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1. Meta‐analysis of primary producer amino acid δ 15 N values and their influence on trophic position estimation

   https://doi.org/10.1111/2041-210X.13678  

   Ramirez, Matthew D. ; Besser, Alexi C. ; Newsome, Seth D. ; McMahon, Kelton W. ( August 2021 , Methods in Ecology and Evolution)

   Compound‐specific stable isotope analysis of individual amino acids (CSIA‐AA) has emerged as a transformative approach to estimate consumer trophic positions (TP_CSIA) that are internally indexed to primary producer nitrogen isotope baselines. Central to accurate TP_CSIAestimation is an understanding of beta (β) values—the differences between trophic and source AA δ¹⁵N values in the primary producers at the base of a consumers’ food web. Growing evidence suggests higher taxonomic and tissue‐specificβvalue variability than typically appreciated.

   This meta‐analysis fulfils a pressing need to comprehensively evaluate relevant sources ofβvalue variability and its contribution to TP_CSIAuncertainty. We first synthesized all published primary producer AA δ¹⁵N data to investigate ecologically relevant sources of variability (e.g. taxonomy, tissue type, habitat type, mode of photosynthesis). We then reviewed the biogeochemical mechanisms underpinning AA δ¹⁵N andβvalue variability. Lastly, we evaluated the sensitivity of TP_CSIAestimates to uncertainty in meanβ_Glx‐Phevalues and Glx‐Phe trophic discrimination factors (TDF_Glx‐Phe).

   We show that variation inβ_Glx‐Phevalues is two times greater than previously considered, with degree of vascularization, not habitat type (terrestrial vs. aquatic), providing the greatest source of variability (vascular autotroph = −6.6 ± 3.4‰; non‐vascular autotroph = +3.3 ± 1.8‰). Within vascular plants, tissue type secondarily contributed toβ_Glx‐Phevalue variability, but we found no clear distinction among C₃, C₄and CAM plantβ_Glx‐Phevalues. Notably, we found that vascular plantβ_Glx‐Lysvalues (+2.5 ± 1.6‰) are considerably less variable thanβ_Glx‐Phevalues, making Lys a useful AA tracer of primary production sources in terrestrial systems. Our multi‐trophic level sensitivity analyses demonstrate that TP_CSIAestimates are highly sensitive to changes in bothβ_Glx‐Pheand TDF_Glx‐Phevalues but that the relative influence ofβvalues dissipates at higher trophic levels.

   Our results highlight that primary producerβvalues are integral to accurate trophic position estimation. We outline four key recommendations for identifying, constraining and accounting forβvalue variability to improve TP_CSIAestimation accuracy and precision moving forward. We must ultimately expand libraries of primary producer AA δ¹⁵N values to better understand the mechanistic drivers ofβvalue variation.

    

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2. Carbon and nitrogen isotope fractionation of amino acids in an avian marine predator, the gentoo penguin ( Pygoscelis papua )

   https://doi.org/10.1002/ece3.1437  

   McMahon, Kelton W. ; Polito, Michael J. ; Abel, Stephanie ; McCarthy, Matthew D. ; Thorrold, Simon R. ( February 2015 , Ecology and Evolution)

   Compound‐specific stable isotope analysis (CSIA) of amino acids (AA) has rapidly become a powerful tool in studies of food web architecture, resource use, and biogeochemical cycling. However, applications to avian ecology have been limited because no controlled studies have examined the patterns inAAisotope fractionation in birds. We conducted a controlledCSIAfeeding experiment on an avian species, the gentoo penguin (Pygoscelis papua), to examine patterns in individualAAcarbon and nitrogen stable isotope fractionation between diet (D) and consumer (C) (Δ¹³C_C‐Dand Δ¹⁵N_C‐D, respectively). We found that essentialAAδ¹³C values and sourceAAδ¹⁵N values in feathers showed minimal trophic fractionation between diet and consumer, providing independent but complimentary archival proxies for primary producers and nitrogen sources respectively, at the base of food webs supporting penguins. Variations in nonessentialAAΔ¹³C_C‐Dvalues reflected differences in macromolecule sources used for biosynthesis (e.g., protein vs. lipids) and provided a metric to assess resource utilization. The avian‐specific nitrogen trophic discrimination factor (TDF_Glu‐Phe= 3.5 ± 0.4‰) that we calculated from the difference in trophic fractionation (Δ¹⁵N_C‐D) of glutamic acid and phenylalanine was significantly lower than the conventional literature value of 7.6‰. Trophic positions of five species of wild penguins calculated using a multi‐TDF_Glu‐Pheequation with the avian‐specificTDF_Glu‐Phevalue from our experiment provided estimates that were more ecologically realistic than estimates using a singleTDF_Glu‐Pheof 7.6‰ from the previous literature. Our results provide a quantitative, mechanistic framework for the use ofCSIAin nonlethal, archival feathers to study the movement and foraging ecology of avian consumers.

    

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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)

   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. Seasonal dynamics of midwater zooplankton and relation to particle cycling in the North Pacific Subtropical Gyre

   https://doi.org/https://doi.org/10.1016/j.pocean.2020.102266  

   Hannides, CCS ; Popp, BN. ; Close, HG ; Benitez-Nelson, CR ; Ka’apu-Lyons, CA ; Gloeckler, K ; Wallsgrove, N ; Uhau, B ; Palmer, E ; Drazen, JC ( January 2020 , Progress in oceanography)

   Midwater zooplankton are major agents of biogeochemical transformation in the open ocean; however their characteristics and activity remain poorly known. Here we evaluate midwater zooplankton biomass, amino acid (AA)-specific stable isotope composition (δ15N values) using compound-specific isotope analysis of amino acids (CSIA-AA), trophic position, and elemental composition in the North Pacific Subtropical Gyre (NPSG). We focus on zooplankton collected in the winter, spring, and summer to evaluate midwater trophic dynamics over a seasonal cycle. For the first time we find that midwater zooplankton respond strongly to seasonal changes in production and export in the NPSG. In summer, when export from the euphotic zone is elevated and this ‘summer pulse’ material is transported rapidly to depth, CSIA-AA indicates that large particles (> 53 μm) dominate the food web base for zooplankton throughout the midwaters, and to a large extent even into the upper bathypelagic zone. In winter, when export is low, zooplankton in the mid-mesopelagic zone continue to rely on large particle basal resources, but resident zooplankton in the lower mesopelagic and upper bathypelagic zones switch to include smaller particles (0.7–53 μm) in their food web base, or even a subset of the small particle pool. Midwater zooplankton migration patterns also vary with season, with migrants distributed more evenly at night through the euphotic zone in summer as compared to being more compressed in the upper mixed layer in winter. Deeper zooplankton migration within the mesopelagic zone is also reduced in late summer, likely due to the increased magnitude of large particle material available at depth during this season. Our observed seasonal change in activity and trophic dynamics drives modestly greater biomass in summer than winter through the mesopelagic zone. In contrast midwater zooplankton carbon (C), nitrogen (N), and phosphorus (P) composition does not change with season. Instead we find increasing C:N, C:P, and N:P ratios with greater depths, likely due to decreases in proteinaceous structures and organic P compounds and increases in storage lipids with depth. Our study highlights the importance and diversity of feeding strategies for small zooplankton in NPSG midwaters. Many small zooplankton, such as oncaeid and oithonid copepods, are able to access small particle resources at depth and may be an important trophic link between the microbial loop and deep dwelling micronekton species that also rely on small particle-based food webs. Our observed midwater zooplankton trophic response to export-driven variation in the particle field at depth has important implications for midwater metabolism and the export of C to the deep sea. 

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5. Small particles and heterotrophic protists support the mesopelagic zooplankton food web in the subarctic northeast Pacific Ocean

   https://doi.org/10.1002/lno.12397  

   Shea, Connor H. ; Wojtal, Paul K. ; Close, Hilary G. ; Maas, Amy E. ; Stamieszkin, Karen ; Cope, Joseph S. ; Steinberg, Deborah K. ; Wallsgrove, Natalie ; Popp, Brian N. ( July 2023 , Limnology and Oceanography)

   A quantitative understanding of the mesopelagic zooplankton food web is key to development of accurate carbon budgets and geochemical models in marine systems. Here we use compound specific nitrogen stable isotope analysis of amino acids to quantify the trophic structure of the microzooplankton and mesozooplankton community during summer in the subarctic northeast Pacific Ocean during the EXport Processes in the Ocean from Remote Sensing (EXPORTS) field campaign. Source amino acid values in particles and zooplankton provide strong evidence that basal resources for the mesopelagic zooplankton food web were primarily small (), suspended or slow‐sinking particles, but that surface organic matter delivered by vertically migrating zooplankton may have also been important. Comparisons of values of source and trophic amino acids provide estimates of food web length, which decrease significantly with depth and suggest that protistan microzooplankton are key components of the food web from the surface to at least 500. These results emphasize the importance of small particles as a source of carbon and nitrogen to mesopelagic communities in this region, support observations of an inverse relationship between zooplankton vertical migration and small particles as sources of carbon to deep‐sea food webs in low productivity environments, and document the role of heterotrophic protists as key trophic intermediaries in the mesopelagic zone at this location.

    

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