Abstract
Evaluating tissue fractionation between mothers and their offspring is fundamental for informing our interpretation of stable isotope values in young individuals and can provide insight into the dynamics of maternal provisioning. The objectives of this study were to investigate the isotopic relationships between maternal reproductive (i.e., yolk, yolk-sac placenta) and somatic tissues (i.e., muscle and liver) relative to embryos in the Bonnethead Shark Sphyrna tiburo, to evaluate the fractionation of stable carbon (δ13C) and nitrogen (δ15N) isotopes between these tissues. Additionally, we examined intra-uterine variability in the isotopic relationships to ascertain whether this species may exhibit variable nutrient allocation. Embryos showed similar magnitudes of enrichment in 13C (i.e., Δδ13C, difference between adult and embryo) relative to adult tissues (Δδ13C = ~1.0‰). However, embryos were depleted in 15N relative to adult muscle tissues (Δδ15N = −1.0‰), a finding that contrasts Δδ15N values reported for other placentotrophic sharks. Embryo-muscle Δδ15N was correlated with length, supporting the contention that the magnitude of enrichment between embryonic and maternal tissues results from the shift from yolk to placental feeding. Embryo δ15N and Δδ15N values showed significant intra-uterine variability; a result not observed for δ13C and Δδ13C values. The contrasting patterns in fractionation among placentotrophic sharks highlight the importance of evaluating these relationships across elasmobranch taxa with consideration for different tissues, reproductive strategies and stages of gestation. The divergent findings support future evaluation of stable isotope relationships between mothers and offspring for purposes of estimating inherent isotopic variability and how this variability may inform physiological and dietary mechanisms.
Similar content being viewed by others
References
Barnes C, Jennings S, Polunin NVC, Lancaster JE (2008) The importance of quantifying inherent variability when interpreting stable isotope field data. Oecologia 155(2):227–235. https://doi.org/10.1007/s00442-007-0904-y
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Physiol Pharmacol 37:911–917
Dalerum F, Angerbjörn A (2005) Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144(4):647–658. https://doi.org/10.1007/s00442-005-0118-0
DeNiro MJ, Epstein S (1977) Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197(4300):261–263. https://doi.org/10.1126/science.327543
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42(5):495–506. https://doi.org/10.1016/0016-7037(78)90199-0
DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:343–351
Doucett RR, Hooper W, Power G (1999) Identification of anadromous and non-anadromous adult brook trout and their progeny in the Tabusintac River, New Brunswick, by means of multiple-stable-isotope analysis. Trans Am Fish Soc 128(2):278–288.
Frankel NS, Vander Zanden HB, Reich KJ, Williams KL, Bjorndal KA (2012) Mother-offspring stable isotope discrimination in loggerhead sea turtles Caretta caretta. Endanger Species Res 17(2):133–138. https://doi.org/10.3354/esr00412
Gannes LZ, O’Brien DM, Martínez del Rio C (1997) Stable isotopes in animal ecology: assumptions, caveats and a call for more laboratory experiments. Ecology 78(4):1271–1276.
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
Hobson KA (1995) Reconstructing avian diets using stable-carbon and nitrogen isotope analysis of egg components: patterns of isotopic fractionation and turnover. Condor 97(3):752–762. https://doi.org/10.2307/1369183
Hobson KA, Atwell L, Wassenaar LI, Yerkes T (2004) Estimating endogenous nutrient allocations to reproduction in redhead ducks: a dual isotope approach using δD and δ13C measurements of female and egg tissues. Funct Ecol 18(5):737–745. https://doi.org/10.1111/j.0269-8463.2004.00890.x
Hobson KA, Thompson JE, Evans MR, Boyd S (2005) Tracing nutrient allocation to reproduction in Barrow's goldeneye. J Wildl Manag 69(3):1221–1228.
Hussey NE, Wintner SP, Dudley SFJ, Cliff G, Cocks DT, MacNeil MA (2010) Maternal investment and size-specific reproductive output in carcharhinid sharks. J Anim Ecol 79(1):184–193. https://doi.org/10.1111/j.1365-2656.2009.01623.x
Hussey NE, MacNeil MA, Olin JA, McMeans BC, Kinney MJ, Chapman DD, Fisk AT (2012a) Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions. J Fish Biol 80(5):1449–1484. https://doi.org/10.1111/j.1095-8649.2012.03251.x
Hussey NE, Olin JA, Kinney MJ, McMeans BC, Fisk AT (2012b) Lipid extraction effects on stable isotope values (δ13C and δ15N) of elasmobranch muscle tissue. J Exp Mar Biol Ecol 434-435:7–15. https://doi.org/10.1016/j.jembe.2012.07.012
Jardine TD, Chernoff E, Curry RA (2008) Maternal transfer of carbon and nitrogen to progeny of sea-run and resident brook trout (Salvelinus fontinalis). Can J Fish Aquat Sci 65(10):2201–2210. https://doi.org/10.1139/F08-132
Le Bourg B, Kiska J, Bustamante P (2014) Mother-embryo isotope (δ15N, δ13C) fractionation and mercury (hg) transfer in aplacental deep-sea sharks. J Fish Biol 84(5):1574–1581. https://doi.org/10.1111/jfb.12357
Lyons K, Lowe CG (2013) Mechanisms of maternal transfer of organochlorine contaminants and mercury in the common thresher shark (Alopias vulpinus). Can J Fish Aquat Sci 70(12):1667–1672. https://doi.org/10.1139/cjfas-2013-0222
MacNeil MA, Skomal GB, Fisk AT (2005) Stable isotopes from multiple tissues reveal diet switching in sharks. Mar Ecol Prog Ser 302:190–206
Manire CA, Rasmussen LEL, Hess DL, Hueter RE (1995) Serum steroid hormones and the reproductive cycle of the female Bonnethead shark, Sphyrna tiburo. Gen Comp Endocrinol 97(3):366–376. https://doi.org/10.1006/gcen.1995.1036
Manire CA, Rasmussen LEL, Gelsleichter J, Hess DL (2004) Maternal serum and yolk hormone concentrations in the placental viviparous Bonnethead shark, Sphyrna tiburo. Gen Comp Endocrinol 136(2):241–247. https://doi.org/10.1016/j.ygcen.2003.12.018
Marsh-Matthews E, Brooks M, Deaton R, Tan H (2005) Effects of maternal and embryo characteristics on post-fertilization provisioning in fishes of the genus Gambusia. Oecologia 144(1):12–24. https://doi.org/10.1007/s00442-005-0030-7
Martínez del Rio C, Wolf N, Carleton SA, Gannes Z (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84(1):91–111. https://doi.org/10.1111/j.1469-185X.2008.00064.x
Matich P, Kiszka JJ, Heithaus MR, Mourier J, Planes S (2015) Short-term shifts of stable isotope (δ13C, δ15N) values in juvenile sharks within nursery areas suggest rapid shifts in energy pathways. J Exp Mar Biol Ecol 465:83–91. https://doi.org/10.1016/j.jembe.2015.01.012
McCarthy ID, Waldron S (2000) Identifying migratory Salmo trutta using carbon and nitrogen stable isotope ratios. Rapid Commun Mass Spectrom 14(15):1325–1331.
McMeans BC, Olin JA, Benz GW (2009) Stable-isotope comparisons between embryos and mothers of a placentotrophic shark species. J Fish Biol 75(10):2464–2474. https://doi.org/10.1111/j.1095-8649.2009.02402.x
Minagawa M, Wada E (1984) Stepwise enrichment of δ15N along food chains: further evidence and the relation between 15N and animal age. Geochim Cosmochim Acta 48(5):1135–1140. https://doi.org/10.1016/0016-7037(84)90204-7
Murchie KJ, Power M (2004) Growth- and feeding-related isotopic dilution and enrichment patterns in young-of-the-year yellow perch (Perca flavescens). Freshw Biol 49(1):41–54. https://doi.org/10.1046/j.1365-2426.2003.01163.x
Needham J (1942) Biochemistry and morphogenesis. Cambridge University press, Cambridge p.785
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. https://doi.org/10.1002/rcm.4946
Olin JA, Hussey NE, Grgicak-Mannion A, Fritts MW, Wintner SP, Fisk AT (2013) Variable δ15N diet-tissue discrimination factors among sharks: implications for trophic position, diet and food web models. PLoS One 8(10):e77567. https://doi.org/10.1371/journal.pone.0077567
Parsons GR (1993) Age determination and growth of the Bonnethead shark Sphyrna tiburo: a comparison of two populations. Mar Biol 117(1):23–31. https://doi.org/10.1007/BF00346422
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18(1):293–320. https://doi.org/10.1146/annurev.es.18.110187.001453
Pinnegar JK, Polunin NVC (1999) Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Funct Ecol 13(2):225–231. https://doi.org/10.1046/j.1365-2435.1999.00301.x
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83(3):703–718.
Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña G (2007) Getting to the fat of the matter: models, methods, and assumptions for dealing with lipids and stable isotope analysis. Oecologia 152(1):179–189. https://doi.org/10.1007/s00442-006-0630-x
R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Robbins CT, Felicetti LA, Florin ST (2010) The impact of protein quality on stable nitrogen isotope ratio discrimination and assimilated diet estimation. Oecologia 162(3):571–579. https://doi.org/10.1007/s00442-009-1485-8
Schlernitzauer DA, Gilbert PW (1966) Placentation and associated aspects of gestation in the Bonnethead shark, Sphyrna tiburo. J Morphol 120(3):219–231. https://doi.org/10.1002/jmor.1051200302
Vander Zanden MJ, Hulshof M (1998) Application of stable isotope techniques to trophic studies of age-0 smallmouth bass. Trans Am Fish Soc 127(5):729–739.
Vaudo JJ, Matich P, Heithaus MR (2010) Mother–offspring isotope fractionation in two species of placentatrophic sharks. J Fish Biol 77(7):1724-1727
Williams G (1966) Natural selection, the costs of reproduction and a refinement of Lack’s principal. Am Nat 100(916):687–690. https://doi.org/10.1086/282461
Witting DA, Chambers RC, Bosley KL, Wainright SC (2004) Experimental evaluation of ontogenetic diet transitions in summer flounder (Paralichthys dentatus), using stable isotopes as diet tracers. Can J Fish Aquat Sci 61(11):2069–2084. https://doi.org/10.1139/f04-156
Acknowledgements
The authors thank M. Heupel, J. Morris, C. Simpfendorfer, T. Wiley and B. Yeiser, and the many volunteer interns from Mote Marine Laboratory (MML) for their assistance with field efforts for this project. We are grateful to S. Ellis and S. Holland for assistance in processing these samples in the laboratory and to A. Fisk and N. Hussey for discussions on earlier drafts of this manuscript. We are grateful for the comments provided by an anonymous reviewer. This research was funded through a University of Windsor scholarship to J. Olin and an NSERC Discovery grant to A. Fisk.
Author information
Authors and Affiliations
Contributions
JAO, BCM initiated the study; JAO, ONS performed the statistical analysis; JAO wrote the first draft of the manuscript and ONS, BCM substantially contributed to revision.
Corresponding author
Rights and permissions
About this article
Cite this article
Olin, J.A., Shipley, O.N. & McMeans, B.C. Stable isotope fractionation between maternal and embryo tissues in the Bonnethead shark (Sphyrna tiburo). Environ Biol Fish 101, 489–499 (2018). https://doi.org/10.1007/s10641-018-0715-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-018-0715-5