Compound-Specific Stable Isotope Analysis of Amino Acids in Pelagic Shark Vertebrae Reveals Baseline, Trophic, and Physiological Effects on Bulk Protein Isotope Records

Sarah Magozzi,Miguel N Santos,Leah Houghton,Stuart Hetherington,Simon R Thorrold,Clive N Trueman,Lisa J Natanson,Gonzalo Mucientes,Nuno Queiroz,Victoria A Bendall

doi:10.3389/fmars.2021.673016

Abstract

Variations in stable carbon and nitrogen isotope compositions in incremental tissues of pelagic sharks can be used to infer aspects of their spatial and trophic ecology across life-histories. Interpretations from bulk tissue isotopic compositions are complicated, however, because multiple processes influence these values, including variations in primary producer isotope ratios and consumer diets and physiological processing of metabolites. Here we challenge inferences about shark tropho-spatial ecology drawn from bulk tissue isotope data using data for amino acids. Stable isotope compositions of individual amino acids can partition the isotopic variance in bulk tissue into components associated with primary production on the one hand, and diet and physiology on the other. The carbon framework of essential amino acids (EAAs) can be synthesised de novo only by plants, fungi and bacteria and must be acquired by consumers through the diet. Consequently, the carbon isotopic composition of EAAs in consumers reflects that of primary producers in the location of feeding, whereas that of non-essential amino acids (non-EAAs) is additionally influenced by trophic fractionation and isotope dynamics of metabolic processing. We determined isotope chronologies from vertebrae of individual blue sharks and porbeagles from the North Atlantic. We measured carbon and nitrogen isotope compositions in bulk collagen and carbon isotope compositions of amino acids. Despite variability among individuals, common ontogenetic patterns in bulk isotope compositions were seen in both species. However, while life-history movement inferences from bulk analyses for blue sharks were supported by carbon isotope data from essential amino acids, inferences for porbeagles were not, implying that the observed trends in bulk protein isotope compositions in porbeagles have a trophic or physiological explanation, or are suprious effects. We explored variations in carbon isotope compositions of non-essential amino acids, searching for systematic variations that might imply ontogenetic changes in physiological processing, but patterns were highly variable and did not explain variance in bulk protein δ13C values. Isotopic effects associated with metabolite processing may overwhelm spatial influences that are weak or inconsistently developed in bulk tissue isotope values, but interpreting mechanisms underpinning isotopic variation in patterns in non-essential amino acids remains challenging.

Highlights

Pelagic shark populations have declined regionally by >90% in the past 20 years, largely as a result of overfishing and bycatch (Worm et al, 2013), while the global abundance of oceanic sharks has declined by 70% since 1970 (Pacoureau et al, 2021)
If ontogenetic patterns in bulk protein δ13C values are matched by variability in δ13C values of essential amino acids, at least a component of variance in the bulk protein signal must be associated with movement across isotopically distinct baselines
We investigated patterns in δ13C values of non-essential amino acids, isotopic spacing between glycolytic and Krebs cycle amino acids, to explore whether systematic variations in nutrient physiology could be encoded in the bulk or amino acid isotope values

Summary

Introduction

Pelagic shark populations have declined regionally by >90% in the past 20 years, largely as a result of overfishing and bycatch (Worm et al, 2013), while the global abundance of oceanic sharks has declined by 70% since 1970 (Pacoureau et al, 2021). Effective management of the remaining shark populations requires a thorough understanding of their spatial ecology (Costa et al, 2012; Briscoe et al, 2016). Movements of pelagic sharks are, difficult to monitor or reconstruct, throughout ontogeny (Graham et al, 2010; Trueman et al, 2012; McMahon et al, 2013). While physical tags have revolutionized our understanding of space use by pelagic fishes, they rarely report over the life-time of a tagged individual, and juvenile animals may be too small to support satellite-linked pop-up tags. Knowledge of juvenile movements, and connections between juvenile and adult habitats, remain poorly understood for many pelagic shark species

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