Coupling stable isotopes with bioenergetics to evaluate sources of variation in organochlorine concentrations in Baltic salmon (Salmo salar)

Canadian Journal of Fisheries and Aquatic Sciences

Volumn 65, Issue 10, 2008, Pages 2114-2126

  Kiljunen, Mikko ^a   Peltonen, Heikki ^b   Jones, Roger I ^a   Kiviranta, Hannu ^c   Vuorinen, Pekka J ^d   Verta, Matti ^b   Karjalainen, Juha ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b FINNISH ENVIRONMENT INSTITUTE   (Finland)

^c NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^d FINNISH FOREST RESEARCH INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BIOENERGETICS; BIOLOGICAL INVASION; CONCENTRATION (COMPOSITION); DIET; GROWTH RESPONSE; LIPID; NITROGEN ISOTOPE; ORGANOCHLORINE; PREDATOR-PREY INTERACTION; SALMONID; SPATIAL VARIATION; STABLE ISOTOPE; TROPHIC STRUCTURE;

CERCOPAGIS PENGOI; SALMO SALAR;

EID: 54249119233     PISSN: 0706652X     EISSN: None     Source Type: Journal    
DOI: 10.1139/F08-121     Document Type: Article

References (72)

1. Ajah, P.O., and Nunoo, F.K.E. 2003. The effects of four preservation methods on length, weight and condition factor of the clupeid Sardinella aurita Val. 1847. J. Appl. Ichthyol. 19: 391-393. doi:10.1111/j.1439-0426.2003.00484.x.
2. Amrhein, J.F., Stow, C.A., and Wible, C. 1999. Whole-fish versus filet polychlorinated-biphenyl concentrations: an analysis using classification and regression tree models. Environ. Toxicol. Chem. 18: 1817-1823. doi:10.1897/1551-5028(1999) 018〈1817:WFVFPB〉2.3.CO;2.
3. Andersson, E. 1980. Merilohen ravinnosta syyspyyntikauden aikana itäisellä Suomelahdella [Diet of Baltic salmon (Salmo salar L.) in the Eastern Gulf of Finland during the autumn fishing season]. Riista- ja kalatalouden tutkimuslaitos, kalantutkimusosasto No. 15. [In Finnish.]
4. Beauchamp, D.A., Stewart, D.J., and Thomas, G.L. 1989. Corroboration of a bioenergetics model for sockeye salmon. Trans. Am. Fish. Soc. 118: 597-607. doi:10.1577/1548-8659(1989) 118〈0597:COABMF〉2.3.CO;2.
5. Becher, G., Nicolaysen, T., and Thomsen, C. 2001. Interlaboratory comparison on dioxins in food 2001. Folkehelsa, Final report 2001:4, Oslo, Norway. Available from www.fhi.no/eway/default. aspx?pid=238&trg= MainLeft_5853&MainArea_5811=5853:0:15,2829:1:0:0:0:0&MainLeft_5853=5825: 45081:1:5857:1:0:0 [accessed 30 April 2007].
6. Berglund, O., Larsson, P., and Broman, D. 2001. Organochlorine accumulation and stable isotope ratios in an Atlantic salmon (Salmo salar) population from the Baltic Sea. Sci. Total Environ. 281: 141-151. doi:10.1016/S0048-9697(01)00842-7. PMID:11778947.
7. Cabana, G., and Rasmussen, J.B. 1994. Modeling food-chain structure and contaminant bioaccumulation using stable isotope nitrogen isotopes. Nature (Lond.), 372: 255-257. doi:10.1038/372255a0.
8. Caut, S., Roemer, G.W., Donlan, C.J., and Courchamp, F. 2006. Coupling stable isotopes with bioenergetics to estimate interspecific interactions. Ecol. Appl. 16: 1893-1900. doi:10.1890/1051-0761(2006)016[1893:CSIWBT]2.0. CO;2. PMID:17069380.
9. Chen, J., Quana, X., Yazhia, Z., Yana, Y., and Yanga, F. 2001. Quantitative structure-property relationship studies on n-octanol/water partitioning coefficients of PCDD/Fs. Chemosphere, 44: 1369-1374. doi:10.1016/S0045-6535(00)00347-7. PMID:11513114.
10. DeNiro, M.J., and Epstein, S. 1978. Influence of diet on the distribution of carbon stable isotopes in animals. Geochim. Cosmochim. Acta, 42: 495-506. doi:10.1016/0016-7037(78)90199-0.
11. European Community. 2006. Commission regulation (EC) No. 199/ 2006, amending regulation (EC) No. 466/2001 setting maximum levels for certain contaminants in foodstuffs as regards dioxins and dioxin-like PCBs. Official Journal of the European Union 199/2006. Available from eur-lex.europa.eu/ LexUriServ/site/en/oj/2006/l_032/l_03220060204en00340038.pdf [accessed 14 August 2007].
12. Flinkman, J., Aro, E., Vuorinen, I., and Viitasalo, M. 1998. Changes in northern Baltic zooplankton and herring nutrition from 1980s to 1990s: top-down and bottom-up processes at work. Mar. Ecol. Prog. Ser. 165: 127-136. doi:10.3354/meps165127.
13. 13C data. Oecologia (Berl.), 115: 337-343. doi:10.1007/s004420050525.
14. Gorokhova, E., Hansson, S., Höglander, H., and Andersen, C.M. 2005. Stable isotopes show food web changes after invasion by the predatory cladoceran Cercopagis pengoi in a Baltic Sea bay. Oecologia (Berl.), 143: 251-259. doi:10.1007/s00442-004-1791-0.
15. oc of PCB congeners: a critical examination of data, assumptions and statistical approaches. Chemosphere, 39: 2209-2228. doi:10.1016/S0045-6535(99)00145-9.
16. Hanson, P.C., Johnson, T.B., Schindler, D.E., and Kitchell, J.F. 1997. Fish bioenergetics 3.0. University of Wisconsin Sea Grant Institute, Madison, Wis.
17. Hansson, S., Karlsson, L., Ikonen, E., Cristensen, O., Mitans, A., Uzars, D., Petersson, E., and Ragnarsson, B. 2001. Stomach analyses of Baltic salmon from 1959-1962 and 1994-1997: possible relation between diet and yolk-sac-fry mortality (M74). J. Fish Biol. 58: 1730-1745. doi:10.1006/jfbi.2001.1585.
18. Hebert, C.E., and Keenleyside, K.A. 1995. To normalize or not to normalize - fat is the question. Environ. Toxicol. Chem. 14: 801-807. doi:10.1897/1552-8618(1995)14[801:TNONTN]2.0.CO;2.
19. Heidarsson, T., Antonsson, T., and Snorrason, S. 2006. The relationship between body and scale growth proportions and validation of two back-calculation methods using individually tagged and recaptured wild Atlantic salmon. Trans. Am. Fish. Soc. 135: 1156-1164. doi:10.1577/T05-286.1.
20. Ikonen, E. 2006. The role of the feeding migration and diet of Atlantic salmon (Salmo salar L.) in yolk-sac-fry mortality (M74) in the Baltic Sea. Ph.D. thesis, Department of Biological and Environmental Science, University of Helsinki, Finland.
21. International Council for the Exploration of the Sea. 2006. Report of the Baltic salmon and trout assessment working group (WGBAST). ICES Advisory Commission on Fishery Management. ICES CM 2006/ACFM:21. Available from ices.dk/iceswork/wgdetailacfm.asp?wg=WGBAST [accessed 14 August 2007].
22. Isosaari, P., Vartiainen, T., Hallikainen, A., and Ruohonen, K. 2002. Feeding trial on rainbow trout: comparison of dry fish feed and Baltic herring as a source of PCDD/Fs and PCBs. Chemosphere, 48: 795-804. doi:10.1016/S0045-6535(02)00128-5. PMID:12222773.
23. Isosaari, P., Lundebye, A.K., Ritchie, G., Lie, O., Kiviranta, H., and Vartiainen, T. 2005. Dietary accumulation efficiencies and biotransformation of polybrominated diphenyl ethers in farmed Atlantic salmon (Salmo salar). Food Addit. Contam. 22: 829-837. doi:10.1080/02652030500195205. PMID:16192069.
24. Isosaari, P., Hallikainen, A., Kiviranta, H., Vuorinen, P.J., Parmanne, R., Koistinen, J., and Vartiainen, T. 2006. Polychlorinated dibenzo-p-dioxins, dibenzofurans, biphenyls, naphthalenes and polybrominated diphenyl ethers in the edible fish caught from the Baltic Sea and lakes in Finland. Environ. Pollut. 141: 213-225. doi:10.1016/j.envpol.2005.08.055. PMID:16226362.
25. Jackson, J. 1996. Contrast of constant and bioenergetics-based assimilation efficiencies in describing ecosystems. Ecol. Appl. 6: 1355-1364. doi:10.2307/2269613.
26. Jardine, T.D., Kidd, K.A., and Fisk, A.T. 2006. Applications, considerations, and source of uncertainty when using stable isotope analysis in toxicology. Environ. Sci. Technol. 40: 7501-7511. doi:10.1021/es061263h. PMID:17256487.
27. Johansen, G.O., Bogstad, B., Mehl, S., and Ulltang, Ø. 2004. Consumption of juvenile herring (Clupea harengus) by cod (Gadus morhua) in the Barents Sea: a new approach to estimating consumption in piscivorous fish. Can. J. Fish. Aquat. Sci. 61: 343-359. doi:10.1139/f03-168.
28. Kallio-Nyberg, I., and Ikonen, E. 1992. Migration patterns of two salmon stocks in the Baltic Sea. ICES J. Mar. Sci. 49: 191-198. doi:10.1093/icesjms/49.2.191.
29. Kallio-Nyberg, I., Peltonen, H., and Rita, H. 1999. Effects of stock-specific and environmental factors on the feeding migration of Atlantic salmon (Salmo salar) in the Baltic Sea. Can. J. Fish. Aquat. Sci. 56: 853-861. doi:10.1139/cjfas-56-5-853.
30. Karlsson, L., Ikonen, E., Mitans, A., and Hansson, S. 1999. The diet of salmon (Salmo salar) in the Baltic Sea and connections with the M74 syndrome. Ambio, 28: 37-42.
31. Kidd, K.A., Schindler, D.W., Hesslein, R.H., and Muir, D.C.G. 1995. Correlation between stable nitrogen isotope ratios and concentrations of organochlorines in biota from a freshwater food-web. Sci. Total Environ. 160-161: 381-390. doi:10.1016/0048-9697(95)04371-7.
32. Kidd, K.A., Schindler, D.W., Hesslein, R.H., and Muir, D.C.G. 1998. Effect of trophic position and lipid on organochlorine concentrations in fishes from subarctic lakes in Yukon Territory. Can. J. Fish. Aquat. Sci. 55: 869-881. doi:10.1139/cjfas-55-4-869.
33. 13C values from aquatic organisms, with implications for isotope mixing models. J. Appl. Ecol. 43: 1213-1222. doi:10.1111/j.1365-2664.2006.01224.x.
34. Kiljunen, M., Vanhatalo, M., Mäntyniemi, S., Peltonen, H., Kuikka, S., Kiviranta, H., Parmanne, R., Tuomisto, J., Vuorinen, P.J., Hallikainen, A., Verta, M., Pönni, J., Jones, R.I., and Karjalainen, J. 2007. Human dietary intake of organochlorines from Baltic herring: implications of individual fish variability and fisheries management. Ambio, 36: 257-264. doi:10.1579/0044-7447(2007)36[257:HDIOOF]2.0.CO;2. PMID:17520942.
35. Kiriluk, R.M., Servos, M.R., Whittle, D.M., Cabana, G., and Rasmussen, J.B. 1995. Using ratios of stable nitrogen and carbon isotopes to characterize the biomagnification of DDE, mirex, and PCB in a Lake Ontario pelagic foodweb. Can. J. Fish. Aquat. Sci. 52: 2660-2674.
36. Kiviranta, H., Vartiainen, T., Parmanne, R., Hallikainen, A., and Koistinen, J. 2003. PCDD/Fs and PCBs in Baltic herring during the 1990s. Chemosphere, 50: 1201-1216. doi:10.1016/S0045-6535(02)00481-2. PMID:12547334.
37. Kooijman, S.A.L.M. 2000. Dynamic energy and mass budgets in biological systems. 2nd ed. Cambridge University Press, Cambridge, UK.
38. Koskela, J., Pirhonen, J., and Jobling, M. 1997a. Effect of low temperature on feed intake, growth rate and body composition of juvenile Baltic salmon. Aquacult. Int. 5: 479-488. doi:10.1023/A:1018397014684.
39. Koskela, J., Pirhonen, J., and Jobling, M. 1997b. Feed intake, growth rate and body composition of juvenile Baltic salmon exposed to different constant temperatures. Aquacult. Int. 5: 351-360. doi:10.1023/A: 1018316224253.
40. Lehtiniemi, M., and Lindén, E. 2006. Cercopagis pengoi and Mysis spp. alter their feeding rate and prey selection under predation risk of herring (Clupea harengus membras). Mar. Biol. (Berl.), 149: 845-854. doi:10.1007/s00227-006-0243-2.
41. Leppäkoski, E., Gollasch, S., Gruszka, P., Ojaveer, H., Olenin, S., and Panov, V. 2002. The Baltic - a sea of invaders. Can. J. Fish. Aquat. Sci. 59: 1175-1188. doi:10.1139/f02-089.
42. Lindström, G., Småstuen Haug, L., and Nicolaysen, T. 2000. International intercalibration on dioxin in food 2000. Folkehelsa, Final report 2000:9, Oslo, Norway. Available from www.fhi.no/eway/default.aspx?pid= 238&trg=MainLeft_5853&MainArea_5811=5853:0:15,2829:1:0:0:0: 0&MainLeft_5853=5825:45081:1:5857:1:0:0 [accessed 30 April 2007].
43. Lundebye, A.K., Berntssen, M.H.G., Lie, O., Ritchie, G., Isosaari, P., Kiviranta, H., and Vartiainen, T. 2004. Dietary uptake of dioxins (PCDD/PCDFs) and dioxin-like PCBs in Atlantic salmon (Salmo salar). Aquacult. Nutr. 10: 199-207. doi:10.1111/j.1365-2095.2004.00299.x.
44. Mackay, D., Shiu, W.Y., and Ma, K.C. 1997. Illustrated handbook of physical-chemical properties and environmental fate for organic chemicals. Vols. I-V. Lewis Publishers, Boca Raton (Fla.), Ann Arbor (Mich.), London (UK).
45. Madenjian, C.P., Carpenter, S.R., and Rand, P.S. 1994. Why are the PCB concentrations of salmonine individuals from the same lake so highly variable? Can. J. Fish. Aquat. Sci. 51: 800-807. doi:10.1139/f94-078.
46. Meakins, R.H. 1976. Variations in energy content of freshwater fish. J. Fish Biol. 8: 221-224. doi:10.1111/j.1095-8649.1976.tb03945.x.
47. Möllmann, C., Kornilovs, G., Fetter, M., and Köster, F.W. 2004. Feeding ecology of central Baltic Sea herring and sprat. J. Fish Biol. 65: 1563-1581. doi:10.1111/j.0022-1112.2004.00566.x.
48. Parmanne, R., Hallikainen, A., Isosaari, P., Kiviranta, H., Koistinen, J., Laine, O., Rantakokko, P., Vuorinen, P.J., and Vartiainen, T. 2006. The dependence of organohalogen compound concentrations on herring age and size in the Bothnian Sea, northern Baltic. Mar. Pollut. Bull. 52: 149-161. doi:10.1016/j.marpolbul.2005.08.013. PMID:16212986.
49. Paterson, G., Drouillard, K.G., and Haffner, G.D. 2006. An evaluation of stable nitrogen isotopes and polychlorinated biphenyls as bioenergetic tracers in aquatic systems. Can. J. Fish. Aquat. Sci. 63: 628-641. doi:10.1139/f05-241.
50. Peltonen, H., Vinni, M., Lappalainen, A., and Pönni, J. 2004. Spatial feeding patterns of herring (Clupea harengus L.), sprat (Sprattus sprattus L.), and the three-spined stickleback (Gasterosteus aculeatus L.) in the Gulf of Finland, Baltic Sea. ICES J. Mar. Sci. 61: 966-971. doi:10.1016/j.icesjms.2004.06.008.
51. Peltonen, H., Kiljunen, M., Kiviranta, H., Vuorinen, P.J., Verta, M., and Karjalainen, J. 2007. Predicting effects of exploitation rate on weight-at-age, population dynamics and bioaccumulation of PCDD/Fs and PCBs in herring (Clupea harengus L.) in the northern Baltic Sea. Environ. Sci. Technol. 41: 1849-1855. doi:10.1021/es0618346.
52. Phillips, D.L. 2001. Mixing models in analyses of diet using multiple stable isotopes: a critique. Oecologia (Berl.), 127: 166-170. doi:10.1007/s004420000571.
53. Raymond, W.F., Canaway, R.J., and Harris, C.E. 1957. An automatic bomb calorimeter. J. Sci. Instrum. 34: 501-503. doi:10.1088/0950-7671/34/12/ 306.
54. 15N of size-fractionated plankton at a coastal station in the northern Baltic proper. Mar. Ecol. Prog. Ser. 203: 47-65. doi:10.3354/meps203047.
55. Rolff, C., and Elmgren, R. 2000. Use of riverine organic matter in plankton food webs of the Baltic Sea. Mar. Ecol. Prog. Ser. 197: 81-101. doi:10.3354/meps197081.
56. Rönkkönen, S., Ojaveer, E., Raid, T., and Viitasalo, M. 2004. Long-term changes in Baltic herring (Clupea harengus membras) growth in the Gulf of Finland. Can. J. Fish. Aquat. Sci. 61: 219-229. doi:10.1139/f03-167.
57. Salminen, M., Kuikka, S., and Erkamo, E. 1994. Divergence in the feeding migration of Baltic salmon (Salmo salar L.): the significance of smolt size. In Workshop on the postsmolt biology of salmonids in ranching systems, 10-12 November 1992, Umeå, Sweden. Edited by T. Eriksson and T. Järvi. Nord. J. Freshw. Res. 69: 32-42.
58. Salminen, M., Erkamo, E., and Salmi, J. 2001. Diet of post-smolt and one-sea-winter Atlantic salmon in the Bothnian Sea, Northern Baltic. J. Fish Biol. 58: 16-35. doi:10.1111/j.1095-8649. 2001.tb00496.x.
59. Sharma, M., McBean, E., and Gowing, A. 2007. Bioconcentration of dioxins and furans in vegetation. Water Air Soil Pollut. 179: 117-124. doi:10.1007/s11270-006-9218-7.
60. Småstuen Haug, L., and Becher, G. 2006. Interlaboratory comparison on dioxins in food 2006. Seventh round of an international study, Final report, rapport 2006:7, Oslo, Norway. Available from www.fhi.no/eway/default.aspx?pid= 238&trg=MainLeft_5895&MainArea_5811=5895:0:15,2829:1:0:0:0: 0&MainLeft_5895=5825:59499:1:5896:1:0:0 [accessed 30 April 2007].
61. Smith, C., and Wootton, R.J. 1995. Experimental analysis of some factors affecting parental expenditure and investment in Gasterosteus acuelatus (Gasterosteidae). Environ. Biol. Fishes, 43: 63-76. doi:10.1007/ BF00001818.
62. 15N fractionation in fishes. J. Exp. Mar. Biol. Ecol. 340: 1-10. doi:10.1016/j.jembe.2006.07.023.
63. Syväranta, J., Hämäläinen, H., and Jones, R.I. 2006. Within-lake variability in carbon and nitrogen stable isotope signatures. Freshw. Biol. 51: 1090-1102. doi:10.1111/j.1365-2427.2006.01557.x.
64. 13C-depleted carbon in the Procellariiformes. Mar. Ecol. Prog. Ser. 208: 265-271. doi:10.3354/meps208265.
65. Türker Saçan, M., and Inel, Y. 1995. Application of the characteristic root index model to the estimation of N-octanol/water partition coefficients. Polychlorinated biphenyls. Chemosphere, 30: 39-50. doi:10.1016/0045-6535(94)00375-5.
66. van den Berg, M., Birnbaum, L., Bosveld, A.T.C., Brunstrom, B., Cook, P., Feeley, M., Giesy, J.P., Hanberg, A., Hasegawa, R., Kennedy, S.W., Kubiak, T., Larsen, J.C., van Leeuwen, F.X.R., Liem, A.K.D., Nolt, C., Peterson, R.E., Poellinger, L., Safe, S., Schrenk, D., Tillitt, D., Tysklind, M., Younes, M., Waern, F., and Zacharewski, T. 1998. Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wildlife. Environ. Health Perspect. 106: 775-792. Available from ehpnet1.niehs.nih.gov/ docs/1998/106p775-792vandenberg/ abstract.html [accessed 14 August 2007]. doi:10.2307/3434121. PMID:9831538.
67. 15N) and literature dietary data. Can. J. Fish. Aquat. Sci. 54: 1142-1158. doi:10.1139/cjfas-54-5-1142.
68. Velinsky, D.J., and Fogel, M.L. 1999. Cycling of dissolved and particulate nitrogen and carbon in the Framvaren Fjord, Norway: stable isotopic variations. Mar. Chem. 67: 161-180. doi:10.1016/S0304-4203(99)00057-2.
69. Vuorinen, P.J., Paasivirta, J., Keinänen, M., Koistinen, J., Rantio, T., Hyötyläinen, T., and Welling, L. 1997. The M74 syndrome of Baltic salmon (Salmo salar) and organochlorine concentrations in the muscle of female salmon. Chemosphere, 34: 1151-1166. doi:10.1016/S0045-6535(97) 00415-3.
70. Vuorinen, P.J., Parmanne, R., Vartiainen, T., Keinänen, M., Kiviranta, H., Kotovuori, O., and Halling, F. 2002. PCDD, PCDF, PCB and thiamine in Baltic herring (Clupea harengus L.) and sprat [Sprattus sprattus (L.)] as a background to the M74 syndrome of Baltic salmon (Salmo salar L.). ICES J. Mar. Sci. 59: 480-496. doi:10.1006/jmsc.2002.1200.
71. Winberg, G.G. 1960. Rate of metabolism and food requirements of fishes. Fish. Res. Board Can. Transl. Ser. No. 194.
72. Zheng, G., Huang, W.H., and Lu, X.H. 2003. Prediction of n-octanol/ water partition coefficients for polychlorinated dibenzo-p-dioxins using a general regression neural network. Anal. Bioanal. Chem. 376: 680-685. doi:10.1007/s00216-003-1910-5. PMID:12761606.