Important sources of variation to be considered when using fin clips as a surrogate for muscle in trophic studies using stable isotopes
David E. Galván A D , Manuela Funes B , Ana L. Liberoff A , Florencia Botto C and Oscar O. Iribarne C
+ Author Affiliations
- Author Affiliations
A Centro Nacional Patagónico, Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Boulevard Brown 2915, (U9120ACV) Puerto Madryn, Chubut, Argentina.
B Facultad de Ciencias Naturales (FCN) – Universidad Nacional de la Patagonia, Boulevard Brown 3051, (U9120ACV) Puerto Madryn, Chubut, Argentina.
C Laboratorio de Ecología, Instituto de Investigaciones Marinas y Costeras (IIMyC), CONICET – UNMDP – 3er Piso, Funes 3250, (B7600WAG) Mar del Plata, Argentina.
D Corresponding author. Email: galvan@cenpat-conicet.gob.ar
Marine and Freshwater Research 66(8) 730-738 https://doi.org/10.1071/MF13346
Submitted: 31 December 2013 Accepted: 18 September 2014 Published: 10 March 2015
Abstract
White muscle is the prevalent tissue for C and N stable isotope analysis in fish, requiring the death of the fish or biopsy procedures that could lead to infections or severe damage. Given that caudal fin-clipping does not seriously affect growth or condition, the present study assessed the suitability of caudal fin tissue as replacement for muscle tissue in trophic studies. Clips of caudal fin were a useful non-lethal surrogate of muscle samples in four studied reef-fish (Diplodus argenteus, Pagrus pagrus, Acanthistius patachonicus and Pinguipes brasilianus). Fin clips were easy to collect in quantities adequate for mass spectrometry analyses and had C : N ratios similar to those of white muscle with low lipid content. However, results showed that fin-muscle correction models should be specific and sampling design should be conducted to reduce spatial and temporal variation. Moreover, species-specific correction factors may not be valid for other populations of the same species if the presumed range of δX values differ from the population used to estimate the correction models. Results also showed that the fin-muscle relationship could vary with size. Thus, unless a non-ecological meaningful fin-muscle correlation with body size was previously identified, correction models should be estimated sampling a representative size range and fin samples should be used with caution to study size-related trophodynamics.
Additional keywords: carbon, growth, marine fish, nitrogen, sampling design, trophodynamic.
References
Andvik, R. T., VanDeHey, J. A., Fincel, M. J., French, W. E., Bertrand, K. N., Chipps, S. R., Klumb, R. A., and Graeb, B. D. S. (2010). Application of non-lethal stable isotope analysis to assess feeding patterns of juvenile pallid sturgeon Scaphirhynchus albus: a comparison of tissue types and sample preservation methods. Journal of Applied Ichthyology 26, 831–835.| Application of non-lethal stable isotope analysis to assess feeding patterns of juvenile pallid sturgeon Scaphirhynchus albus: a comparison of tissue types and sample preservation methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1emt7vE&md5=25dfc04fd1a238f66b5c2b9e8ab09ff4CAS |
Böckelmann, P. K., and Bechara, I. J. (2009). The regeneration of the tail fin actinotrichia of carp (Cyprinus carpio, Linnaeus, 1758) under the action of naproxen. Brazilian Journal of Biology 69, 1165–1172.
| The regeneration of the tail fin actinotrichia of carp (Cyprinus carpio, Linnaeus, 1758) under the action of naproxen.Crossref | GoogleScholarGoogle Scholar |
Brankevich, A., Roux, A., and Bastida, R. (1990). Relevamiento de un banco de besugo (Spagrus pagrus) en la plataforma bonaerense. Carcterísticas fisiográficas generales y aspectos ecológicos preliminares. Frente Marítimo 7, 75–86.
Church, M. R., Ebersole, J. L., Rensmeyer, K. M., Couture, R. B., Barrows, F. T., and Noakes, D. L. G. (2009). Mucus: a new tissue fraction for rapid determination of fish diet switching using stable isotope analysis. Canadian Journal of Fisheries and Aquatic Sciences 66, 1–5.
| Mucus: a new tissue fraction for rapid determination of fish diet switching using stable isotope analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1agt7c%3D&md5=211d99453275ec0a09b806d7d02e3166CAS |
Crawley, M. J. (2007). ‘The R book.’ (Wiley: Chichester, UK.)
DeNiro, M. J., and Epstein, S. (1976). You are what you eat (plus a few ‰) the carbon isotope cycle in food chains. Geological Society of America 6, 834–835.
Dietrich, J. P., and Cunjak, R. A. (2006). Evaluation of the impacts of Carlin tags, fin clips, and Panjet tattoos on juvenile Atlantic salmon. North American Journal of Fisheries Management 26, 163–169.
| Evaluation of the impacts of Carlin tags, fin clips, and Panjet tattoos on juvenile Atlantic salmon.Crossref | GoogleScholarGoogle Scholar |
Dubiaski-Silva, J., and Masunari, S. (2006). Ontogenetic and seasonal variation in the diet of Marimbá, Diplodus argenteus (Valenciennes, 1830) (Pisces, Sparidae) associated with the beds of Sargassum cymosum C. Agardh, 1820 (Phaeophyta) at Ponta das Garoupas, Bombinhas, Santa Catarina. Journal of Coastal Research SI, 1190–1192.
Estrada, J. A., Lutcavage, M., and Thorrold, S. R. (2005). Diet and trophic position of Atlantic bluefin tuna (Thunnus thynnus) inferred from stable carbon and nitrogen isotope analysis. Marine Biology 147, 37–45.
| Diet and trophic position of Atlantic bluefin tuna (Thunnus thynnus) inferred from stable carbon and nitrogen isotope analysis.Crossref | GoogleScholarGoogle Scholar |
Fincel, M. J., Vandehey, J. A., and Chipps, S. R. (2012). Non-lethal sampling of walleye for stable isotope analysis: a comparison of three tissues. Fisheries Management and Ecology 19, 283–292.
| Non-lethal sampling of walleye for stable isotope analysis: a comparison of three tissues.Crossref | GoogleScholarGoogle Scholar |
Funes, M., Liberoff, L., and Galván, D. E. (2014). Cambios tamaño-dependientes en la dieta de peces marinos y su estudio mediante análisis de isótopos estables. Ecología Austral 24, 118–126.
Galván, D. E., Venerus, L., Irigoyen, A., Parma, A. M., and Gosztonyi, A. (2005). Extension of the distributional range of the silver porgy, Diplodus argenteus (Valenciennes 1830), and the red porgy, Pagrus pagrus (Linnaeus 1758) (Sparidae) in northern Patagonia, south-western Atlantic. Journal of Applied Ichthyology 21, 444–447.
| Extension of the distributional range of the silver porgy, Diplodus argenteus (Valenciennes 1830), and the red porgy, Pagrus pagrus (Linnaeus 1758) (Sparidae) in northern Patagonia, south-western Atlantic.Crossref | GoogleScholarGoogle Scholar |
Galván, D. E., Botto, F., Parma, A. M., Bandieri, L., Mohamed, N., and Iribarne, O. (2009a). Food partitioning and spatial subsidy in shelter-limited fish species inhabiting patchy reefs of Patagonia. Journal of Fish Biology 75, 2585–2605.
| Food partitioning and spatial subsidy in shelter-limited fish species inhabiting patchy reefs of Patagonia.Crossref | GoogleScholarGoogle Scholar | 20738509PubMed |
Galván, D. E., Venerus, L. A., and Irigoyen, A. J. (2009b). The reef-fish fauna of the Northern Patagonian gulfs, Argentina, southwestern Atlantic. The Open Fish Science Journal 2, 90–98.
| The reef-fish fauna of the Northern Patagonian gulfs, Argentina, southwestern Atlantic.Crossref | GoogleScholarGoogle Scholar |
Galván, D. E., Sweeting, C. J., and Reid, W. D. K. (2010). Power of stable isotope techniques to detect size-based feeding in marine fishes. Marine Ecology Progress Series 407, 271–278.
| Power of stable isotope techniques to detect size-based feeding in marine fishes.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 |
Greenwood, N. D. W., Sweeting, C. J., and Polunin, N. V. C. (2010). Elucidating the trophodynamics of four coral reef fishes of the Solomon Islands using δ15N and δ13C. Coral Reefs 29, 785–792.
| Elucidating the trophodynamics of four coral reef fishes of the Solomon Islands using δ15N and δ13C.Crossref | GoogleScholarGoogle Scholar |
Hanisch, J. R., Tonn, W. M., Paszkowski, C. A., and Scrimgeour, G. J. (2010). δ13C and δ15N signatures in muscle and fin tissues: nonlethal sampling methods for stable isotope analysis of salmonids. North American Journal of Fisheries Management 30, 1–11.
| δ13C and δ15N signatures in muscle and fin tissues: nonlethal sampling methods for stable isotope analysis of salmonids.Crossref | GoogleScholarGoogle Scholar |
Heady, W. N., and Moore, J. W. (2013). Tissue turnover and stable isotope clocks to quantify resource shifts in anadromous rainbow trout. Oecologia 172, 21–34.
| Tissue turnover and stable isotope clocks to quantify resource shifts in anadromous rainbow trout.Crossref | GoogleScholarGoogle Scholar | 23183819PubMed |
Hesslein, R., Hallard, K., and Ramial, P. (1993). Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in responce 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 responce to a change in diet traced by δ34S, δ13C, and δ15N.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXktVOqs7o%3D&md5=17d069a942f5cb365ce63adf95425ec4CAS |
Huntingford, F. A., Adams, C., Braithwaite, V. A., Kadri, S., Pottinger, T. G., Sandoe, P., and Turnbull, J. F. (2006). Current issues in fish welfare. Journal of Fish Biology 68, 332–372.
| Current issues in fish welfare.Crossref | GoogleScholarGoogle Scholar |
Irigoyen, A., and Galván, D.E. (Eds) (2009). ‘Peces de Arrecife Argentinos.’ (Proyecto Arrecife: Puerto Madryn, Argentina.)
Jardine, T., Gray, M., Mc William, S., and Cunjak, R. (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=fb37d8b9f5eae17b5df618c9a6ed3b5aCAS |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtFGmsQ%3D%3D&md5=7e811c341da7b9e8e74bb3b643fa4e53CAS |
Jiao, Y., Chen, Y., Schneider, D., and Wroblewski, J. (2004). A simulation study of impacts of error structure on modeling stock recruitment data using generalized linear models. Canadian Journal of Fisheries and Aquatic Sciences 61, 122–133.
| A simulation study of impacts of error structure on modeling stock recruitment data using generalized linear models.Crossref | GoogleScholarGoogle Scholar |
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 |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXls1yrsbo%3D&md5=e1b67f81afbdb32ee2284d04e71def17CAS | 10920350PubMed |
Miller, T. (2006). Tissue-specific response of δ15N in adult Pacific herring (Clupea pallasi) following an isotopic shift in diet. Environmental Biology of Fishes 76, 177–189.
| Tissue-specific response of δ15N in adult Pacific herring (Clupea pallasi) following an isotopic shift in diet.Crossref | GoogleScholarGoogle Scholar |
Perga, M. E., and Gerdeaux, D. (2005). ‘Are fish what they eat’ all year round? Oecologia 144, 598–606.
| ‘Are fish what they eat’ all year round?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MvmvVOhsw%3D%3D&md5=5c0cc2ed58303caaaa3ebac1d074bdfaCAS | 15891838PubMed |
Pinnegar, J., 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 |
R Development Core Team (2012). R: A language and environment for statistical computing. (R Foundation for Statistical Computing: Vienna, Austria.) Available at: http://www.R-project.org [Verified February 2012].
Rodgers, K., and Wing, S. (2008). Spatial structure and movement of blue cod Parapercis colias in Doubtful Sound, New Zealand, inferred from δ13C and δ15N. Marine Ecology Progress Series 359, 239–248.
| Spatial structure and movement of blue cod Parapercis colias in Doubtful Sound, New Zealand, inferred from δ13C and δ15N.Crossref | GoogleScholarGoogle Scholar |
Sanderson, B. L., Tran, C. D., Coe, H. J., Pelekis, V., Steel, E. A., and Reichert, W. L. (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 |
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 |
Sweeting, C. J., Polunin, N. V. C., and Jennings, S. (2006). Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Communications in Mass Spectrometry 20, 595–601.
| Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhslOns70%3D&md5=d5e0eb66ea7870420427e8a7887ec254CAS | 16429479PubMed |
Sweeting, C. J., Barry, J. P., Barnes, C., Polunin, N. V. C., and Jennings, S. (2007a). Effects of body size and environment on diet-tissue δ15N fractionation in fishes. Journal of Experimental Marine Biology and Ecology 340, 1–10.
| Effects of body size and environment on diet-tissue δ15N fractionation in fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1SgsbfL&md5=427cf132fb7bede799503ce4129ff046CAS |
Sweeting, C. J., Barry, J. P., Polunin, N. V. C., and Jennings, S. (2007b). Effects of body size and environment on diet-tissue δ13C fractionation in fishes. Journal of Experimental Marine Biology and Ecology 352, 165–176.
| Effects of body size and environment on diet-tissue δ13C fractionation in fishes.Crossref | GoogleScholarGoogle Scholar |
Tronquart, N. H., Mazeas, L., Reuilly-Manenti, L., Zahm, A., and Belliard, J. (2012). Fish fins as non-lethal surrogates for muscle tissues in freshwater food web studies using stable isotopes. Rapid Communications in Mass Spectrometry 26, 1603–1608.
| Fish fins as non-lethal surrogates for muscle tissues in freshwater food web studies using stable isotopes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1Wrtrs%3D&md5=f13e61f39005b7cc63bba17dd07d97cbCAS |
Valladares, S., and Planas, M. (2012). Non-lethal dorsal fin sampling for stable isotope analysis in seahorses. Aquatic Ecology 46, 363–370.
| Non-lethal dorsal fin sampling for stable isotope analysis in seahorses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFSltrbJ&md5=71a47f2533feaaf32aa63c1a5df4815cCAS |
Watanabe, Y., Seikai, T., and Tominaga, O. (2005). Estimation of growth and food consumption in juvenile Japanese flounder Paralichthys olivaceus using carbon stable isotope ratio δ13C under laboratory conditions. Journal of Experimental Marine Biology and Ecology 326, 187–198.
| Estimation of growth and food consumption in juvenile Japanese flounder Paralichthys olivaceus using carbon stable isotope ratio δ13C under laboratory conditions.Crossref | GoogleScholarGoogle Scholar |
Willis, T., Sweeting, C., Bury, S., Handley, S., Brown, J., Freeman, D., Cairney, D., and Page, M. (2013). Matching and mismatching stable isotope (δ13C and δ15N) ratios among fish species in fin and muscle tissue: a critical review. Marine Biology 160, 1633–1644.
| Matching and mismatching stable isotope (δ13C and δ15N) ratios among fish species in fin and muscle tissue: a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVSmtrrN&md5=52261bb020ca3fa345ba02d201095b2bCAS |
Wills, A. A., Kidd, A. R., Lepidina, A., and Poss, K. D. (2008). Fgfs control homeostatic regeneration in adult zebrafish fins. Development 135, 3063–3070.
| Fgfs control homeostatic regeneration in adult zebrafish fins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlansrbI&md5=c85585e76360071c85a7f95f31d6e07bCAS | 18701543PubMed |
