023, Geochimica et Cosmochimica Acta)

   Stable isotope proxies measured in the proteinaceous fraction of archaeological mollusc shell represents an increasingly important archive for reconstructing past ecological and biogeochemical conditions of nearshore environments. A major issue, however, is understanding the impact of diagenetic alteration in sub-fossil shell isotope values. “Bulk” stable isotope values of nitrogen (δ15N), and especially carbon (δ13C) often shift strongly with increasing C/N ratios in degraded shell, resulting in unreliable data. Here, we examine preservation of an entirely new set of shell paleo-proxies, compound-specific isotopes of amino acids (CSI-AA). We examine carbon (δ13CAA) and nitrogen (δ15NAA) patterns and values from the organic fraction of California mussel (Mytilus californianus) shells from the California Channel Islands. Archaeological shell samples ranging in age from ca. 6,100 to 250 cal BP exhibiting a wide range of degradation states were collected from varied depositional environments (e.g., exposed coastal bluff, buried strata, etc.), and were directly compared to modern shells of the same species and region. Our results indicate organic matter C/N ratios as the best bulk diagnostic indicator of the relative degradation state of shell organic fraction, including changes at the molecular level. Modern shell organic C/N ratios ranged from 2.8 to 3.5, while those in archaeological shell were substantially elevated (3.4–9.5), exhibiting strong and significant negative correlations with bulk δ13C values, weight %C, and weight %N, and a significant but weaker correlation with δ15 N values. An additional “cleaning” step using weak NaOH helped to remove possible exogenous contaminants and improved bulk values of some samples. However, relative molar AA abundances revealed that some AAs, especially the two most abundant, Glycine and Alanine, progressively decreased with increasing C/N ratio. The loss of these amino acids permanently alters bulk isotope values regardless of removal of contaminants. Modeling the bulk isotope change expected due to amino acid molar composition showed major and predictable shifts in bulk δ13C values from selected AA loss, and similarly large but far more variable impacts from exogenous contaminants. In contrast to bulk data, key CSI-AA values and patterns remained almost entirely unaltered, even in the most degraded shell samples, closely matching expected biosynthetic isotope patterns in modern mussel shell. AA isotope proxies for “baseline” (δ15N-Phenylalanine and average δ13C-Essential AAs) and planktonic trophic structure (δ15N-Glutamic Acid and δ15N-Phenylalanine) were not statistically altered with degradation in any sample. Overall, we conclude that while bulk isotopes, particularly δ13C, are very likely to be unreliable in archaeological or subfossil shell with C/N ratios higher than ∼4.0, CSI-AA proxies can still be used to reconstruct past climatic and ecological conditions of the nearshore marine environment. 

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5. Relative Importance of Macroalgae and Phytoplankton to Nearshore Consumers and Growth Across Climatic Conditions in the Northern Gulf of Alaska

   https://doi.org/10.1007/s12237-024-01371-6  

   Corliss, Katherine; von_Biela, Vanessa; Coletti, Heather; Bodkin, James; Esler, Daniel; Iken, Katrin (September 2024, Estuaries and Coasts)

   Abstract Macroalgae and phytoplankton support the base of highly productive nearshore ecosystems in cold-temperate regions. To better understand their relative importance to nearshore food webs, this study considered four regions in the northern Gulf of Alaska where three indicator consumers were collected, filter-feeding mussels (Mytilus trossulus), pelagic-feeding Black Rockfish (Sebastes melanops), and benthic-feeding Kelp Greenling (Hexagrammos decagrammus). The study objectives were to (1) estimate the proportional contributions of macroalgal and phytoplankton organic matter using carbon and nitrogen stable isotopes, (2) determine if macroalgal use affected consumer growth using annual growth rings in shells or otoliths, and (3) describe changes in organic matter use and growth during the Pacific Marine Heatwave (PMH; 2014–2016) in one consumer, mussels. Macroalgae were the major organic matter source (> 60%) to the diet for all three consumers. The relationships between macroalgal contribution and growth were neutral for both fish species and significantly positive for mussels. During the PMH, mussels had a drop (> 10%) in macroalgal contributions and grew 45% less than in other time periods. Simultaneously, the relationship between macroalgal contribution and mussel growth was strongest during the PMH, explaining 48% variation compared to 3–12% before or after the PMH. Collectively, the results suggest that macroalgae is likely more important to cold-temperate nearshore food webs than phytoplankton. Management actions aimed at conserving and expanding macroalgae are likely to benefit nearshore food webs under all climate scenarios and especially during marine heatwaves. 

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