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Bulk and amino acid nitrogen isotopes suggest shifting nitrogen balance of pregnant sharks across gestation

  • Physiological ecology – original research
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Abstract

Nitrogen isotope (δ15N) analysis of bulk tissues and individual amino acids (AA) can be used to assess how consumers maintain nitrogen balance with broad implications for predicting individual fitness. For elasmobranchs, a ureotelic taxa thought to be constantly nitrogen limited, the isotopic effects associated with nitrogen-demanding events such as prolonged gestation remain unknown. Given the linkages between nitrogen isotope variation and consumer nitrogen balance, we used AA δ15N analysis of muscle and liver tissue collected from female bonnethead sharks (Sphyrna tiburo, n = 16) and their embryos (n = 14) to explore how nitrogen balance may vary across gestation. Gestational stage was a strong predictor of bulk tissue and AA δ15N values in pregnant shark tissues, decreasing as individuals neared parturition. This trend was observed in trophic (e.g., Glx, Ala, Val), source (e.g., Lys), and physiological (e.g., Gly) AAs. Several potential mechanisms may explain these results including nitrogen conservation, scavenging, and bacterially mediated breakdown of urea to free ammonia that is used to synthesize AAs. We observed contrasting patterns of isotopic discrimination in embryo tissues, which generally became enriched in 15N throughout development. This was attributed to greater excretion of nitrogenous waste in more developed embryos, and the role of physiologically sensitive AAs (i.e., Gly and Ser) to molecular processes such as nucleotide synthesis. These findings underscore how AA isotopes can quantify shifts in nitrogen balance, providing unequivocal evidence for the role of physiological condition in driving δ15N variation in both bulk tissues and individual AAs.

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Fig. 1

Source: The Northeast Gulf of Mexico, Google Earth, Accessed 27th May 2021

Fig. 2
Fig. 3

source amino acids (including Thr). Horizontal bars represent 95% (thin lines) and 75% (thick lines) confidence intervals for model coefficients

Fig. 4

source amino acids (Δ15NT-S) for muscle and liver tissue sampled from early-term (gray) and late-term (orange) female bonnethead sharks. Horizontal lines represent median values and large circles represent the mean, boxes display 25th and 75th percentiles and whiskers represent upper and lower quartiles ± 1.5*IQR, remaining points are outliers, and stars represent statistically significant differences as α = 0.05 level. Bottom panels: generalized linear model predictions illustrating the relationship between δ15N values of representative trophic and source amino acids and FLEmbryo for muscle (left four panels) and liver (right four panels). Best fit line and 95% CIs are shown for significant relationships at alpha = 0.05 level (see Table 2)

Fig. 5

source and physiological (middle panel), and threonine (right panel)

Fig. 6
Fig. 7

source pairs for bonnethead fertilized egg embryo tissues across: fertilized egg (n = 2), early-term (n = 4, whole body), mid-term (n = 4, liver), and late-term (n = 4, liver). b Linear regressions illustrating the relationship between average embryo length (cm) and whole body embryo (grey circles) and embryo liver tissue ( orange circles) trophic–source offsets normalized to fertilized egg (Δ15N-EmbryoTrophicAA-SourceAA—Δ15 N-EggTrophicAA-SourceAA). Vertical shaded blue region represents the length at which embryos typically transition from egg to placental resource use

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Data availability

Data will be uploaded to the only repository IsoBank (www.isobank.org) upon acceptance for publication.

References

  • Ballantyne JS (1997) Jaws: the inside story. The metabolism of elasmobranch fishes. Comp Biochem Physiol B: Biochem Mol Biol 118(4):703–742

    Article  Google Scholar 

  • Ballantyne JS (2016) Some of the most interesting things we know, and don't know, about the biochemistry and physiology of elasmobranch fishes (sharks, skates and rays). Comp Biochem Physiol B: Biochem Mol Biol 199:21–28

    Article  CAS  Google Scholar 

  • Baremore IE, Hale LF (2012) Reproduction of the sandbar shark in the western north Atlantic ocean and Gulf of Mexico. Mar Coast Fish: Dyn Manag Ecosyst Sci 4:560–572

    Article  Google Scholar 

  • Barnes C, Sweeting CJ, Jennings S, Barry JT, Polunin NV (2007) Effect of temperature and ration size on carbon and nitrogen stable isotope trophic fractionation. Funct Ecol 21(2):356–362

    Article  Google Scholar 

  • Bethea DM, Hale L, Carlson JK, Cortés E, Manire CA, Gelsleichter J (2007) Geographic and ontogenetic variation in the diet and daily ration of the bonnethead shark, Sphyrna tiburo, from the eastern Gulf of Mexico. Mar Biol 152(5):1009–1020

    Article  Google Scholar 

  • Bethea, D.M., G.A. Casselberry, J.K. Carlson, J. Hendon, R.D. Grubbs, C. Peterson, T.S. Daly-Engel, M.O. Pfleger, R. Hueter, J. Morris, J. Gardiner (2016) Shark nursery grounds and essential fish habitat studies. Gulfspan Gulf of Mexico-FY15. An Internal Report to NOAA Fisheries Highly Migratory Species Division. NMFS Panama City Laboratory Contribution No. PC-16/02.

  • Boecklen WJ, Yarnes CT, Cook BA, James AC (2011) On the use of stable isotopes in trophic ecology. Annu Rev Ecol Evol Syst 42:411–440

    Article  Google Scholar 

  • Borrell A, Gómez-Campos E, Aguilar A (2016) Influence of reproduction on stable-isotope ratios: nitrogen and carbon isotope discrimination between mothers, fetuses, and milk in the fin whale, a capital breeder. Physiol Biochem Zool 89(1):41–50

    Article  CAS  PubMed  Google Scholar 

  • Bryan HM, Darimont CT, Paquet PC, Wynne-Edwards KE, Smits JE (2013) Stress and reproductive hormones in grizzly bears reflect nutritional benefits and social consequences of a salmon foraging niche. PLoS ONE 8(11):e80537

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carlisle AB, Litvin SY, Madigan DJ, Lyons K, Bigman JS, Ibarra M, Bizzarro JJ (2017) Interactive effects of urea and lipid content confound stable isotope analysis in elasmobranch fishes. Can J Fish Aquat Sci 74(3):419–428

    Article  CAS  Google Scholar 

  • Carlson JK, Brusher JH (1999) An Index of Abundance for coastal species of Juvenile sharks from the northeast Gulf of Mexico. Mar Fish Rev 61(3):37–45

    Google Scholar 

  • Chua KW, Liew JH, Wilkinson CL, Ahmad AB, Tan HH, Yeo DC (2021) Land-use change erodes trophic redundancy in tropical forest streams: evidence from amino acid stable isotope analysis. J Anim Ecol 90(6):1433–1443

    Article  PubMed  Google Scholar 

  • Clark CT, Fleming AH, Calambokidis J, Kellar NM, Allen CD, Catelani KN, Harvey JT (2016) Heavy with child? Pregnancy status and stable isotope ratios as determined from biopsies of humpback whales. Conser Physiol 4(1):1–13

    Article  CAS  Google Scholar 

  • Conrath CL, Musick JA (2012) Reproductive biology of elasmobranchs. In: Biology of sharks and their relatives, vol 2, pp 291–311

  • Cortés E (2000) Life history patterns and correlations in sharks. Rev Fish Sci 8(4):299–344

    Article  Google Scholar 

  • Dagenais-Bellefeuille S, Morse D (2013) Putting the N in dinoflagellates. Front Microbiol 4:369

    Article  PubMed  PubMed Central  Google Scholar 

  • de Sousa Rangel B, Hammerschlag N, Sulikowski JA, Moreira RG (2021) Dietary and reproductive biomarkers in a generalist apex predator reveal differences in nutritional ecology across life stages. Mar Ecol Prog Ser 664:149–163

    Article  Google Scholar 

  • Delauney AJ, Hu CA, Kishor PB, Verma DP (1993) Cloning of ornithine delta-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J Biol Chem 268(25):18673–18678

    Article  CAS  PubMed  Google Scholar 

  • Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM, Harrison LR, White WT (2014) Extinction risk and conservation of the world’s sharks and rays. Elife 3:00590

    Article  Google Scholar 

  • Estrada JA, Rice AN, Natanson LJ, Skomal GB (2006) Use of isotopic analysis of vertebrae in reconstructing ontogenetic feeding ecology in white sharks. Ecology 87(4):829–834

    Article  PubMed  Google Scholar 

  • Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci 6(3):121–126

    Article  CAS  PubMed  Google Scholar 

  • Fleming AH, Kellar NM, Allen CD, Kurle CM (2018) The utility of combining stable isotope and hormone analyses for marine megafauna research. Front Mar Sci 5:338

    Article  Google Scholar 

  • Folch J (1957) A sample method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:479–500

    Article  Google Scholar 

  • Frisk MG, Miller TJ, Dulvy NK (2005) Life histories and vulnerability to exploitation of elasmobranchs: inferences from elasticity, perturbation and phylogenetic analyses. J Northwest Atl Fish Sci 35:27–45

    Article  Google Scholar 

  • Fuller BT, Fuller JL, Sage NE, Harris DA, O’Connell TC, Hedges RE (2004) Nitrogen balance and δ15N: why you’re not what you eat during pregnancy. Rapid Commun Mass Spectrom 18(23):2889–2896

    Article  CAS  PubMed  Google Scholar 

  • Fuller BT, Fuller JL, Sage NE, Harris DA, O’Connell TC, Hedges RE (2005) Nitrogen balance and δ15N: why you’re not what you eat during nutritional stress. Rapid Commun Mass Spectrom 19(18):2497–2506

    Article  CAS  PubMed  Google Scholar 

  • Gallagher AJ, Skubel RA, Pethybridge HR, Hammerschlag N (2017) Energy metabolism in mobile, wild-sampled sharks inferred by plasma lipids. Conserv Physiol. https://doi.org/10.1093/conphys/cox002

    Article  PubMed  PubMed Central  Google Scholar 

  • Galvan DE, Sweeting CJ, Reid WDK (2010) Power of stable isotope techniques to detect size-based feeding in marine fishes. Mar Ecol Prog Ser 407:271–278

    Article  Google Scholar 

  • Galvan DE, Jañez J, Irigoyen AJ (2016) Estimating tissue-specific discrimination factors and turnover rates of stable isotopes of nitrogen and carbon in the smallnose fanskate Sympterygia bonapartii (Rajidae). J Fish Biol 89(2):1258–1270

    Article  CAS  PubMed  Google Scholar 

  • Gannes LZ, Del Rio CM, Koch P (1998) Natural abundance variations in stable isotopes and their potential uses in animal physiological ecology. Comp Biochem Physiol a: Mol Integr Physiol 119(3):725–737

    Article  CAS  Google Scholar 

  • Gorokhova E (2018) Individual growth as a non-dietary determinant of the isotopic niche metrics. Methods Ecol Evol 9(2):269–277

    Article  Google Scholar 

  • Graves GR, Newsome SD, Willard DE, Grosshuesch DA, Wurzel WW, Fogel ML (2012) Nutritional stress and body condition in the Great Gray Owl (Strix nebulosa) during winter irruptive migrations. Can J Zool 90(7):787–797

    Article  CAS  Google Scholar 

  • Grimes DJ, Brayton P, Colwell RR, Gruber SH (1985) Vibrios as autochthonous flora of neritic sharks. Syst Appl Microbiol 6(2):221–226

    Article  Google Scholar 

  • Hamlett WC, Jones CJP, Paulesu LR (2005) Placentotrophy in sharks. In: Hamlett WC, Jamieson BGM (eds) Reproductive biology and phylogeny. Science publishers Inc., NH, pp 463–502

    Google Scholar 

  • Hammerschlag N, Skubel RA, Sulikowski J, Irschick DJ, Gallagher AJ (2018) A comparison of reproductive and energetic states in a marine apex predator (the tiger shark, Galeocerdo cuvier). Physiol Biochem Zool 91(4):933–942

    Article  PubMed  Google Scholar 

  • Hebert CE, Popp BN, Fernie KJ, Ka’apu-Lyons C, Rattner BA, Wallsgrove N (2016) Amino acid specific stable nitrogen isotope values in avian tissues: insights from captive American kestrels and wild herring gulls. Environ Sci Technol 50(23):12928-12937

  • Hobson KA, Alisauskas RT, Clark RG (1993) Stable-nitrogen isotope enrichment in avian tissues due to fasting and nutritional stress: implications for isotopic analyses of diet. The Condor 95(2):388–394

    Article  Google Scholar 

  • Hussey NE, Olin JA, Kinney MJ, McMeans BC, Fisk AT (2012) Lipid extraction effects on stable isotope values (δ13C and δ15N) of elasmobranch muscle tissue. J Exp Mar Biol Ecol 434:7–15

    Article  CAS  Google Scholar 

  • Kajimura M, Walsh PJ, Wood CM (2008) The spiny dogfish Squalus acanthias L. maintains osmolyte balance during long-term starvation. J Fish Biol 72(3):656–670

    Article  CAS  Google Scholar 

  • Kalhan SC (2016) One carbon metabolism in pregnancy: Impact on maternal, fetal and neonatal health. Mol Cell Endocrinol 435:48–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim SL, Martínez del Rio C, Casper D, Koch PL (2012) Isotopic incorporation rates for shark tissues from a long-term captive feeding study. J Exp Biol 215:2495–2500

    Article  PubMed  Google Scholar 

  • King JC (2000) Physiology of pregnancy and nutrient metabolism. Am J Clin Nutr 71(5):1218S-1225S

    Article  CAS  PubMed  Google Scholar 

  • Kishor PK, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao KRSS, Sreenath Rao, Reddy KJ, Theriappan P, Sreenivasulu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438

  • Knight IT, Grimes DJ, Colwell RR (1988) Bacterial hydrolysis of urea in the tissues of carcharhinid sharks. Can J Fish Aquat Sci 45(2):357–360

    Article  CAS  Google Scholar 

  • Kounig B, Riester J, Markl H (1988) Maternal care in house mice (Mus musculus) II. The energy cost of lactation as a function of litter size. J Zool 216(2):195–210

    Article  Google Scholar 

  • Kouwenberg AL, Mark Hipfner J, McKay DW, Storey AE (2013) Corticosterone and stable isotopes in feathers predict egg size in A tlantic P uffins F ratercula arctica. Ibis 155(2):413–418

    Article  Google Scholar 

  • Larsen T, Taylor DL, Leigh MB, O’Brien DM (2009) Stable isotope fingerprinting: a novel method for identifying plant, fungal, or bacterial origins of amino acids. Ecology 90(12):3526–3535

    Article  PubMed  Google Scholar 

  • Laxson CJ, Condon NE, Drazen JC, Yancey PH (2011) Decreasing urea∶ trimethylamine N-oxide ratios with depth in chondrichthyes: a physiological depth limit? Physiol Biochem Zool 84(5):494–505

    Article  CAS  PubMed  Google Scholar 

  • Layman CA, Araujo MS, Boucek R, Hammerschlag-Peyer CM, Harrison E, Jud ZR, Bearhop S (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev 87(3):545–562

    Article  PubMed  Google Scholar 

  • Lee TN, Buck CL, Barnes BM, O’Brien DM (2012) A test of alternative models for increased tissue nitrogen isotope ratios during fasting in hibernating arctic ground squirrels. J Exp Biol 215(19):3354–3361

    CAS  PubMed  Google Scholar 

  • Leigh SC, Papastamatiou YP, German DP (2018) Seagrass digestion by a notorious “carnivore.” Proc R Soc B 285:20181583

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leon M, Woodside B (1983) Energetic limits on reproduction: maternal food intake. Physiol Behav 30(6):945–957

    Article  CAS  PubMed  Google Scholar 

  • Lindsay KL, Hellmuth C, Uhl O, Buss C, Wadhwa PD, Koletzko B, Entringer S (2015) Longitudinal metabolomic profiling of amino acids and lipids across healthy pregnancy. PLoS ONE 10(12):e0145794

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lübcker N, Whiteman JP, Millar RP, de Bruyn PN, Newsome SD (2020) Fasting affects amino acid nitrogen isotope values: a new tool for identifying nitrogen balance of free-ranging mammals. Oecologia 193(1):53–65

    Article  PubMed  Google Scholar 

  • Lübcker N, Whiteman JP, Newsome SD, Millar RP, de Bruyn PN (2020) Can the carbon and nitrogen isotope values of offspring be used as a proxy for their mother’s diet? Using foetal physiology to interpret bulk tissue and amino acid δ15N values. Conserv Physiol. https://doi.org/10.1093/conphys/coaa060

    Article  PubMed  PubMed Central  Google Scholar 

  • MacNeil MA, Drouillard KG, Fisk AT (2006) Variable uptake and elimination of stable nitrogen isotopes between tissues in fish. Can J Fish Aquat Sci 63(2):345–353

    Article  CAS  Google Scholar 

  • Matich P, Kiszka JJ, Heithaus MR, Le Bourg B, Mourier J (2019) Inter-individual differences in ontogenetic trophic shifts among three marine predators. Oecologia 189(3):621–636

    Article  PubMed  Google Scholar 

  • Matich P, Shipley ON, Wiedeli O (2021) Quantifying spatial variation in isotopic baselines reveals size-based feeding in a model estuarine predator: implications for trophic studies in dynamic ecotones. Mar Biol. https://doi.org/10.1007/s00227-021-03920-0

    Article  Google Scholar 

  • McConnaughey T, McRoy CP (1979) Food-web structure and the fractionation of carbon isotopes in the Bering Sea. Mar Biol 53(3):257–262

    Article  CAS  Google Scholar 

  • McMahon KW, McCarthy MD (2016) Embracing variability in amino acid δ15N fractionation: mechanisms, implications, and applications for trophic ecology. Ecosphere 7(12):e01511

    Article  Google Scholar 

  • McMahon KW, Thorrold SR, Elsdon TS, McCarthy MD (2015) Trophic discrimination of nitrogen stable isotopes in amino acids varies with diet quality in a marine fish. Limnol Oceanogr 60(3):1076–1087

    Article  CAS  Google Scholar 

  • McMeans BC, Olin JA, Benz GW (2009) Stable-isotope comparisons between embryos and mothers of a placentatrophic shark species. J Fish Biol 75(10):2464–2474

    Article  CAS  PubMed  Google Scholar 

  • Narkewicz MR, Jones G, Thompson H, Kolhouse F, Fennessey PV (2002) Folate cofactors regulate serine metabolism in fetal ovine hepatocytes. Pediatr Res 52(4):589–594

    Article  CAS  PubMed  Google Scholar 

  • Nielsen JM, Popp BN, Winder M (2015) Meta-analysis of amino acid stable nitrogen isotope ratios for estimating trophic position in marine organisms. Oecologia 178(3):631–642

    Article  PubMed  Google Scholar 

  • O’Connell T (2017) ‘Trophic’and ‘source’amino acids in trophic estimation: a likely metabolic explanation. Oecologia 184(2):317–326

    Article  PubMed  PubMed Central  Google Scholar 

  • Ohkouchi N, Chikaraishi Y, Close HG, Fry B, Larsen T, Madigan DJ, Yokoyama Y (2017) Advances in the application of amino acid nitrogen isotopic analysis in ecological and biogeochemical studies. Org Geochem 113:150–174

    Article  CAS  Google Scholar 

  • Olin JA, Hussey NE, Fritts M, Heupel MR, Simpfendorfer CA, Poulakis GR, Fisk AT (2011) Maternal meddling in neonatal sharks: implications for interpreting stable isotopes in young animals. Rapid Commun Mass Spectrom 25(8):1008–1016

    Article  CAS  PubMed  Google Scholar 

  • Olin JA, Shipley ON, McMeans BC (2018) Stable isotope fractionation between maternal and embryo tissues in the Bonnethead shark (Sphyrna tiburo). Environ Biol Fishes 101(3):489–499

    Article  Google Scholar 

  • Pastor-Anglada M, Remesar X (1986) Urinary amino acid excretion in the pregnant rat. Nutr Res 6(6):709–718

    Article  CAS  Google Scholar 

  • Ruiz-Cooley RI, Gerrodette T, Fiedler PC, Chivers SJ, Danil K, Ballance LT (2017) Temporal variation in pelagic food chain length in response to environmental change. Sci Adv 3(10):1701140

    Article  CAS  Google Scholar 

  • Schlernitzauer DA, Gilbert PW (1966) Placentation and associated aspects of gestation in the bonnethead shark, Sphyrna tiburo. J Morphol 120(3):219–231

    Article  CAS  PubMed  Google Scholar 

  • Silfer JA, Engel MH, Macko SA, Jumeau EJ (1991) Stable carbon isotope analysis of amino acid enantiomers by conventional isotope ratio mass spectrometry and combined gas chromatography/isotope ratio mass spectrometry. Anal Chem 63(4):370–374

    Article  CAS  Google Scholar 

  • Shipley ON, Matich P (2020) Studying animal niches using bulk stable isotope ratios: an updated synthesis. Oecologia 193:27–51

    Article  PubMed  Google Scholar 

  • Shipley ON, Olin JA, Polunin NV, Sweeting CJ, Newman SP, Brooks EJ, Hussey NE (2017) Polar compounds preclude mathematical lipid correction of carbon stable isotopes in deep-water sharks. J Exp Mar Biol Ecol 494:69–74

    Article  CAS  Google Scholar 

  • Shipley ON, Brooks EJ, Madigan DJ, Sweeting CJ, Grubbs RD (2017) Stable isotope analysis in deep-sea chondrichthyans: recent challenges, ecological insights, and future directions. Rev Fish Biol Fisheries 27(3):481–497

    Article  Google Scholar 

  • Shipley ON, Newton AL, Frisk MG, Henkes GA, LaBelle JS, Camhi MD, Olin JA (2021) Telemetry-validated nitrogen stable isotope clocks identify ocean-to-estuarine habitat shifts in mobile organisms. Methods Ecol Evol 12(5):897–908

    Article  Google Scholar 

  • Skinner C, Mill AC, Fox MD, Newman SP, Zhu Y, Kuhl A, Polunin NVC (2021) Offshore pelagic subsidies dominate carbon inputs to coral reef predators. Sci Adv 7(8):eabf3792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith HW (1936) The retention and physiological role of urea in the Elasmobranchii. Biol Rev 11(1):49–82

    Article  CAS  Google Scholar 

  • Smith HW, James PB, Herbert S (1929) The composition of the body fluids of elasmobranchs. J Biol Chem 81(2):407–419

    Article  CAS  Google Scholar 

  • Sponheimer M, Robinson T, Ayliffe L, Roeder B, Hammer J, Passey B, Ehleringer J (2003) Nitrogen isotopes in mammalian herbivores: hair δ15N values from a controlled feeding study. Int J Osteoarchaeol 13(1–2):80–87

    Article  Google Scholar 

  • Stein RW, Mull CG, Kuhn TS, Aschliman NC, Davidson LN, Joy JB, Smith GJ, Dulvy NK, Mooers AO (2018) Global priorities for conserving the evolutionary history of sharks, rays and chimaeras. Nat Ecol Evol 2(2):288–298

    Article  PubMed  Google Scholar 

  • Sweeting CJ, Polunin NVC, Jennings S (2006) Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Commun Mass Spectrom 20(4):595–601

    Article  CAS  PubMed  Google Scholar 

  • Tieszen LL, Boutton TW, Tesdahl KG, Slade NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57(1–2):32–37

    Article  CAS  PubMed  Google Scholar 

  • Whiteman JP, Kim SL, McMahon KW, Koch PL, Newsome SD (2018) Amino acid isotope discrimination factors for a carnivore: physiological insights from leopard sharks and their diet. Oecologia 188(4):977–989

    Article  PubMed  Google Scholar 

  • Whiteman JP, Elliott Smith EA, Besser AC, Newsome SD (2019) A guide to using compound-specific stable isotope analysis to study the fates of molecules in organisms and ecosystems. Diversity 11(1):8

    Article  CAS  Google Scholar 

  • Whiteman JP, Newsome SD, Bustamante P, Cherel Y, Hobson KA (2021) Quantifying capital versus income breeding: new promise with stable isotope measurements of individual amino acids. J Anim Ecol 90(6):1408–1418

    Article  PubMed  Google Scholar 

  • Whiteman JP, Rodriguez Curras M, Feeser KL, Newsome SD (2021) Dietary protein content and digestibility influences discrimination of amino acid nitrogen isotope values in a terrestrial omnivorous mammal. Rapid Commun Mass Spectrom 35(11):e9073

    Article  CAS  PubMed  Google Scholar 

  • Widdowson EM (1976) The response of the sexes to nutritional stress. Proc Nutr Soc 35(2):175–180

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Giacomin M (2016) Feeding through your gills and turning a toxicant into a resource: how the dogfish shark scavenges ammonia from its environment. J Exp Biol 219(20):3218–3226

    Article  PubMed  Google Scholar 

  • Wood CM, Pärt P, Wright PA (1995) Ammonia and urea metabolism in relation to gill function and acid-base balance in a marine elasmobranch, the spiny dogfish (Squalus acanthias). J Exp Biol 198(7):1545–1558

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Liew HJ, De Boeck G, Hoogenboom JL, Anderson WG (2019) Nitrogen handling in the elasmobranch gut: a role for microbial urease. J Exp Biol 222(3):jeb194787

    PubMed  Google Scholar 

  • Wright PA (1995) Nitrogen excretion: three end products, many physiological roles. J Exp Biol 198(2):273–281

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Ott TL, Knabe DA, Bazer FW (1999) Amino acid composition of the fetal pig. J Nutr 129(5):1031–1038

    Article  CAS  PubMed  Google Scholar 

  • Wu G, Bazer FW, Burghardt RC, Johnson GA, Kim SW, Knabe DA, Spencer TE (2010) Functional amino acids in swine nutrition and production. Dyn Anim Nutr 69:98

    Google Scholar 

  • Wu G, Bazer FW, Burghardt RC, Johnson GA, Kim SW, Knabe DA, Spencer TE (2011) Proline and hydroxyproline metabolism: implications for animal and human nutrition. Amino Acids 40(4):1053–1063

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Becker D (2015) Connecting proline metabolism and signaling pathways in plant senescence. Front Plant Sci 6:552

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors would like to thank S. Farr, P. Manlick, N. Lübcker, G. Busquets-Vass, L. Burkemper, and V. Atudorei for laboratory assistance. We are grateful to the NOAA Fisheries Panama City Laboratory Shark Population Assessment Group, especially B. Burleson, G. Casselberry, J. Clayton, D. DeLorenzo, S. Dunnigan, E. Heikkinen, P. Higginson, R. Jones, C. Larash, B. Meath, A. Mowle, A. Pacicco, R. Peters, C. Rewis, and H. Wood for volunteering time to help collect and process samples in the field and laboratory. We are also grateful for the input received from anonymous reviewers that greatly improved the manuscript.

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Authors and Affiliations

  1. Department of Biology, University of New Mexico, Albuquerque, NM, 87131, USA

    Oliver N. Shipley & Seth D. Newsome

  2. Biological Sciences, Great Lakes Research Center, Michigan Technological University, Houghton, MI, 49931, USA

    Jill A. Olin

  3. Department of Biological Sciences, Old Dominion University, Norfolk, VA, 23529, USA

    John P. Whiteman

  4. NOAA Fisheries Southeast Regional Office, Saint Petersburg, FL, 33701, USA

    Dana M. Bethea

  5. Beneath the Waves, PO Box 126, Herndon, VA, 20172, USA

    Oliver N. Shipley

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Contributions

ONS, JAO, JPW, and SDN conceived the project ideas and designed the methodology. JAO and DB conducted fieldwork and collected samples. ONS and SDN conducted laboratory analyses and analyzed the data. ONS led the writing of the manuscript with significant input from all authors. All authors approved the final version of the manuscript.

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Correspondence to Oliver N. Shipley.

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Communicated by Donovan P German.

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Shipley, O.N., Olin, J.A., Whiteman, J.P. et al. Bulk and amino acid nitrogen isotopes suggest shifting nitrogen balance of pregnant sharks across gestation. Oecologia 199, 313–328 (2022). https://doi.org/10.1007/s00442-022-05197-6

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