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  1. 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 (δ13CAA) 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 (δ13CEAA) 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 ofδ13CAAfingerprints. A 10°C range in temperature conditions did not have significant impacts on variance inδ13CAAvalues or the diagnostic microalgalδ13CEAAfingerprints. Theseδ13CEAAfingerprints 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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  2. Abstract

    Compound‐specific stable isotope analysis of individual amino acids (CSIA‐AA) has emerged as a transformative approach to estimate consumer trophic positions (TPCSIA) that are internally indexed to primary producer nitrogen isotope baselines. Central to accurate TPCSIAestimation 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 TPCSIAuncertainty. 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 TPCSIAestimates to uncertainty in meanβGlx‐Phevalues and Glx‐Phe trophic discrimination factors (TDFGlx‐Phe).

    We show that variation inβGlx‐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 toβGlx‐Phevalue variability, but we found no clear distinction among C3, C4and CAM plantβGlx‐Phevalues. Notably, we found that vascular plantβGlx‐Lysvalues (+2.5 ± 1.6‰) are considerably less variable thanβGlx‐Phevalues, making Lys a useful AA tracer of primary production sources in terrestrial systems. Our multi‐trophic level sensitivity analyses demonstrate that TPCSIAestimates are highly sensitive to changes in bothβGlx‐Pheand TDFGlx‐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 TPCSIAestimation 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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  3. Pelagic-benthic coupling provides essential ecosystem functions, including energy transfer in surface and deep ocean food webs, regulation of biogeochemical cycling, and climate feed-back mechanisms. Despite its importance, access to long-term data sets of export production through different food web pathways are scarce. Therefore, to fill a critical data gap in our understanding of the patterns and drivers of variation in export production on ecologically relevant time scales, this study applied compound-specific stable nitrogen isotope analysis of amino acids to a 38 year (1981-2019) time series of pelagic copepod bioarchives (large-bodied Calanus finmarchicus and small-bodied Centropages typicus) and deep ocean bioarchives (deep-sea coral Primnoa resedaeformis) in the Gulf of Maine. Key metrics of food web dynamics that regulate export production were calculated including water nitrogen source, degree of heterotrophic microbial reworking on organic matter (∑V), and relative contribution to the trophic position of metazoan (TPGlx-Phe) and microbial (TPAla-Phe), all of which revealed strong pelagic-benthic coupling in both magnitude and temporal trend. As hypothesized, there was particularly strong agreement across all metrics between large-bodied C. finmarchicus and deep-sea P. resedaeformis, including a steady increase in the heterotrophic microbial reworking of exported production over time. The strong reliance of C. finmarchicus on microbial loop processes, including elevated TPAla-Phe transfers (4+/- 0.3) and a high level of ∑V (2.0 ± 0.5), was mirrored in P. resedaeformis, creating a direct mechanism to link surface microbial loop food web dynamics to the deep ocean through the biological pump. Identifying this strong microbial loop connectivity between the pelagic and benthic systems improves our understanding of Gulf of Maine export dynamics and our ability to better parameterize new mechanistic General Ecosystem Models. 
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  4. In southern New England, rapid ocean warming over the past two decades has caused substantial redistributions of fishes, invertebrates, and the fisheries they support. The rapid emergence of the warm water-tolerant Jonah crab (Cancer borealis) fishery, once discarded as bycatch from the now declining lobster fishery, illustrates a prime example of climate-adaptive shifts in southern New England fisheries. However, limited data exist on the basic life history of Jonah crabs, despite their growing economic and societal value. This hinders ocean management capacity to meet multiple ecological, economic, and socio-cultural goals of sustainable harvest. Off the southern coast of Rhode Island, Jonah crabs are currently harvested in two fishery zones (inshore and offshore) delineated as holdovers from the lobster management zones. Jonah crabs landed in the offshore fishing zone are significantly larger, on average, than those landed in the inshore fishing zone. This presentation gives an overview of a study developed to test the hypothesis that these size differences reflect ontogenetic migration of Jonah crabs from the inshore to offshore fishing zones. To do this, we developed seasonally resolved isoscapes (isotope maps) of the region, which revealed distinct geospatial gradients in environmental stable isotope values between inshore and offshore necessary to track potential movement of Jonah crabs between fishing zones. We then used stable isotope analysis of three Jonah crab tissues with differential metabolic turnover times: the carapace (reflecting residence one year ago), muscle (reflecting residence averaged over the last ~4 months), and hepatopancreas (reflecting residence averaged over the last ~4 weeks) to construct an “isotopic clock” of residence throughout the regional isoscapes. This work provides key data on critical life history characteristics of the Jonah crab through a collaborative effort by scientists at the University of Rhode Island and the Rhode Island Department of Environmental Management to inform management decisions on this emerging climate-adaptive fishery. 
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  5. The impacts of climate change are increasingly apparent in the physical oceanographic environment of the global ocean, with cascading effects through individual species to entire food webs. Despite their importance, these ecosystem effects can be challenging to quantify and track. One angle from which to analyse ecosystem linkages is via compound-specific stable isotope analysis of carbon and nitrogen focused on individual amino acids. These analyses can provide individual-level information (e.g., dietary sources, trophic position) as well as ecosystem-level information (e.g., variability in biogeochemical cycling at the base of the food web, nutrient regimes, food web structure). In this study, we analyzed C and N stable isotopes in archived scales of haddock (Melanogrammus aeglefinus) collected over almost a century from Georges Bank (northeast US) to investigate changes in the diet and trophic status of the haddock population driven by climate change. Specifically, we used nitrogen isotopes to identify secular changes in the input of warm slope waters to the Gulf of Maine over the time series. In contrast, carbon isotopes in essential amino acids suggest that there have been relatively small changes in the source of carbon fueling haddock biomass over the past 100 years and nitrogen isotopes indicate negligible changes in haddock trophic position despite major oceanographic and climatic changes over this time period. Overall, we demonstrate the application of cutting edge molecular isotope tools to a historical archive to examine food web architecture over time in a changing oceanographic environment. 
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  6. Nitrogen is a major limiting element for biological productivity, and thus understanding past variations in nitrogen cycling is central to understanding past and future ocean biogeochemical cycling, global climate cycles, and biodiversity. Organic nitrogen encapsulated in fossil biominerals is generally protected from alteration, making it an important archive of the marine nitrogen cycle on seasonal to million-year timescales. The isotopic composition of fossil-bound nitrogen reflects variations in the large-scale nitrogen inventory, local sources and processing, and ecological and physiological traits of organisms. The ability to measure trace amounts of fossil-bound nitrogen has expanded with recent method developments. In this article, we review the foundations and ground truthing for three important fossil-bound proxy types: diatoms, foraminifera, and corals. We highlight their utility with examples of high-resolution evidence for anthropogenic inputs of nitrogen to the oceans, glacial–interglacial-scale assessments of nitrogen inventory change, and evidence for enhanced CO 2 drawdown in the high-latitude ocean. Future directions include expanded method development, characterization of ecological and physiological variation, and exploration of extended timescales to push reconstructions further back in Earth's history. 
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