Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Muscle and carapace tissue–diet isotope discrimination factors for the freshwater crayfish Cherax destructor

Debashish Mazumder A C , Mathew P. Johansen A , Brian Fry B and Emma Davis A
+ Author Affiliations
- Author Affiliations

A Australian Nuclear Science and Technology Organisation, Locked Bag 2001, Kirrawee DC, NSW 2232, Australia.

B Australian Rivers Institute, Griffith University, 170 Kessels Road, Brisbane, Qld 4111, Australia.

C Corresponding author. Email: debashish.mazumder@ansto.gov.au

Marine and Freshwater Research - https://doi.org/10.1071/MF16360
Submitted: 24 October 2016  Accepted: 14 July 2017   Published online: 8 September 2017

Abstract

This study examined a range of diets and two tissue types (muscle and carapace, representing protein and chitin biochemistry respectively) of Cherax destructor (Clark, 1936) to allow more accurate use of isotope data in trophic source estimates. The resulting Δ13Ctissue–diet and Δ15Ntissue–diet discrimination factors of muscle and carapace tissues showed significant differences among diets. For muscle, Δ13Ctissue–diet was higher (2.11–2.33‰) when C. destructor was fed with lamb, turkey and mixed animal and plant-based diets, 1.27–1.96‰ when C. destructor was fed with beef and kangaroo diets and negative (–1.36‰) when C. destructor was fed with an aquatic meat (tuna) diet. The Δ15Ntissue–diet discrimination factors were lower for muscle when C. destructor was fed aquatic meat (0.12‰) and mixed plant–animal diets (1.67‰), but higher for terrestrial meat diets (2.79–3.74‰). The Δ13Ctissue–diet for carapace followed similar patterns to that of muscle, but Δ15Ntissue–diet values were lower for carapace than muscle. Strong correlations were observed between muscle and carapace for δ13C (r = 0.96, P < 0.0001) and δ15N (r = 0.82, P < 0.0012) across the six diets evaluated, indicating that carapace can be used as a non-lethal alternative to muscle during field sampling.

Additional keywords: 13C, 15N, crustacean, non-lethal, stable isotopes.


References

Barnes, C., Sweeting, C. J., Jennings, S., Barry, J. T., and Polunin, N. V. C. (2007). Effect of temperature and ration size on carbon and nitrogen stable isotope trophic fractionation. Functional Ecology 21, 356–362.
Effect of temperature and ration size on carbon and nitrogen stable isotope trophic fractionation.CrossRef |

Beltran, R. S., Peterson, S. H., McHuron, E. A., Reichmuth, C., Hückstädt, L. A., and Costa, D. P. (2016). Seals and sea lions are what they eat, plus what? Determination of trophic discrimination factors for seven pinniped species. Rapid Communications in Mass Spectrometry 30, 1115–1122.
Seals and sea lions are what they eat, plus what? Determination of trophic discrimination factors for seven pinniped species.CrossRef | 1:CAS:528:DC%2BC28XlslWmu7Y%3D&md5=bd99b558cd6ffb391c83d5655d9aa96cCAS |

Ben-David, M., and Flaherty, E. A. (2012). Stable isotopes in mammalian research: a beginner’s guide. Journal of Mammalogy 93, 312–328.
Stable isotopes in mammalian research: a beginner’s guide.CrossRef |

Bodin, N., Le Loc’h, F., and Hily, C. (2007). Effect of lipid removal on carbon and nitrogen stable isotope ratios in crustacean tissues. Journal of Experimental Marine Biology and Ecology 341, 168–175.
Effect of lipid removal on carbon and nitrogen stable isotope ratios in crustacean tissues.CrossRef | 1:CAS:528:DC%2BD2sXntlykug%3D%3D&md5=0db674e250f06f345c2f84a7a6aa85a9CAS |

Bond, A. L., and Diamond, A. W. (2011). Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecological Applications 21, 1017–1023.
Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors.CrossRef |

Bosley, K. L., and Wainright, S. C. (1999). Effects of preservatives and acidification on the stable isotope ratios (15N : 14N, 13C : 12C) of two species of marine animals. Canadian Journal of Fisheries and Aquatic Sciences 56, 2181–2185.
Effects of preservatives and acidification on the stable isotope ratios (15N : 14N, 13C : 12C) of two species of marine animals.CrossRef |

Carolan, J. V., Mazumder, D., Dimovski, C., Diocares, R., and Twining, J. (2012). Biokinetics and discrimination factors for δ13C and δ15N in the omnivorous freshwater crustacean, Cherax destructor. Marine and Freshwater Research 63, 878–886.
Biokinetics and discrimination factors for δ13C and δ15N in the omnivorous freshwater crustacean, Cherax destructor.CrossRef | 1:CAS:528:DC%2BC38XhsFynsrrM&md5=1dfaeaf998b4b71b562156d700ab30a8CAS |

Caut, S., Angulo, E., and Courchamp, F. (2008). Discrimination factors (Δ15N and Δ13C) in an omnivorous consumer: effect of diet isotopic ratio. Functional Ecology 22, 255–263.
Discrimination factors (Δ15N and Δ13C) in an omnivorous consumer: effect of diet isotopic ratio.CrossRef |

Caut, S., Angulo, E., and Courchamp, F. (2009). Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46, 443–453.
Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction.CrossRef | 1:CAS:528:DC%2BD1MXkslGgu7k%3D&md5=40cd67d87589c84fed331373a8b7daf4CAS |

Chikaraishi, Y., Steffan, S. A., Takano, Y., and Ohkouchi, N. (2015). Diet quality influences isotopic discrimination among amino acids in an aquatic vertebrate. Ecology and Evolution 5, 2048–2059.
Diet quality influences isotopic discrimination among amino acids in an aquatic vertebrate.CrossRef |

Crawley, K. R., Hyndes, G. A., and Vanderklift, M. A. (2007). Variation among diets in discrimination of δ13C and δ15N in the amphipod Allorchestes compressa. Journal of Experimental Marine Biology and Ecology 349, 370–377.
Variation among diets in discrimination of δ13C and δ15N in the amphipod Allorchestes compressa.CrossRef | 1:CAS:528:DC%2BD2sXovFegu7s%3D&md5=fa7328a1385e0808a28245ce4d7aef13CAS |

Dalerum, F., and Angerbjörn, A. (2005). Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 144, 647–658.
Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes.CrossRef | 1:STN:280:DC%2BD2MvmsFKhtg%3D%3D&md5=cc7756b71eea5459c0d29b239f80beb3CAS |

De Niro, M. J., and Epstein, S. (1981). Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351.
Influence of diet on the distribution of nitrogen isotopes in animals.CrossRef | 1:CAS:528:DyaL3MXktVGmtLw%3D&md5=80313d7382a3205b5803068c5242c48fCAS |

deVries, M. S., del Rio, C. M., Tunstall, T. S., and Dawson, T. E. (2015). Isotopic incorporation rates and discrimination factors in mantis shrimp crustaceans. PLoS One 10, e0122334.
Isotopic incorporation rates and discrimination factors in mantis shrimp crustaceans.CrossRef |

Felicetti, L. A., Schwartz, C. C., Rye, R. O., Haroldson, M. A., Gunther, K. A., Phillips, D. L., and Robbins, C. T. (2003). Use of sulfur and nitrogen stable isotopes to determine the importance of whitebark pine nuts to Yellowstone grizzly bears. Canadian Journal of Zoology 81, 763–770.
Use of sulfur and nitrogen stable isotopes to determine the importance of whitebark pine nuts to Yellowstone grizzly bears.CrossRef |

Florin, S. T., Felicetti, L. A., and Robbins, C. T. (2011). The biological basis for understanding and predicting dietary‐induced variation in nitrogen and sulphur isotope ratio discrimination. Functional Ecology 25, 519–526.
The biological basis for understanding and predicting dietary‐induced variation in nitrogen and sulphur isotope ratio discrimination.CrossRef |

Fry, B. (2006) ‘Stable Isotope Ecology.’ (Springer: New York, NY, USA.)

Fry, B., and Arnold, C. (1982). Rapid 13C/12C turnover during growth of brown shrimp (Penaeus aztecus). Oecologia 54, 200–204.
Rapid 13C/12C turnover during growth of brown shrimp (Penaeus aztecus).CrossRef |

Haramis, G. M., Jorde, D. G., Macko, S. A., Walker, J. L., and Karasov, W. (2001). Stable-isotope analysis of canvasback winter diet in upper Chesapeake Bay. The Auk 118, 1008–1017.
Stable-isotope analysis of canvasback winter diet in upper Chesapeake Bay.CrossRef |

Herzka, S. Z., and Holt, G. J. (2000). Changes in isotopic composition of red drum (Sciaenops ocellatus) larvae in response to dietary shifts: potential applications to settlement studies. Canadian Journal of Fisheries and Aquatic Sciences 57, 137–147.
Changes in isotopic composition of red drum (Sciaenops ocellatus) larvae in response to dietary shifts: potential applications to settlement studies.CrossRef |

Hilderbrand, G., Robbins, C., and Farley, S. (1998). Response: use of stable isotopes to determine diets of living and extinct bears. Canadian Journal of Zoology 76, 2301–2303.
Response: use of stable isotopes to determine diets of living and extinct bears.CrossRef |

Hobson, K. A., and Clark, R. G. (1992). Assessing avian diets using stable isotopes II: factors influencing diet–tissue fractionation. The Condor 94, 189–197.
Assessing avian diets using stable isotopes II: factors influencing diet–tissue fractionation.CrossRef |

Hollows, J. W., Townsend, C. R., and Collier, K. J. (2002). Diet of the crayfish Paranephrops zealandicus in bush and pasture streams: insights from stable isotopes and stomach analysis. New Zealand Journal of Marine and Freshwater Research 36, 129–142.
Diet of the crayfish Paranephrops zealandicus in bush and pasture streams: insights from stable isotopes and stomach analysis.CrossRef |

Hussey, N. E., Brush, J., McCarthy, I. D., and Fisk, A. T. (2010). δ15N and δ13C diet–tissue discrimination factors for large sharks under semi-controlled conditions. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 155, 445–453.
δ15N and δ13C diet–tissue discrimination factors for large sharks under semi-controlled conditions.CrossRef |

Iles, J., Kelleway, J., Kobayashi, T., Mazumder, D., Knowles, L., Priddel, D., and Saintilan, N. (2010). Grazing kangaroos act as local recyclers of energy on semiarid floodplains. Australian Journal of Zoology 58, 145–149.
Grazing kangaroos act as local recyclers of energy on semiarid floodplains.CrossRef |

Jardine, T. D., Hunt, R. J., Pusey, B. J., and Bunn, S. E. (2011). A non-lethal sampling method for stable carbon and nitrogen isotope studies of tropical fishes. Marine and Freshwater Research 62, 83–90.
A non-lethal sampling method for stable carbon and nitrogen isotope studies of tropical fishes.CrossRef | 1:CAS:528:DC%2BC3MXmtFGmsQ%3D%3D&md5=27251bce9ce98330f2fc7e370f3f91c3CAS |

Kaehler, S., and Pakhomov, E. (2001). Effects of storage and preservation on the δ13C and δ15N signatures of selected marine organisms. Marine Ecology Progress Series 219, 299–304.
Effects of storage and preservation on the δ13C and δ15N signatures of selected marine organisms.CrossRef | 1:CAS:528:DC%2BD3MXptVers7c%3D&md5=e181dcd5e0455e646a2eeb89a8d3f2b0CAS |

Kelly, L. J., and Del Rio, C. M. (2010). The fate of carbon in growing fish: an experimental study of isotopic routing. Physiological and Biochemical Zoology 83, 473–480.
The fate of carbon in growing fish: an experimental study of isotopic routing.CrossRef |

Kim, S. L., and Koch, P. L. (2012). Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environmental Biology of Fishes 95, 53–63.
Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis.CrossRef |

Klamt, M., Davis, J., Thompson, R. M., Marchant, R., and Grant, T. R. (2016). Trophic relationships of the platypus: insights from stable isotope and cheek pouch dietary analyses. Marine and Freshwater Research 67, 1196–1204.
Trophic relationships of the platypus: insights from stable isotope and cheek pouch dietary analyses.CrossRef | 1:CAS:528:DC%2BC28Xht1Kku7jK&md5=d49a7264c0e9df042bdcca85d06ae31dCAS |

Logan, J. M., Jardine, T. D., Miller, T. J., Bunn, S. E., Cunjak, R. A., and Lutcavage, M. E. (2008). Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. Journal of Animal Ecology 77, 838–846.
Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods.CrossRef |

Macko, S. A., Helleur, R., Hartley, G., and Jackman, P. (1990). Diagenesis of organic matter – a study using stable isotopes of individual carbohydrates. Organic Geochemistry 16, 1129–1137.
Diagenesis of organic matter – a study using stable isotopes of individual carbohydrates.CrossRef | 1:CAS:528:DyaK3MXisFShu7o%3D&md5=255f22ea7aea3b6bc3c2969a0a169037CAS |

Mariotti, A., Germon, J., Hubert, P., Kaiser, P., Letolle, R., Tardieux, A., and Tardieux, P. (1981). Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes. Plant and Soil 62, 413–430.
Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes.CrossRef | 1:CAS:528:DyaL38XmslOjtQ%3D%3D&md5=724aad2122d04517c8799090fbe4b0c1CAS |

Marques, T. S., Tassoni-Filho, M., Ferronato, B. O., Guardia, I., Verdade, L. M., and de Camargo, P. B. (2011). Isotopic signatures (δ13C and δ15N) of muscle, carapace and claw in Phrynops geoffroanus (Testudines: Chelidae). Zoologia 28, 407–410.
Isotopic signatures (δ13C and δ15N) of muscle, carapace and claw in Phrynops geoffroanus (Testudines: Chelidae).CrossRef |

Martínez del Rio, C., and Carleton, S. A. (2012). How fast and how faithful: the dynamics of isotopic incorporation into animal tissues. Journal of Mammalogy 93, 353–359.
How fast and how faithful: the dynamics of isotopic incorporation into animal tissues.CrossRef |

Martínez del Rio, C., Wolf, N., Carleton, S. A., and Gannes, L. Z. (2009). Isotopic ecology ten years after a call for more laboratory experiments. Biological Reviews of the Cambridge Philosophical Society 84, 91–111.
Isotopic ecology ten years after a call for more laboratory experiments.CrossRef |

Mazumder, D., Iles, J., Kelleway, J., Kobayashi, T., Knowles, L., Saintilan, N., and Hollins, S. (2010). Effect of acidification on elemental and isotopic compositions of sediment organic matter and macro-invertebrate muscle tissues in food web research. Rapid Communications in Mass Spectrometry 24, 2938–2942.
Effect of acidification on elemental and isotopic compositions of sediment organic matter and macro-invertebrate muscle tissues in food web research.CrossRef | 1:CAS:528:DC%2BC3cXht1Gqtr3E&md5=58dfc3155f99af2846f57eefe6303cd4CAS |

Mazumder, D., Wen, L., Johansen, M. P., Kobayashi, T., and Saintilan, N. (2016). Inherent variation in carbon and nitrogen isotopic assimilation in the freshwater macro-invertebrate Cherax destructor. Marine and Freshwater Research 67, 1928–1937.
Inherent variation in carbon and nitrogen isotopic assimilation in the freshwater macro-invertebrate Cherax destructor.CrossRef | 1:CAS:528:DC%2BC28XhvF2hurfI&md5=8d807d855c029b538c5a214d17a63a05CAS |

McCarthy, I. D., and Waldron, S. (2000). Identifying migratory Salmo trutta using carbon and nitrogen stable isotope ratios. Rapid Communications in Mass Spectrometry 14, 1325–1331.
Identifying migratory Salmo trutta using carbon and nitrogen stable isotope ratios.CrossRef | 1:CAS:528:DC%2BD3cXls1yrsbo%3D&md5=fc448e1b5b82f6be6e40b26cde5a399dCAS |

McCutchan, J. H., Lewis, W. M., Kendall, C., and McGrath, C. C. (2003). Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102, 378–390.
Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur.CrossRef | 1:CAS:528:DC%2BD3sXmsl2qurg%3D&md5=26b7784c09b48a71df0afac6c7830351CAS |

McMahon, K. W., Fogel, M. L., Elsdon, T. S., and Thorrold, S. R. (2010). Carbon isotope fractionation of amino acids in fish muscle reflects biosynthesis and isotopic routing from dietary protein. Journal of Animal Ecology 79, 1132–1141.
Carbon isotope fractionation of amino acids in fish muscle reflects biosynthesis and isotopic routing from dietary protein.CrossRef |

Middelburg, J. J. (2014). Stable isotopes dissect aquatic food webs from the top to the bottom. Biogeosciences 11, 2357–2371.
Stable isotopes dissect aquatic food webs from the top to the bottom.CrossRef |

Mirón, M. L. L., Herrera, M. L. G., Ramírez, P. N., and Hobson, K. A. (2006). Effect of diet quality on carbon and nitrogen turnover and isotopic discrimination in blood of a New World nectarivorous bat. The Journal of Experimental Biology 209, 541–548.
Effect of diet quality on carbon and nitrogen turnover and isotopic discrimination in blood of a New World nectarivorous bat.CrossRef |

Mizutani, H., Fukuda, M., Kabaya, Y., and Wada, E. (1990). Carbon isotope ratio of feathers reveals feeding behavior of cormorants. The Auk 107, 400–403.
Carbon isotope ratio of feathers reveals feeding behavior of cormorants.CrossRef |

Newsome, S. D., Clementz, M. T., and Koch, P. L. (2010). Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science 26, 509–572.
| 1:CAS:528:DC%2BC3cXhtVaksrzJ&md5=02566d1c87c7349a20c53ddd3c68738aCAS |

Nyström, P.E.R., Stenroth, P., Holmqvist, N., Berglund, O., Larsson, P.E.R., and Granéli, W. (2006). Crayfish in lakes and streams: individual and population responses to predation, productivity and substratum availability. Freshwater Biology 51, 2096–2113.
Crayfish in lakes and streams: individual and population responses to predation, productivity and substratum availability.CrossRef |

Parkyn, S. M., Collier, K. J., and Hicks, B. J. (2001). New Zealand stream crayfish: functional omnivores but trophic predators? Freshwater Biology 46, 641–652.
New Zealand stream crayfish: functional omnivores but trophic predators?CrossRef |

Pearson, S. F., Levey, D. J., Greenberg, C. H., and Martínez del Rio, C. (2003). Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird. Oecologia 135, 516–523.
Effects of elemental composition on the incorporation of dietary nitrogen and carbon isotopic signatures in an omnivorous songbird.CrossRef |

Perga, M. E., and Gerdeaux, D. (2003). Using the δ13C and δ15N of whitefish scales for retrospective ecological studies: changes in isotope signatures during the restoration of Lake Geneva, 1980–2001. Journal of Fish Biology 63, 1197–1207.
Using the δ13C and δ15N of whitefish scales for retrospective ecological studies: changes in isotope signatures during the restoration of Lake Geneva, 1980–2001.CrossRef |

Perga, M.-E., and Grey, J. (2010). Laboratory measures of isotope discrimination factors: comments on Caut, Angulo & Courchamp (2008, 2009). Journal of Applied Ecology 47, 942–947.
Laboratory measures of isotope discrimination factors: comments on Caut, Angulo & Courchamp (2008, 2009).CrossRef | 1:CAS:528:DC%2BC3cXhtVyhs7zE&md5=c4b5ba82dc9a6aa322839447a6615adfCAS |

Perkins, M. J., McDonald, R. A., van Veen, F. J. F., Kelly, S. D., Rees, G., and Bearhop, S. (2013). Important impacts of tissue selection and lipid extraction on ecological parameters derived from stable isotope ratios. Methods in Ecology and Evolution 4, 944–953.

Perkins, M. J., McDonald, R. A., van Veen, F. J. F., Kelly, S. D., Rees, G., and Bearhop, S. (2014). Application of nitrogen and carbon stable isotopes (δ15N and δ13C) to quantify food chain length and trophic structure. PLoS One 9, e93281.
Application of nitrogen and carbon stable isotopes (δ15N and δ13C) to quantify food chain length and trophic structure.CrossRef |

Phillips, D., and Gregg, J. (2003). Source partitioning using stable isotopes: coping with too many sources. Oecologia 136, 261–269.
Source partitioning using stable isotopes: coping with too many sources.CrossRef |

Phillips, D. L., and Koch, P. L. (2002). Incorporating concentration dependence in stable isotope mixing models. Oecologia 130, 114–125.
Incorporating concentration dependence in stable isotope mixing models.CrossRef |

Podlesak, D. W., and McWilliams, S. R. (2006). Metabolic routing of dietary nutrients in birds: effects of diet quality and macronutrient composition revealed using stable isotopes. Physiological and Biochemical Zoology 79, 534–549.
Metabolic routing of dietary nutrients in birds: effects of diet quality and macronutrient composition revealed using stable isotopes.CrossRef | 1:CAS:528:DC%2BD28XmtlKjsLw%3D&md5=dbcaaf50be9561a9a6bba8ef58296974CAS |

Post, D. M. (2002). Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.
Using stable isotopes to estimate trophic position: models, methods, and assumptions.CrossRef |

Post, D., Layman, C., Arrington, D. A., Takimoto, G., Quattrochi, J., and Montaña, C. (2007). Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179–189.
Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses.CrossRef |

Rasmussen, J. B., Trudeau, V., and Morinville, G. (2009). Estimating the scale of fish feeding movements in rivers using δ13C signature gradients. Journal of Animal Ecology 78, 674–685.
Estimating the scale of fish feeding movements in rivers using δ13C signature gradients.CrossRef |

Reich, K. J., Bjorndal, K. A., and Martínez del Rio, C. (2008). Effects of growth and tissue type on the kinetics of 13C and 15N incorporation in a rapidly growing ectotherm. Oecologia 155, 651–663.
Effects of growth and tissue type on the kinetics of 13C and 15N incorporation in a rapidly growing ectotherm.CrossRef |

Robbins, C. T., Felicetti, L. A., and Sponheimer, M. (2005). The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds. Oecologia 144, 534–540.
The effect of dietary protein quality on nitrogen isotope discrimination in mammals and birds.CrossRef |

Roth, J. D., and Hobson, K. A. (2000). Stable carbon and nitrogen isotopic fractionation between diet and tissue of captive red fox: implications for dietary reconstruction. Canadian Journal of Zoology 78, 848–852.
Stable carbon and nitrogen isotopic fractionation between diet and tissue of captive red fox: implications for dietary reconstruction.CrossRef |

Sarà, G., and Sarà, R. (2007). Feeding habits and trophic levels of bluefin tuna Thunnus thynnus of different size classes in the Mediterranean Sea. Journal of Applied Ichthyology 23, 122–127.
Feeding habits and trophic levels of bluefin tuna Thunnus thynnus of different size classes in the Mediterranean Sea.CrossRef |

Schimmelmann, A. (2011) Carbon, nitrogen and oxygen stable isotope ratios in chitin. In ‘Chitin: Formation and Diagenesis, Topics in Geobiology’. (Ed. N. S. Gupta.) Vol. 34, pp. 81–103. (Springer.)10.1007/978-90-481-9684-5

Schimmelmann, A., Wintsch, R. P., Lewan, M. D., and DeNiro, M. J. (1998) Chitin: ‘forgotten’ source of nitrogen. In ‘Nitrogen-Containing Macromolecules in the Biol- and Geosphere’. (Eds B. A. Stankiewicz and P. F. van Bergen.) Vol. 707, pp. 226–242. (American Chemical Society: Las Vegas, NV, USA.)

Schwarcz, H. P. (1991). Some theoretical aspects of isotope paleodiet studies. Journal of Archaeological Science 18, 261–275.
Some theoretical aspects of isotope paleodiet studies.CrossRef |

Sotiropoulos, M. A., Tonn, W. M., and Wassenaar, L. I. (2004). Effects of lipid extraction on stable carbon and nitrogen isotope analyses of fish tissues: potential consequences for food web studies. Ecology Freshwater Fish 13, 155–160.
Effects of lipid extraction on stable carbon and nitrogen isotope analyses of fish tissues: potential consequences for food web studies.CrossRef |

Stenroth, P., Holmqvist, N., Nyström, P., Berglund, O., Larsson, P., and Granéli, W. (2006). Stable isotopes as an indicator of diet in omnivorous crayfish (Pacifastacus leniusculus): the influence of tissue, sample treatment, and season. Canadian Journal of Fisheries and Aquatic Sciences 63, 821–831.
Stable isotopes as an indicator of diet in omnivorous crayfish (Pacifastacus leniusculus): the influence of tissue, sample treatment, and season.CrossRef | 1:CAS:528:DC%2BD28XksFKnu7k%3D&md5=2fd5a2402eb85f55663d0e8876d63f37CAS |

Tibbets, T. M., Wheeless, L. A., and Del Rio, C. M. (2008). Isotopic enrichment without change in diet: an ontogenetic shift in δ15N during insect metamorphosis. Functional Ecology 22, 109–113.

Tieszen, L. L., Boutton, T. W., Tesdahl, K. G., and Slade, N. A. (1983). Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57, 32–37.
Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet.CrossRef | 1:STN:280:DC%2BC1cznvVKlsA%3D%3D&md5=70a6c64863505f7d360e96b88d248ad2CAS |

Vanderklift, M. A., and Ponsard, S. (2003). Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136, 169–182.
Sources of variation in consumer-diet δ15N enrichment: a meta-analysis.CrossRef |

Waddington, K., and MacArthur, L. (2008). Diet quality and muscle tissue location influence consumer-diet discrimination in captive-reared rock lobsters (Panulirus cygnus). Marine Biology 154, 569–576.
Diet quality and muscle tissue location influence consumer-diet discrimination in captive-reared rock lobsters (Panulirus cygnus).CrossRef | 1:CAS:528:DC%2BD1cXkvVSns74%3D&md5=1738330db4bc776c13157aa52c0b11f9CAS |

Webb, S., Hedges, R., and Simpson, S. (1998). Diet quality influences the δ13C and δ15N of locusts and their biochemical components. The Journal of Experimental Biology 201, 2903–2911.
| 1:CAS:528:DyaK1cXnvVCkt7g%3D&md5=4ac953fdbb50989de90f65e5055a6381CAS |

Webb, C. E., Lewis, J., Shain, A., Kastrisianaki-Guyton, E., Honch, N. V., Stewart, A., Miller, B., Tarlton, J., and Evershed, R. P. (2017). The influence of varying proportions of terrestrial and marine dietary protein on the stable carbon-isotope compositions of pig tissues from a controlled feeding experiment. STAR: Science & Technology of Archaeological Research 3, 36–52.
The influence of varying proportions of terrestrial and marine dietary protein on the stable carbon-isotope compositions of pig tissues from a controlled feeding experiment.CrossRef |

Wolf, N., Carleton, S. A., and Martínez del Rio, C. (2009). Ten years of experimental animal isotopic ecology. Functional Ecology 23, 17–26.
Ten years of experimental animal isotopic ecology.CrossRef |

Yokoyama, H., Tamaki, A., Harada, K., Shimoda, K., Koyama, K., and Ishihi, Y. (2005). Variability of diet–tissue isotopic fractionation in estuarine macrobenthos. Marine Ecology Progress Series 296, 115–128.
Variability of diet–tissue isotopic fractionation in estuarine macrobenthos.CrossRef | 1:CAS:528:DC%2BD2MXhtFSktbvO&md5=23b1f8143a0aca4b11c3da3592fe6287CAS |

Zanden, M. J. V., and Rasmussen, J. B. (2001). Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46, 2061–2066.
Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies.CrossRef |



Export Citation