Abstract
Pulp mill effluent is known to affect freshwater biota in various ways. However, its effects on riparian birds that feed on insects emerging from aquatic ecosystems have not been examined. This study examined diet, circulating sex steroids, highly carboxylated porphyrins (HCPs), activity of the mixed function oxygenase enzyme 7-ethoxyresorufin-O-deethylase (EROD), the liver somatic index and reproductive performance and nestling size in tree swallows, an insectivorous bird, at sites located upstream and downstream from two pulp mills in western Canada during 1993–1996. The tree swallow diet consisted of 50–60% insects of aquatic origin. In general, physiological biomarkers in tree swallows located downstream from the pulp mill effluents did not differ from those at upstream sites, suggesting that dietary exposures to pulp mill effluents at these sites were insufficient to elicit responses. Nevertheless, it is noteworthy that 17β-oestradiol was lower in incubating females at a site downstream from one of the pulp mills in 1 of 2 years. In addition, HCPs in tree swallows downstream from the other pulp mill were elevated significantly. Reproductive performance by tree swallows did not differ significantly between upstream and downstream locations at either mill although there was a definite trend towards enhanced reproduction at downstream sites. At both pulp mills, 16 day old nestlings were significantly larger at downstream sites compared to their counterparts at upstream sites in at least 1 year. The improved reproduction and larger nestlings at downstream sites may be the result of a greater food supply, consistent with the nutrient enrichment effect often seen below pulp mills.
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References
Adams, S.M., Ham, K.D., Greeley, M.S., LeHew, R.F., Hinton, D.E. and Saylor, C.F. (1996) Downstream gradients in bioindicator responses: point sources contaminant effects on fish health. Can. J. Fish. Aquatic Sci. 53, 2177–87.
Anderson, A.M. (1989) An Assessment of the Effects of the Combined Pulp Mill and Municipal Effluents at Hinton on the Water Quality and Zoobenthos of the Athabasca River. Edmonton, Alberta: Environmental Quality Monitoring Branch, Alberta Environmental Protection.
Ankley, G.T., Niemi, G.J., Lodge, K.B., Hallett, J.H., Beaver, D.L., Tillitt, O.E., Schwuitz, T.R., Geisy, J.P., Jones, P.D. and Hagley, C. (1993) Uptake of planar polychlorinated biphenyls and 2,3,7,8-substituted polychlorinated dibenzofurans and dibenzop- dioxins by birds nesting in the lower Fox River and Green Bay Wisconsin USA. Arch. Environ. Contam. Toxicol. 24, 332–44.
Bishop, C.A., Koster, M.D., Chek, A.A., Hussell, D.J.T. and Jock, K. (1995) Chlorinated hydrocarbons and mercury in sediments, red-winged blackbirds (Agelaeuis phoeniceus) and tree swallows (Tachycineta bicolor) from wetlands in the Great Lakes-St Lawrence River system. Environ. Toxicol. Chem. 14, 491–501.
Blancher, P.J. and McNicol, D.K. (1988) Breeding biology of tree swallows in relation to wetland acidity. Can. J. Zool. 66, 842–9.
Blancher, P.J. and McNicol, D.K. (1991) Tree swallow diet in relation to wetland acidity. Can. J. Zool. 69, 2629–37.
Bluhm, C.K. (1988) Temporal patterns of pair formation and reproduction in annual cycles and associated endocrinology in waterfowl. In R.F. Johnston (ed.) Current ornithology, Vol. 5, pp. 123–85. New York: Plenum Press.
Bothwell, M.L. (1992) Eutrophication of rivers by nutrients in treated kraft pulp mill effluent Water Pollut. Res. J. Can. 27, 447–72.
Brown, S.B., Evans, R.E. and Vandenbyllaardt, L. (1996) Analyses for Circulating Gonadal Sex Steroids and Gonad Morphology in Fish, Peace, Athabasca and Slave River basins, September to December 1994, Edmonton: Northern River Basins Study Project.
Burnison, B.K., Comba, M.E. and Carey, J.H. (1997) Isolation and tentative identification of the compound responsible for fish MFO-induction in BKME. In J.S. Goudey, S.M. Swanson, M.D. Treissman and A.J. Niimi (eds) Proceedings of the 23rd Annual Aquatic Toxicity Workshop, pp. 86–7. Calgary: Can. Tech. Rept. Fish. Aquat. Sci.
Cash, K.J., Ouellet, M.S.J., Wrona, F.J. and Wagner, G. (1996) An Assessment of the Utility of Benthic Macroinvertebrate and Fish Community Structure in Biomonitoring, Peace, Athabasca and Slave River Basins, Edmonton: Northern River Basins Study.
Conover, W.J. and Iman, R.L. (1981) Rank transformations as a bridge between parametric and non-parametric statistics. Am. Stat. 35, 124–129.
Desteven, D. (1978) The influence of age on the breeding biology of the tree swallow Iridoprocne bicolor. Ibis 120, 516–23.
Dillon, W.R. and Goldstein, M. (1984) Multivariate Analysis: Methods and Applications. New York: John Wiley & Sons.
Dunn, P.O. and Hannon, S.J. (1992) Effects of food abundance and male parental care on reproductive success and monogamy in tree swallows. Auk 109, 488–99.
Edgington, E.S. (1995) Randomization Tests, 2nd edn. New York: Marcel Dekker.
Eeva, T., Lehikoinen, E. and Pohjalainen, T. (1997) Pollution-related variation in food supply and breeding success in two holenesting passerines. Ecology 78, 1120–31.
Elliott, J.E., Kennedy, S.W. and Lorenzen, A. (1997) Comparative toxicity of polychlorinated biphenyls to Japanese quail (Coturnix c-japonica) and American kestrels (Falco sparverius). J. Toxicol. Environ. Health 51, 57–75.
Environment Canada and Fisheries and Oceans Canada (1992) Aquatic Environmental Effects Monitoring Requirements. Ottawa: Environmental Protection Service.
Fox, G.A., Kennedy, S.W., Norstrom, R.J. and Wigfield, D.C. (1988) Pophyria in herring gulls: a biochemical response to chemical contamination of Great Lakes food chains. Environ. Toxicol. Chem. 7, 831–9.
Fraikin, C.G.J., Swanson, S.M., Holley, K., Graham, D.M. and Firth, B.K. (1997) Environmental effects monitoring: trends in an ecosystem's response with technological changes at pulpmill. In J.S. Goudey, S.M., Swanson, M.D. Treissman and A.J. Niimi (eds) Proceedings of the 23rd Annual Aquatic Toxicity Workshop pp. 137–38. Calgary: Can. Tech. Rept. Fish. Aquat. Sci.
Gagnon, M.M., Dodson, J.J., Hodson, P.V., Van Der Kraak, G. and Carey, J.H. (1994) Seasonal effects of bleached kraft mill effluent on reproductive parameters of white sucker (Catostomus commersoni) populations of the St Maurice River, Quebec, Canada. Can. J. Fish. Aquatic Sci. 51, 337–47.
Gagnon, M.M., Bussieres, D., Dodson, J.J. and Hodson, P.V. (1995) White sucker (Catostomus commersoni) growth and sexual maturation in pulp mill-contaminated and reference rivers. Environ. Toxicol. Chem. 14, 317–27.
Goldstein, J.A., Hickman, P. and Jue, D.L. (1974) Experimental hepatic porphyria induced by polychlorinated biphenyls. Toxicol. Appl. Pharmacol. 27, 437–48.
Government of Canada (1991) Effluents from Pulp Mills using Bleaching. Ottawa: Canadian Environmental Protection Act, Priority Substances List Assessment Report.
Haley, R.K., Hall, T.J. and Bousquet, T.M. (1995) Effects of biologically treated bleached-kraft mill effluent before and after mill conversion to increased chlorine dioxide substitution: results of an experimental streams study. Environ. Toxicol. Chem. 14, 287–98.
Hall, T.J., Haley, R.K. and LaFleur, L.E. (1991) Effects of biologically-treated bleached kraft mill effluent on cold water stream productivity in experimental stream channels. Environ. Toxicol. Chem. 10, 1051–60.
Hewitt, L.M., Carey, J.H., Dixon, D.G. and Munkittrick, K.R. (1996) Examination of bleached kraft mill effluent fractions for potential inducers of mixed function oxygenase activity in rainbow trout. In M.R. Servos, K.R. Munkittrick, J.H. Carey and G.J. Van Der Kraak (eds) Environmental fate and effects of pulp and paper mill effluents, pp. 79–94. Delray Beach, FL: St Lucie Press.
Hodson, P.V. (1996) Mixed function oxygenase induction by pulp mill effluents: advances since 1991. In M.R. Servos, K.R. Munkittrick, J.H. Carey and G.J. Van Der Kraak (eds) Environmental fate and effects of pulp and paper mill effluents, pp. 349–58. Delray Beach, FL: St Lucie Press.
Hodson, P.V., McWhirter, M., Ralph, K., Gray, B., Thivierge, D., Carey, J.H., Van Der Kraak, G., Whittle, D.M. and Levesque, M.C. (1992) Effects of bleached kraft mill effluent on fish in the St Maurice River, Quebec. Environ. Toxicol. Chem. 11, 1635–51.
Holroyd, G.L. (1983) Foraging strategies and food of a swallow guild. PhD dissertation, University of Toronto, Toronto.
Hussell, D.J.T. (1983) Age and plumage color in female tree swallows. J. Field Ornithol. 54, 312–18.
Hussell, D.J.T. and Quinney, T.E. (1986) Food abundance and clutch size of tree swallows Tachycineta bicolor. Ibis 129, 243–58.
Johnson, E.J. Best, L.B. and Heagy, P.A. (1980) Food sampling bias associated with the ‘ligature method’. Condor 82, 186–92.
Kennedy, S.W. and James, C.A. (1993) Improved method to extract and concentrate porphyrins from liver tissue for analysis by high performance liquid chromatography. J. Chromatogr. Biomed. Appl. 619, 127–32.
Kennedy, S.W., Lorenzen, A., Jones, S.P., Hahn, M.E. and Stegeman, J.J. (1996) Cytochrome P4501A induction in avian hepatocyte cultures: a promising approach for predicting the sensitivity of avian species to toxic effects of halogenated aromatic hydrocarbons. Toxicol. Appl. Pharmacol. 141, 214–30.
Kloepper-Sams, P.J. and Benton, E. (1994) Exposure of fish to biologically-treated bleached kraft mill effluent. 2. Induction of hepatic cytochrome P4501A in mountain whitefish (Prosopium williamsoni) and other species. Environ. Toxicol. Chem. 13, 1483–96.
Kloepper-Sams, P.J., Swanson, S.M., Marchant, T., Schreyer, R. and Owens, J.W. (1994) Exposure of fish to biologically treated bleached-kraft effluent. 1. Biochemical, physiological and pathological assessment of rocky mountain whitefish (Prosopium williamsoni) and longnose sucker (Catostomus catostomus). Environ. Toxicol. Chem. 13, 1469–82.
Klotz, A.V., Stegeman, J.J. and Walsh, C. (1984) An alternative 7- ethoxyresorufin O-deethylase activity assay: a continuous visible spectrophotometric method for measurement of cytochrome P- 450 monooxygenase activity. Anal. Biochem. 140, 138–45.
Knutson, S., Solomon, K., Hodson, P. and Van Der Kraak, G. (1995) Effects of sitosterol on fish reproduction. In SETAC 16th Annual Meeting.
Kovats, Z.E. and Ciborowski, J.J.H. (1989) Aquatic insect adults as indicators of organochlorine contamination. J. Great Lakes Res. 15, 623–34.
Lorenzen, A., Kennedy, S.W., Bastien, L.J. and Hahn, M.E. (1997a) Effects of pulp mill effluents on tree swallows 249 Halogenated aromatic hydrocarbon-mediated porphyrin accumulation and induction of cytochrome P4501A in nestling embryo hepatocytes. Biochem. Pharmacol. 53, 373–84.
Lorenzen, A., Shutt, J.L. and Kennedy, S.W. (1997b) Sensitivty of common tern (Sterna hirundo) embryo hepatocyte cultures to CYP1A induction and porphyrin accumulation by halogenated aromatic hydrocarbons and common tern egg extracts. Arch. Environ. Contam. Toxicol. 32, 126–34.
Lowell, R.B., Culp, J.M., Wrona, F.J. and Bothwell, M.L. (1996) Effects of pulp mill effluent on benthic freshwater invertebrates: food availability and stimulation of increased growth and development. In M.R. Servos, K.R. Munkittrick, J.H. Carey and G.J. Van Der Kraak (eds) Environmental fate and effects of pulp and paper mill effluents, pp. 525–32. Delray Beach, FL: St Lucie Press.
Luoma, M.E., Shelast, B.M., Brayford, K.T., Steinback, B.J., Moore, D.J. and Smith, G.S. (1997) Benthic invertebrate community survey for environmental effects monitoring on the Athabasca River for Alberta Newsprint Company, Whitecourt, Alberta. In J.S. Goudey, S.M. Swanson, M.D. Treissman and A.J. Niimi (eds) Proceedings of the 23rd Annual Aquatic Toxicity Workshop p. 138. Calgary: Can. Tech. Rept. Fish. Aquat. Sci.
Martel, P.H., Kovacs, T.G. and Voss, R.H. (1996) Effluents from Canadian pulp and paper mills: a recent investigation of their potential to induce mixed function oxygenase activity in fish. In M.R. Servos, K.R. Munkittrick, J.H. Carey and G.J. Van Der Kraak (eds) Environmental fate and effects of pulp and paper mill effluents, pp. 410–12. Delray Beach, FL: St Lucie Press.
McCarty, J.P. (1997) Aquatic community characteristics influence the foraging patterns of tree swallows. Condor 99, 210–13.
McMaster, M.E., Van Der Kraak, G.J., Portt, C.B., Munkittrick, K.R., Sibley, P.K., Smith, I.R. and Dixon, D.G. (1991) Changes in hepatic mixed-function oxygenase (MFO) activity, plasma steroid levels and age at maturity of a white sucker (Catostomus commersoni) population exposed to bleached kraft mill effluent. Aquatic Toxicol. 21, 199–218.
McMaster, M.E., Van Der Kraak, G.J. and Munkittrick, K.R. (1996) An epidemiological evaluation of the biochemical basis for steroid hormonal depressions in fish exposed to industrial wastes. J. Great Lakes Res. 22, 153–71.
Miranda, C.L., Henderson, M.C., Wang, J.-L., Nakaue, H.S. and Buhler, D.R. (1987) Effects of polychlorinated biphenyls on porphyrin synthesis and cytochrome P-450-dependent monooxygenases in small intestine and liver of Japanese quail. J. Toxicol. Environ. Health 20, 27–35.
Muir, D.C.G. and Servos, M.R. (1996) Bioaccumulation of bleached kraft organic chemicals by fish. In M.R. Servos, K.R. Munkittrick, J.H. Carey and G.J. Van Der Kraak (eds) Environmental fate and effects of pulp and paper mill effluents, pp. 283–96. Delray Beach, FL: St Lucie Press.
Munkittrick, K.R., Portt, C.B., Van Der Kraak, G.J., Smith, I.R. and Rokosh, D.A. (1991) Impact of bleached kraft mill effluent on population characteristics, liver MFO activity, and serum steroid levels of a Lake Superior white sucker (Catostomus commersoni) population. Can. J. Fish. Aquatic Sci. 48, 1371–80.
Munkittrick, K.R., McMaster, M.E., Portt, C.B., Van Der Kraak, G.J., Smith, I.R. and Dixon, D.G. (1992a) Changes in maturity, plasma sex steroid levels, hepatic mixed-function oxygenase activity, and the presence of external lesions in lake whitefish (Coregonus clupeaformis) exposed to bleached kraft mill effluent. Can. J. Fish. Aquatic Sci. 49, 1560–9.
Munkittrick, K.R., Van Der Kraak, G.J., McMaster, M.E. and Portt, C.B. (1992b) Response of hepatic MFO activity and plasma sex steroids to secondary treatment of bleached kraft mill effluent and mill shutdown. Environ. Toxicol. Chem. 11, 1427–39.
Munkittrick, K.R., Van Der Kraak, G.J., McMaster, M.E., Portt, C.B., Van den Heuval, M.R. and Servos, M.R. (1994) Survey of receiving-water environmental impacts associated with discharges from pulp mills. 2. Gonad size, liver size, hepatic erod activity and plasma sex steroid levels in white sucker. Environ. Toxicol. Chem. 13, 1089–101.
Owens, J.W. (1991) The hazard assessment of pulp and paper mill effluents in the aquatic environment. Environ. Toxicol. Chem. 10, 1511–40.
Peterson, G.L. (1977) A simplification of the protein assay method of Lowry et al. Anal. Biochem. 83, 346–56.
Podemski, C. and Culp, J.M. (1996) Nutrient and contaminant effects of bleached kraft mill effluent on benthic algae and insects of the Athabasca River. In M.R. Servos, K.R. Munkittrick, J.H. Carey and G.J. Van Der Kraak (eds) Environmental fate and effects of pulp and paper mill effluents, pp. 571–80. Delray Beach, FL: St Lucie, Press.
Pohl, R.J. and Fouts, J.R. (1980) A rapid method for assaying the metabolism of 7-ethoxyresorufin by microsomal subcellular fractions. Anal. Biochem. 107, 150–5.
Pyykko, K. (1983) Characterization and stability of rat liver microsomes isolation by a rapid gel filtration method. Acta Pharmacol. Toxicol. 52, 39–46.
Quinney, T.E. and Ankney, C.D. (1985) Prey size selection by tree swallows. Auk 102, 245–50.
Quinney, T.E., Hussell, D.J.T. and Ankney, C.D. (1986) Sources of variation in growth of tree swallows. Auk 103, 389–400.
Robertson, R.J., Stutchbury, B.J. and Cohen, R.R. (1992) Tree swallow. In A. Poole, P. Stettenheim and F. Gill (eds) The birds of North America, No. 11 pp 1–27. Philadelphia: The Academy of Natural Sciences and the American Ornithologists' Union.
St Louis, V.L., Breebaart, L. and Barlow, J.C. (1990) Foraging behaviour of tree swallows over acidified and non-acidified lakes. Can. J. Zool. 68, 2385–92.
St Louis, V.L., Breebaart, L., Barlow, J.C. and Klaverkamp, J.F. (1993) Metal accumulation and mettalothionein concentrations in tree swallow nestlings near acidified lakes. Environ. Toxicol. Chem. 12, 1203–7.
SAS Institute (1988) SAS Procedures Guide Release 6.03. Cary, NC: SAS Institute.
Schryer, R.P., Leis, A.L., Swanson, S.M., Holley, K., Marchant, T.A., Graham, D. and Firth, B.K. (1995) Sex steroids in wild fish exposed to BKME: challenges in data collection and interpretation. In SETAC 16th Annual Meeting.
Servos, M.R. (1996) Origins of effluent chemicals and toxicity: recent research and future directions. In M.R. Servos, K.R. Munkittrick, J.H. Carey and G.J. Van Der Kraak (eds) Environmental fate and effects of pulp and paper mill effluents, pp. 159–68. Delray Beach, FL: St Lucie Press.
Servos, M.R., Huestis, S.Y., Whittle, D.M., Van Der Kraak, G.J. and Munkittrick, K.R. (1994) Survey of receiving water environmental impacts associated with discharges from pulp mills. 3. Polychlorinated dioxins and furans in muscle and liver of white sucker (Catostomus commersoni). Environ. Toxicol. Chem. 13, 1103–15.
Smits, J.E.G., Wobeser, B.A. and Schiefer, H.B. (1995) Physiological, reproductive and pathological effects of dietary bleached pulp mill effluent on mink (Mustela vison). Environ. Toxicol. Chem. 14, 2095–105.
Smits, J.E.G., Blakley, B.R. and Wobeser, G.A. (1996) Immunotoxicity studies in mink (Mustela vison) chronically exposed to dietary bleached kraft pulp mill effluent. J. Wildl. Dis. 32, 199–208.
Sokal, R.R. and Rohlf, F.J. (1981) Biometry, 2nd edn. San Francisco: W.H. Freeman.
Stromberg, L., Morck, R., de Sousa, F. and Dahlman, O. (1996) Effects of internal process changes and external treatment on effluent chemistry. In M.R. Servos, K.R. Munkittrick, J.H. Carey and G.J. Van Der Kraak (eds) Environmental fate and effects of pulp and paper mill effluents, pp. 3–20. Delray Beach, FL: St Lucie Press.
Stutchbury, B.J. and Robertson, R.J. (1988) Within-season and agerelated patterns of reproductive performance in female tree swallows (Tachycineta bicolor). Can. J. Zool. 66, 827–34.
Swanson, G.A., Krapu, G.L., Bartonek, J.C., Serie, J.R. and Johnson, D.H. (1974) Advantages of mathematically weighting waterfowl food habits data. J. Wildl. Manage. 38, 302–7.
Swanson, S.M., Schryer, R., Shelast, R., Holley, K., Berbekar, I., Kloepper-Sams, P.J., Owens, J.W., Steeves, L., Birkholz, D. and Marchant, T. (1993) Wapiti / Smoky River Ecosystem Study. Calgary: Sentar Consultants.
Swanson, S.M., Schryer, R., Shelast, R., Kloepper-Sams, P.J. and Owens, J.W. (1994) Exposure of fish to biologically treated bleached-kraft mill effluent. 3. Fish habitat and population assessment. Environ. Toxicol. Chem. 13, 1497–507.
Swanson, S.M., Holley, K., Bourree, G.R., Pryke, D.C. and Owens, J.W. (1996a) Concentrations of chlorinated organic compounds in various receiving environment compartments following implementation of technological changes at a pulp mill. In M.R. Servos, K.R. Munkittrick, J.H. Carey and G.J. Van Der Kraak (eds) Environmental fate and effects of pulp and paper mill effluents, pp. 253–60. Delray Beach, FL: St Lucie Press.
Swanson, S.M., Schryer, R. and Firth, B. (1996b) Whole organism and population response of sentinel fish species in a large river receiving pulp mill effluents. In M.R. Servos, K.R. Munkittrick, J.H. Carey and G.J. Van Der Kraak (eds) Environmental fate and effects of pulp and paper mill effluents, pp. 555–70. Delray Beach, FL: St Lucie Press.
Thomas, G.P. and Munteanu, N. (1997) Benthic community populations near two adjacent northern pulpmill discharges. Water. Sci. Technol. 35, 381–8.
Van Der Kraak, G.J., Dye, H.M. and Donaldson, E.M. (1984) Effects of LH-RH and desgly10 [D-ala6]LH-RH-ethylamide on plasma sex steroid profiles in adult female coho salmon (Oncorrhynchus kisutch). Gen. Comp. Endocrinol. 55, 36–45.
Van Der Kraak, G.J., Munkittrick, K.R., McMaster, M.E., Portt, C.B. and Chang, J.P. (1992) Exposure to bleached kraft mill effluent disrupts the pituitary-gonadal axis of white sucker at multiple sites. Toxicol. Appl. Pharmacol. 115, 224–33.
Vannote, R.L., Minshall, G.W., Cummins, K.W., Sedell, J.R. and Cushing, C.E. (1980) The river continuum concept. Can. J. Fish. Aquatic Sci. 37, 130–7.
Wingfield, J.C. and Farner, D.S. (1980) Control of seasonal reproduction in temperate-zone birds. Prog. Reproduct. Biol. 5, 62–101.
Wingfield, J.C. and Farner, D.S. (1993) Endocrinology of reproduction in wild species. In D.S. Farner, J.R. King and K.C. Parkes (eds) Avian biology, Vol. IX, pp. 164–342. London: Academic Press.
Wrubleski, D.A. (1987) Chironomidae (Diptera) of peatlands and marshes in Canada. In D.M. Rosenberg and H.V. Danks (eds) Aquatic insects of peatlands and marshes in Canada, pp. 141–61. Mem. Ent. Soc. Can.
Xu, H., Lesage, S. and Munkittrick, K.R. (1994) Suitability of carboxylated porphyrin profiles as a biochemical indicator in whitefish (Coregonus clupeaformis) exposed to bleached kraft pulp mill effluent. Environ. Toxicol. Water Qual. 9, 223–30.
Yorks, A., Melancon, M. and Eisemann, J. (1996) Tree swallow (Tachycineta bicolor) as a sentinel species for PCB exposure and effects. In SETAC 17th Annual Meeting.
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Wayland, M., Trudeau, S., Marchant, T. et al. The Effect of Pulp and Paper Mill Effluent on an Insectivorous Bird, the Tree Swallow. Ecotoxicology 7, 237–251 (1998). https://doi.org/10.1023/A:1008942929560
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DOI: https://doi.org/10.1023/A:1008942929560