A non-lethal sampling method for stable carbon and nitrogen isotope studies of tropical fishes
Timothy D. Jardine A C , Richard J. Hunt B , Bradley J. Pusey A and Stuart E. Bunn A
+ Author Affiliations
- Author Affiliations
A Australian Rivers Institute, Griffith University, Nathan, Qld 4111, Australia.
B Queensland Department of Environment and Resource Management, Mareeba, Qld 4880, Australia.
C Corresponding author. Email: t.jardine@griffith.edu.au
Marine and Freshwater Research 62(1) 83-90 https://doi.org/10.1071/MF10211
Submitted: 6 August 2010 Accepted: 6 November 2010 Published: 18 January 2011
Abstract
Despite prior studies showing good agreement between fin and muscle isotope ratios in temperate fishes, the non-lethal method of fin sampling has yet to become a standard technique in isotopic food-web studies, and the relationship between the two tissues has never been tested in the tropics. We hypothesised that fin and muscle δ13C and δ15N would be strongly correlated in tropical fishes, thus allowing non-lethal sampling of these species. To test this hypothesis, we analysed fin and muscle tissues from 174 tropical fishes representing 27 species from the Mitchell River, Queensland, Australia. Fin tissue was a strong predictor of muscle-tissue δ13C (r2 = 0.91 for all species) and was slightly enriched in 13C (0.9‰), consistent with the results of studies on temperate species. Fin tissue was a poorer predictor of muscle-tissue δ15N (r2 = 0.56 for all species) although the mean difference between the tissues was small (<0.1‰). Differences were smallest in the largest fish, possibly because the elemental composition (%N) of fin more closely resembled that of muscle. These measurements provide more impetus for increased use of fin tissue as a non-destructive means of testing hypotheses about fish food webs in the tropics and elsewhere.
Additional keywords: δ13C, δ15N, fin tissue, fractionation, muscle tissue, size, turnover.
References
Araujo-Lima, C. A. R. M., Forsberg, B. R., Victoria, R. L., and Martinelli, L. A. (1986). Energy sources for detritivorous fishes in the Amazon. Science 234, 1256–1258.| Energy sources for detritivorous fishes in the Amazon.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvivFOitA%3D%3D&md5=4472399d4b318f14a55c7d4af61252dbCAS | 17778007PubMed |
Baker, R. F., Blanchfield, P. J., Paterson, M. J., Flett, R. J., and Wesson, L. (2004). Evaluation of nonlethal methods for the analysis of mercury in fish tissue. Transactions of the American Fisheries Society 133, 568–576.
| Evaluation of nonlethal methods for the analysis of mercury in fish tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsVCqsLs%3D&md5=e1a98710a713ed180762a0bcef65bd32CAS |
Brodeur, N. N., Noel, M. V., Venter, O., Bernatchez, L., Dayanandan, S., et al. (2008). No evidence of kin bias in dispersion of young-of-the-year Atlantic salmon Salmo salar L. in a natural stream. Journal of Fish Biology 73, 2361–2370.
| No evidence of kin bias in dispersion of young-of-the-year Atlantic salmon Salmo salar L. in a natural stream.Crossref | GoogleScholarGoogle Scholar |
Bunn, S. E., Loneragan, N. R., and Kempster, M. A. (1995). Effects of acid washing on stable-isotope ratios of C and N in penaeid shrimp and seagrass – implications for food-web studies using multiple stable isotopes. Limnology and Oceanography 40, 622–625.
| Effects of acid washing on stable-isotope ratios of C and N in penaeid shrimp and seagrass – implications for food-web studies using multiple stable isotopes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXotFGms7c%3D&md5=974b5e693f1bed4825e0b9ec598ab3deCAS |
Cabana, G., and Rasmussen, J. B. (1996). Comparison of aquatic food chains using nitrogen isotopes. Proceedings of the National Academy of Sciences, USA 93, 10 844–10 847.
| Comparison of aquatic food chains using nitrogen isotopes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmtVOlu70%3D&md5=18b25825719fa7e3f8537f0cdda03ed7CAS |
Champagne, C. E., Austin, J. D., Jelks, H. L., and Jordan, F. (2008). Effects of fin clipping on survival and position-holding behavior of brown darters, Etheostoma edwini. Copeia 2008, 916–919.
| Effects of fin clipping on survival and position-holding behavior of brown darters, Etheostoma edwini.Crossref | GoogleScholarGoogle Scholar |
Cherel, Y., Fontaine, C., Richard, P., and Labat, J.-P. (2010). Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnology and Oceanography 55, 324–332..
| 1:CAS:528:DC%2BC3cXitVSgur0%3D&md5=b3037182b6aaa3f44daf93c606540d8bCAS |
Church, M. R., Ebersole, J. L., Rensmeyer, K. M., Couture, R. B., Barrows, F. T., et al. (2009). Mucus: a new tissue fraction for rapid determination of fish diet switching using stable isotopes. Canadian Journal of Fisheries and Aquatic Sciences 66, 1–5.
| Mucus: a new tissue fraction for rapid determination of fish diet switching using stable isotopes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1agt7c%3D&md5=496330abc2b26df406d271cd6d5691f0CAS |
Cox, M. K., and Hartman, K. J. (2005). Nonlethal estimation of proximate composition in fish. Canadian Journal of Fisheries and Aquatic Sciences 62, 269–275.
| Nonlethal estimation of proximate composition in fish.Crossref | GoogleScholarGoogle Scholar |
Dalerum, F., and Angerbjorn, 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 | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MvmsFKhtg%3D%3D&md5=7c955ecb10c80aff3b90d145a0dc0c53CAS | 16041545PubMed |
Davies P. M., Bunn S. E., and Hamilton S. K. (2008). Primary production in tropical streams and rivers. In ‘Tropical Stream Ecology’. (Ed. D. Dudgeon.) pp. 23–42. (Academic Press: San Diego, CA, USA.)
Dube, M. G., Benoy, G. A., Blenkinsopp, S., Ferone, J. M., Brua, R. B., et al. (2005). Application of multi-stable isotope (C-13, N-15, S-34, Cl-37) assays to assess spatial separation of fish (longnose sucker Catostomus catostomus) in an area receiving complex effluents. Water Quality Research Journal of Canada 40, 275–287..
| 1:CAS:528:DC%2BD2MXht1yksrfN&md5=eb313b776acad3c3e9805acaaeb18850CAS |
Finlay, J. C., Khandwala, S., and Power, M. E. (2002). Spatial scales of carbon flow in a river food web. Ecology 83, 1845–1859.
| Spatial scales of carbon flow in a river food web.Crossref | GoogleScholarGoogle Scholar |
Forsberg, B. R., Araujo-Lima, C. A. R. M., Martinelli, L. A., Victoria, R. L., and Bonassi, J. A. (1993). Autotrophic carbon sources for fish of the central Amazon. Ecology 74, 643–652.
| Autotrophic carbon sources for fish of the central Amazon.Crossref | GoogleScholarGoogle Scholar |
German, D. P., and Miles, R. D. (2010). Stable carbon and nitrogen incorporation in blood and fin tissue of the catfish Pterygoplichthys disjunctivus (Siluriformes, Loricariidae). Environmental Biology of Fishes 89, 117–133.
| Stable carbon and nitrogen incorporation in blood and fin tissue of the catfish Pterygoplichthys disjunctivus (Siluriformes, Loricariidae).Crossref | GoogleScholarGoogle Scholar |
Gremillion, P. T., Cizdziel, J. V., and Cody, N. R. (2005). Caudal fin mercury as a non-lethal predictor of fish-muscle mercury. Environmental Chemistry 2, 96–99.
| Caudal fin mercury as a non-lethal predictor of fish-muscle mercury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvVChs7k%3D&md5=59c037c039e57bdef6f5eea018b1940bCAS |
Hanisch, J. R., Tonn, W. M., and Paszkowski, C. A. (2010). δ13C and δ15N signatures in muscle and fin tissues: non-lethal sampling methods for stable isotope analysis of salmonids. North American Journal of Fisheries Management 30, 1–11..
Hansen, T., and Sommer, U. (2007). Increasing the sensitivity of δ13C and δ15N measurements by a high sensitivity elemental analyzer connected to an isotope ratio mass spectrometer. Rapid Communications in Mass Spectrometry 21, 314–318.
| Increasing the sensitivity of δ13C and δ15N measurements by a high sensitivity elemental analyzer connected to an isotope ratio mass spectrometer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitValsb0%3D&md5=82a0974e38eb803c786374a12193bc5cCAS | 17200974PubMed |
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 | 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 delta-S-34, delta-C-13, and delta-N-15. 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 delta-S-34, delta-C-13, and delta-N-15.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXktVOqs7o%3D&md5=3816eb81f776e67e81f72a382caaba1aCAS |
Jardine, T. D., and Cunjak, R. A. (2005). Analytical error in stable isotope ecology. Oecologia 144, 528–533.
| Analytical error in stable isotope ecology.Crossref | GoogleScholarGoogle Scholar | 15761780PubMed |
Jardine, T. D., Gray, M. A., McWilliam, S. M., and Cunjak, R. A. (2005). Stable isotope variability in tissues of temperate stream fishes. Transactions of the American Fisheries Society 134, 1103–1110.
| Stable isotope variability in tissues of temperate stream fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtF2qtrrM&md5=317907b41adb145fb3f124fec9edcafdCAS |
Jardine, T. D., Kidd, K. A., and Fisk, A. T. (2006). Applications, considerations and sources of uncertainty when using stable isotope analysis in ecotoxicology. Environmental Science & Technology 40, 7501–7511.
| Applications, considerations and sources of uncertainty when using stable isotope analysis in ecotoxicology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFWnurfK&md5=7a8ecc4176efa3b2160d12f4240ac31bCAS | 17256487PubMed |
Kelly, M. H., Hagar, W. G., Jardine, T. D., and Cunjak, R. A. (2006). Nonlethal sampling of sunfish and slimy sculpin for stable isotope analysis: how scale and fin tissue compare with muscle tissue. North American Journal of Fisheries Management 26, 921–925.
| Nonlethal sampling of sunfish and slimy sculpin for stable isotope analysis: how scale and fin tissue compare with muscle tissue.Crossref | GoogleScholarGoogle Scholar |
Layman, C. A., Arrington, D. A., Montana, C. G., and Post, D. M. (2007). Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88, 42–48.
| Can stable isotope ratios provide for community-wide measures of trophic structure?Crossref | GoogleScholarGoogle Scholar | 17489452PubMed |
Logan, J. M., Jardine, T. D., Miller, T. J., Bunn, S. E., Cunjak, R. A., et al. (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 | GoogleScholarGoogle Scholar | 18489570PubMed |
Martinez del Rio, C. M., 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 | 19046398PubMed |
Masci, K. D., Ponniah, M., and Hughes, J. M. (2008). Patterns of connectivity between the Lake Eyre and Gulf drainages, Australia: a phylogeographic approach. Marine and Freshwater Research 59, 751–760.
| Patterns of connectivity between the Lake Eyre and Gulf drainages, Australia: a phylogeographic approach.Crossref | GoogleScholarGoogle Scholar |
McCarthy, I. D., and Waldron, S. (2000). Identifying migratory Salmo trutta using carbon and nitrogen isotope ratios. Rapid Communications in Mass Spectrometry 14, 1325–1331.
| Identifying migratory Salmo trutta using carbon and nitrogen isotope ratios.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXls1yrsbo%3D&md5=1d743677318d0583fa599e903ddca75bCAS | 10920350PubMed |
McConnaughey, T. A., Burdett, J., Whelan, J. F., and Paull, C. K. (1997). Carbon isotopes in biological carbonates: respiration and photosynthesis. Geochimica et Cosmochimica Acta 61, 611–622.
| Carbon isotopes in biological carbonates: respiration and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsFagtrg%3D&md5=b09ad5fb8626c5e4fa80865357f3ccd3CAS |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsl2qurg%3D&md5=b2ea71c7379fee798030efc05327b9e0CAS |
Pinnegar, J. K., and Polunin, N. V. C. (1999). Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Functional Ecology 13, 225–231.
| Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions.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 |
Pratt, T. C., and Fox, M. G. (2002). Effect of fin clipping on overwinter growth and survival of age-0 walleyes. North American Journal of Fisheries Management 22, 1290–1294.
| Effect of fin clipping on overwinter growth and survival of age-0 walleyes.Crossref | GoogleScholarGoogle Scholar |
Pusey B., Kennard M., and Arthington A. (2004). ‘Freshwater Fishes of North-Eastern Australia.’ (CSIRO Publishing: Melbourne.)
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 | GoogleScholarGoogle Scholar | 19076260PubMed |
Rolfhus, K. R., Sandheinrich, M. B., Wiener, J. G., Bailey, S. W., Thoreson, K. A., et al. (2008). Analysis of fin clips as a nonlethal method for monitoring mercury in fish. Environmental Science & Technology 42, 871–877.
| Analysis of fin clips as a nonlethal method for monitoring mercury in fish.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFKhug%3D%3D&md5=50a915d62cff7393ec80598de35f61c1CAS | 18323115PubMed |
Sanderson, B. L., Tran, C. D., Coe, H. J., Pelekis, V., Steel, E. A., et al. (2009). Nonlethal sampling of fish caudal fins yields valuable stable isotope data for threatened and endangered fishes. Transactions of the American Fisheries Society 138, 1166–1177.
| Nonlethal sampling of fish caudal fins yields valuable stable isotope data for threatened and endangered fishes.Crossref | GoogleScholarGoogle Scholar |
Solomon, C. T., Weber, P. K., Cech, J. J., Ingram, B. L., Conrad, M. E., et al. (2006). Experimental determination of the sources of otolith carbon and associated isotopic fractionation. Canadian Journal of Fisheries and Aquatic Sciences 63, 79–89.
| Experimental determination of the sources of otolith carbon and associated isotopic fractionation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitFWitLY%3D&md5=5927f84a71c27af5d3909d1525224bc0CAS |
Suring, E., and Wing, S. R. (2009). Isotopic turnover rate and fractionation in multiple tissues of red rock lobster (Jasus edwardsii) and blue cod (Parapercis colias): consequences for ecological studies. Journal of Experimental Marine Biology and Ecology 370, 56–63.
| Isotopic turnover rate and fractionation in multiple tissues of red rock lobster (Jasus edwardsii) and blue cod (Parapercis colias): consequences for ecological studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvFGrtbk%3D&md5=01a17132adf9489cb663e9d941073a72CAS |
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 |
Thompson, D. A., and Blankenship, H. L. (1997). Regeneration of adipose fins given complete and incomplete clips. North American Journal of Fisheries Management 17, 467–469.
| Regeneration of adipose fins given complete and incomplete clips.Crossref | GoogleScholarGoogle Scholar |
Vander Haegen, G. E., Blankenship, H. L., Hoffmann, A., and Thompson, D. A. (2005). The effects of adipose fin clipping and coded wire tagging on the survival and growth of spring Chinook salmon. North American Journal of Fisheries Management 25, 1161–1170.
| The effects of adipose fin clipping and coded wire tagging on the survival and growth of spring Chinook salmon.Crossref | GoogleScholarGoogle Scholar |
Vander Zanden, M. J., Casselman, J. M., and Rasmussen, J. B. (1999). Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401, 464–467.
| Stable isotope evidence for the food web consequences of species invasions in lakes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmslyru78%3D&md5=3575e47be233b380931ebdc07876cfe3CAS |
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 | 12802678PubMed |
Winemiller, K. O. (1990). Spatial and temporal variation in tropical fish trophic networks. Ecological Monographs 60, 331–367.
| Spatial and temporal variation in tropical fish trophic networks.Crossref | GoogleScholarGoogle Scholar |
