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RESEARCH ARTICLE

Biokinetics and discrimination factors for δ13C and δ15N in the omnivorous freshwater crustacean, Cherax destructor

J. Veliscek Carolan A B , D. Mazumder A , C. Dimovski A , R. Diocares A and J. Twining A
+ Author Affiliations
- Author Affiliations

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

B Corresponding author. Email: jvc@ansto.gov.au

Marine and Freshwater Research 63(10) 878-886 https://doi.org/10.1071/MF11240
Submitted: 31 October 2011  Accepted: 7 August 2012   Published: 29 October 2012

Abstract

Knowledge and understanding of biokinetics and discrimination factors for carbon-13 (δ13C) and nitrogen-15 (δ15N) are important when using stable isotopes for food-web studies. Therefore, we performed a controlled laboratory diet-switch experiment to examine diet–tissue and diet–faeces discrimination factors as well as the biokinetics of stable-isotope assimilation in the omnivorous freshwater crustacean, Cherax destructor. The biokinetics of δ13C could not be established; however, the δ15N value of C. destructor tissue reached equilibrium after 80 ± 35 days, with an estimated biological half-time for 15N of 19 ± 5 days. Metabolic activity contributed to the turnover of 15N by nearly an order of magnitude more than growth. The diet–tissue discrimination factors at the end of the exposure were estimated as –1.1 ± 0.5‰ for δ13C and +1.5 ± 1.0‰ for δ15N, indicating that a δ15N diet–tissue discrimination factor different from the typically assumed +3.4‰ may be required for freshwater macroinvertebrates such as C. destructor. The diet–faeces discrimination factor for δ15N after 120 days was estimated as +0.9 ± 0.5‰. The present study provides an increased understanding of the biokinetics and discrimination factors for a keystone freshwater macroinvertebrate that will be valuable for future food-web studies in freshwater ecosystems.

Additional keywords : biokinetics, Cherax destructor, fractionation, laboratory study, stable isotopes.


References

Al-Maslamani, I., Le Vay, L., and Kennedy, H. (2009). Feeding on intertidal microbial mats by postlarval tiger shrimp, Penaeus semisulcatus De Haan. Marine Biology 156, 2001–2009.
Feeding on intertidal microbial mats by postlarval tiger shrimp, Penaeus semisulcatus De Haan.Crossref | GoogleScholarGoogle Scholar |

Alves-Stanley, C. D., and Worthy, G. A. J. (2009). Carbon and nitrogen stable isotope turnover rates and diet–tissue discrimination in florida manatees (Trichechus manatus latirostris). The Journal of Experimental Biology 212, 2349–2355.
Carbon and nitrogen stable isotope turnover rates and diet–tissue discrimination in florida manatees (Trichechus manatus latirostris).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFGhu7rP&md5=38059563ab94fbf68f27c1b6cd8af855CAS |

Beatty, S. J. (2006). The diet and trophic positions of translocated, sympatric populations of Cherax destructor and Cherax cainii in the Hutt River, Western Australia: evidence of resource overlap. Marine and Freshwater Research 57, 825–835.
The diet and trophic positions of translocated, sympatric populations of Cherax destructor and Cherax cainii in the Hutt River, Western Australia: evidence of resource overlap.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1OgsLfP&md5=d8423071d616d46053bb2028e86766e2CAS |

Benke, A. C., Huryn, A. D., Smock, L. A., and Wallace, J. B. (1999). Length–mass relationships for freshwater macroinvertebrates in North America with particular reference to the southeastern United States. Journal of the North American Benthological Society 18, 308–343.
Length–mass relationships for freshwater macroinvertebrates in North America with particular reference to the southeastern United States.Crossref | GoogleScholarGoogle Scholar |

Bosley, K. L., Witting, D. A., Chambers, C., and Wainright, S. C. (2002). Estimating turnover rates of carbon and nitrogen in recently metamorphosed winter flounder Pseudopleuronectes americanus with stable isotopes. Marine Ecology Progress Series 236, 233–240.
Estimating turnover rates of carbon and nitrogen in recently metamorphosed winter flounder Pseudopleuronectes americanus with stable isotopes.Crossref | GoogleScholarGoogle Scholar |

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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkslGgu7k%3D&md5=d636cf80c178ac3da013f2025792f57aCAS |

Checkley, D. M., and Entzeroth, L. C. (1985). Elemental and isotopic fractionation of carbon and nitrogen by marine, planktonic copepods and implications to the marine nitrogen cycle. Journal of Plankton Research 7, 553–568.
Elemental and isotopic fractionation of carbon and nitrogen by marine, planktonic copepods and implications to the marine nitrogen cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlslOnsrc%3D&md5=1508a33c1f0a4d884860cde572a44b76CAS |

DeNiro, M. J., and Epstein, S. (1978). Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506.
Influence of diet on the distribution of carbon isotopes in animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXls1WrsbY%3D&md5=ade4fa89b82da73ad8e6fea7e38179abCAS |

DeNiro, 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 | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXktVGmtLw%3D&md5=91fb3d34cfd50525524407925d4fe3a0CAS |

Dennis, C. A., MacNeil, M. A., Rosati, J. Y., Pitcher, T. E., and Fisk, A. T. (2010). Diet discrimination factors are inversely related to δ15N and δ13C values of food for fish under controlled conditions. Rapid Communications in Mass Spectrometry 24, 3515–3520.
Diet discrimination factors are inversely related to δ15N and δ13C values of food for fish under controlled conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVeksbzM&md5=b73c45cd1e0faaa16717b580fbfc19ccCAS |

Dubois, S., Jean-Louis, B., Bertrand, B., and Lefebvre, S. (2007). Isotope trophic-step fractionation of suspension-feeding species: implications for food partitioning in coastal ecosystems. Journal of Experimental Marine Biology and Ecology 351, 121–128.
Isotope trophic-step fractionation of suspension-feeding species: implications for food partitioning in coastal ecosystems.Crossref | GoogleScholarGoogle Scholar |

Duffy, R. E., Godwin, I., Nolan, J., and Purvis, I. (2011). The contribution of naturally occurring food items to the diet of Cherax destructor when fed formulated diets of differing protein levels. Aquaculture 313, 107–114.
The contribution of naturally occurring food items to the diet of Cherax destructor when fed formulated diets of differing protein levels.Crossref | GoogleScholarGoogle Scholar |

Dumas, J. B. A. (1826). Memoire sur quelques points de la theorie atomique. Annales de Chimie et Physique 33, 334–414.

Fagan, K.-A., Koops, M. A., Arts, M. T., and Power, M. (2011). Assessing the utility of C : N ratios for predicting lipid content in fishes. Canadian Journal of Fisheries and Aquatic Sciences 68, 374–385.
Assessing the utility of C : N ratios for predicting lipid content in fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFyqt7g%3D&md5=db34de9b20ca4f4fb9cdcd57c1ddbf54CAS |

Fantle, M. S., Dittel, A. I., Schwalm, S. M., Epifanio, C. E., and Fogel, M. L. (1999). A food web analysis of the juvenile blue crab, Callinectes sapidus, using stable isotopes in whole animals and individual amino acids. Oecologia 120, 416–426.
A food web analysis of the juvenile blue crab, Callinectes sapidus, using stable isotopes in whole animals and individual amino acids.Crossref | GoogleScholarGoogle Scholar |

Fila, L., Carmichael, R. H., Shriver, A., and Valiela, I. (2001). Stable N isotopic signatures in bay scallop tissue, feces, and pseudofeces in Cape Cod estuaries subject to different N loads. The Biological Bulletin 201, 294–296.
Stable N isotopic signatures in bay scallop tissue, feces, and pseudofeces in Cape Cod estuaries subject to different N loads.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MnjvVKntg%3D%3D&md5=989aae2810179f25e3acdcee3e25a22dCAS |

Fisk, A. T., Tittlemier, S. A., Pranschke, J. L., and Norstrom, R. J. (2002). Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of Greenland sharks. Ecology 83, 2162–2172.
Using anthropogenic contaminants and stable isotopes to assess the feeding ecology of Greenland sharks.Crossref | GoogleScholarGoogle Scholar |

Fisk, A. T., Sash, K., Maerz, J., Palmer, W., Carroll, J. P., and MacNeil, M. A. (2009). Metabolic turnover rates of carbon and nitrogen stable isotopes in captive juvenile snakes. Rapid Communications in Mass Spectrometry 23, 319–326.
Metabolic turnover rates of carbon and nitrogen stable isotopes in captive juvenile snakes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVKqsbw%3D&md5=82e39e5394017b00bce2b8fffc38a3e5CAS |

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 | GoogleScholarGoogle Scholar |

Gannes, L. Z., O’Brien, D. M., and Martinez del Rio, C. (1997). Stable isotopes in animal ecology: assumptions, caveats and a call for more laboratory experiments. Ecology 78, 1271–1276.
Stable isotopes in animal ecology: assumptions, caveats and a call for more laboratory experiments.Crossref | GoogleScholarGoogle Scholar |

Hesslein, R. H., Hallard, K. A., and Ramlal, P. (1993). Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N. Canadian Journal of Fisheries and Aquatic Sciences 50, 2071–2076.
Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXktVOqs7o%3D&md5=ca42ea597a9aad445228b907a4311665CAS |

Hobson, K. A., and Clark, R. G. (1992). Assessing avian diets using stable isotopes I: turnover of 13C in tissues. The Condor 94, 181–188.
Assessing avian diets using stable isotopes I: turnover of 13C in tissues.Crossref | GoogleScholarGoogle Scholar |

Hwang, Y. T., Millar, J. S., and Longstaffe, F. J. (2007). Do δ15N and δ13C values of feces reflect the isotopic composition of diets in small mammals? Canadian Journal of Zoology 85, 388–396.
Do δ15N and δ13C values of feces reflect the isotopic composition of diets in small mammals?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtFehu70%3D&md5=863e1375375ac6a2be05d7f1c066ebe0CAS |

Johannes, R. E., and Satomi, M. (1966). Composition and nutritive value of fecal pellets of a marine crustacean. Limnology and Oceanography 11, 191–197.
Composition and nutritive value of fecal pellets of a marine crustacean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF28XksFShsbs%3D&md5=bcbb82a60fd565d0c0ffb0de317a9a6dCAS |

Johannsson, O. E., Leggett, M. F., Rudstam, L. G., Servos, M. R., Mohammadian, M. A., Gal, G., Dermott, R. M., and Hesslein, R. H. (2001). Diet of Mysis relicta in Lake Ontario as revealed by stable isotope and gut content analysis. Canadian Journal of Fisheries and Aquatic Sciences 58, 1975–1986.
Diet of Mysis relicta in Lake Ontario as revealed by stable isotope and gut content analysis.Crossref | GoogleScholarGoogle Scholar |

Johnston, K., Robson, B. J., and Fairweather, P. G. (2011). Trophic positions of omnivores are not always flexible: evidence from four freshwater crayfish. Austral Ecology 36, 269–279.
Trophic positions of omnivores are not always flexible: evidence from four freshwater crayfish.Crossref | GoogleScholarGoogle Scholar |

Kelleway, J., Mazumder, D., Wilson, G., Saintilan, N., Knowles, L., and Kobayah, T. (2010). Trophic structure of benthic resources and consumers varies across a regulated floodplain wetland. Marine and Freshwater Research 61, 430–440.
Trophic structure of benthic resources and consumers varies across a regulated floodplain wetland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlt1SjsLg%3D&md5=c6a2a394e6649b09ccb0392a3ec27628CAS |

MacAvoy, S. E., Arneson, L. S., and Basset, E. (2006). Correlation of metabolism with tissue carbon and nitrogen turnover rate in small mammals. Oecologia 150, 190–201.
Correlation of metabolism with tissue carbon and nitrogen turnover rate in small mammals.Crossref | GoogleScholarGoogle Scholar |

MacNeil, M. A., Drouillard, K. G., and Fisk, A. T. (2006). Variable uptake and elimination of stable nitrogen isotopes between tissues in fish. Canadian Journal of Fisheries and Aquatic Sciences 63, 345–353.
Variable uptake and elimination of stable nitrogen isotopes between tissues in fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XivVSgsLw%3D&md5=fe0871b7dd96b7280f052cae96f0a135CAS |

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 | GoogleScholarGoogle Scholar |

Overmyer, J. P., MacNeil, M. A., and Fisk, A. T. (2008). Fractionation and metabolic turnover of carbon and nitrogen stable isotopes in black fly larvae. Rapid Communications in Mass Spectrometry 22, 694–700.
Fractionation and metabolic turnover of carbon and nitrogen stable isotopes in black fly larvae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjvVansLw%3D&md5=371c73fde4d17f5a6187bc1fe0e339a3CAS |

Parker, P. L., Anderson, R. K., and Lawrence, A. (1989). A 13C and I5N tracer study of nutrition in aquaculture: Penaeus vannamei in a pond grow-out system. In ‘Stable isotopes in ecological research’. (Eds P. W. Rundel, J. R. Ehleringer and K. A. Nagy.) pp. 289–303. (Springer-Verlag Inc.: New York.)

Perga, M., and Grey, J. (2010). Laboratory measures of isotopic discrimination factors: comments on Caut, Angulo & Couchamp (2008, 2009). Journal of Applied Ecology 47, 942–947.
Laboratory measures of isotopic discrimination factors: comments on Caut, Angulo & Couchamp (2008, 2009).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyhs7zE&md5=bff2a74c9261f27fdbe8503acb3160cdCAS |

Peterson, B. J., and Fry, B. (1987). Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293–320.
Stable isotopes in ecosystem studies.Crossref | GoogleScholarGoogle Scholar |

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 | GoogleScholarGoogle Scholar |

Post, D. M., Layman, C. A., Arrington, D. A., Takimoto, G., Quattrochi, J., and Montana, C. G. (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 | GoogleScholarGoogle Scholar |

Reich, K. J., Bjorndal, K. A., and Martinez 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 | GoogleScholarGoogle Scholar |

Sponheimer, M., Robinson, T., Ayliffe, L., Passey, B., Roeder, B., Shipley, L., Lopez, E., Cerling, T., Dearing, D., and Ehleringer, J. (2003). An experimental study of carbon-isotope fractionation between diet, hair and feces of mammalian herbivores. Canadian Journal of Zoology 81, 871–876.
An experimental study of carbon-isotope fractionation between diet, hair and feces of mammalian herbivores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtVOjs7Y%3D&md5=3fe477a1f01412ae959c6f34546fbad6CAS |

Stenroth, P., Holmqvist, N., Nystrom, P., Berglund, O., Larsson, P., and Graneli, 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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksFKnu7k%3D&md5=c893aba156658598e798d78f5e4c642cCAS |

Suzuki, K. W., Kasai, A., Nakayama, K., and Tanaka, M. (2005). Differential isotopic enrichment and half-life among tissues in Japanese temperate bass (Lateolabrax japonicus) juveniles: implications for analyzing migration. Canadian Journal of Fisheries and Aquatic Sciences 62, 671–678.
Differential isotopic enrichment and half-life among tissues in Japanese temperate bass (Lateolabrax japonicus) juveniles: implications for analyzing migration.Crossref | GoogleScholarGoogle Scholar |

Sweeting, C. J., Jennings, S., and Polunin, N. V. C. (2005). Variance in isotopic signatures as a descriptor of tissue turnover and degree of omnivory. Functional Ecology 19, 777–784.
Variance in isotopic signatures as a descriptor of tissue turnover and degree of omnivory.Crossref | GoogleScholarGoogle Scholar |

Systat Software Inc (2004). ‘SigmaStat for Windows, Version 3.11.’ (Systat Software: Point Richmond, CA.)

Tarboush, R. A., MacAvoy, S. E., Macko, S. A., and Connaughton, V. (2006). Contribution of catabolic tissue replacement to the turnover of stable isotopes in Danio rerio. Canadian Journal of Zoology 84, 1453–1460.
Contribution of catabolic tissue replacement to the turnover of stable isotopes in Danio rerio.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1akurc%3D&md5=0b3ee2b87f979f23bcc18c9e338330eeCAS |

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 | GoogleScholarGoogle Scholar |

Underwood, A. J., and Chapman, M. G. (1989). ‘GMAV5 for Windows. An Analysis of Variance Program.’ (Institute of Marine Ecology, University of Sydney: Sydney.)

Vander Zanden, M. J., and Rasmussen, J. B. (2001). Variation in δ 15N and δ 13C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46, 2061–2066.
Variation in δ 15N and δ 13C trophic fractionation: implications for aquatic food web studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xht12ltA%3D%3D&md5=cda26bd0a2861e8235fd7744853ec9feCAS |

Vander Zanden, M. J., Shuter, B. J., Lester, N., and Rasmussen, J. B. (1999). Patterns of food chain length in lakes: a stable isotope study. American Naturalist 154, 406–416.
Patterns of food chain length in lakes: a stable isotope study.Crossref | GoogleScholarGoogle Scholar |

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 | GoogleScholarGoogle Scholar |

Voigt, C. C., Rex, K., Michener, R. H., and Speakman, J. R. (2008). Nutrient routing in omnivorous animals tracked by stable carbon isotopes in tissue and exhaled breath. Oecologia 157, 31–40.
Nutrient routing in omnivorous animals tracked by stable carbon isotopes in tissue and exhaled breath.Crossref | GoogleScholarGoogle Scholar |

Whicker, F. W., and Schultz, V. (1982). ‘Radioecology: Nuclear Energy and the Environment.’ (CRC Press: Boca Raton, FL.)

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