Abstract
David Peakall and co-workers pioneered innovative approaches that utilized extra-embryonic membranes to assess accumulation of organochlorine pesticides in eggs. This technique provided the foundation for an entire line of research to improve non-lethal methods for assessing contaminant exposure in oviparous wildlife. Currently, analysis of chorioallantoic membranes (CAMs) provides predictable estimates of chlorinated contaminant presence in eggs and in maternal tissues. Field studies have been conducted with herons, stilts, alligators, crocodiles, and sea turtles. Controlled dose-response studies have been completed in chickens. The following manuscript presents the foundations for the CAM approach and a review of research findings involving this technique.
Similar content being viewed by others
References
Albro, P.W. and Parker, C.E. (1979). Comparison of the compositions of Aroclor 1242 and Aroclor 1016. J. Chromatogr. 169, 161-6.
Albro, P.W., Corbett, J.T. and Schroeder, J.L. (1981). Quantitative characterization of polychlorinated biphenyl mixtures (Aroclors® 1248, 1254 and 1260) by gas chromatography using capillary columns. J. Chromatogr. 205, 103-11.
Bargar, T.A., Scott, G.I. and Cobb, G.P. (2001a). Uptake and distribution of three PCB congeners and endosulfan by developing white leghorn chicken embryos (Gallus domesticus). Arch. Environ. Contam. Toxicol. 41, 508-14.
Bargar, T.A., Scott, G.I. and Cobb, G.P. (2001b). Maternal transfer of contaminants: a case study of the excretion of three PCB congeners and technical grade endosulfan into eggs by white leghorn chickens (Gallus domesticus). Environ. Toxicol. Chem. 20(1), 61-7.
Bellairs, A.A. (1987). The crocodilia. In G. Webb, S. Manolis and P. Whitehead (eds) Wildlife Management: Crocodiles and Alligators, pp. 5-8. Chipping Norton Australia: Surrey Beatty and Sons.
Bergeron, J.M., Crews, D. and McLachlan, J.A. (1994). PCBs as environmental estrogens: turtle sex determination as a biomarker of environmental contamination. Environ. Health Perspect. 102(9), 780-1.
Bidleman, T.F. and Svastits, A.C. (1983). Baseline studies of petroleum hydrocarbons in Winyah Bay. Final Report to NOAA. Coastal Energy Impact Program Grant No. CEIP82-08/20361, January, 1983, pp. 7-8.
Bishop, C.A., Brown, G.P., Brooks, R.J., Lean, D.R.S. and Carey, J.H. (1994). Organochlorine contaminant concentrations in eggs and their relationship to body size, and clutch charachteristics of the female common snapping turtle (Chelydra serpentina serpentina) in Lake Ontario, Canada. Arch. Environ. Contam. Toxicol. 27, 82-7.
Bishop, C.A., Brooks, R.J., Carey, J.H., Ming, P., Norstrom, R.J. and Lean, D.R.S. (1991). The case for a cause-effect linkage between environmental contamination and development in eggs of the common snapping turtle (Chelydra S. Serpentina) from ontario, canada. J. Toxicol. Environ. Health 33, 521-47.
Bjorndal, K.A. and Wetherall, J.A. (1999). Twenty-six years of green turtle nesting at Tortuguero, Costa Rica: an encouraging trend. Conserv. Biol. 13, 126-34.
Blus, L.J. (1982). Further interpretation of the relation of organochlorine residues in brown Pelican eggs to reproductive success. Environ. Pollut. 28, 15-33.
Bowerman, W.W., Best, D.A., Evans, E.D., Postupalsky, S., Marteli, M.S., Kozie, K.D., Welch, R.L., Scheel, R.H., Durling, K.F., Rogers, J.C., Kubiak, T.J., Tillet, D.E., Schwartz, T.R., Jones, P.D. and Giesy, J.P. (1990). PCB concentrations in plasma of nestling bald eagles from the Great Lakes Basin, North America. Organohalogen Cmpnds. 4, 203-6.
Calambokidis, J., Speich, S., Peard, J., Steiger, G.H., Cubbage, J.C., Frye, D.M. and Lowenstine, L.J. (1985). NOAA technical memorandum. 159pp. Rockville MD: National Oceanic and Atmospheric Administration.
Clark, D.R. and Krynitsky, A.J. (1980). Fish, wildlife, and estuaries: organochlorine residues in eggs of loggerhead and green sea turtles nesting at Merritt Island, Florida, July and August 1976. Pesti. Monitor. J. 14, 7-10.
Cobb, G.P., Houlis, P.D. and Bargar, T.A. (2001). Polychlorinated biphenyl occurrence in American alligators (Alligator mississippiensis) from Louisiana and South Carolina. Environ. Pollut. 118(1), 1-4.
Cobb, G.P., Wood, P.D. and Quinn, M.O. (1997). Polychlorinated biphenyls in eggs and chorioallantoic membranes american alligators (Alligator mississipiensis) from Coastal South Carolina. Environ. Toxicol. Chem. 16, 1456-62.
Cobb, G.P. and Wood, P.D. (1997). PCB concentrations in eggs and chorioallantoic membranes of Loggerhead sea turtles (Caretta caretta) from the Cape Romain National Wildlife Refuge. Chemosphere 34, 539-49.
Cobb, G.P., Norman, D.M. and Kendall, R.J. (1994). Organochlorine contaminant assessment in great blue herons using traditional and nonlethal monitoring techniques. Environ. Pollut. 83, 299-309.
Cobb, G.P., Norman, D.M. and Brewer, L.W. (1995). Organochlorine contaminants in chorio-allantoic membranes of great blue herons (Ardea herodias) from Naval Air Station Whidbey Island. Chemosphere 30, 151-64.
Cobb, G.P. and Hooper, M.J. (1993). Nonlethal wildlife monitoring to determine exposure to xenobiotics and resulting impacts. In R.J. Kendall and T. Lacher (eds) The Population Ecology and Wildlife Toxicology of Agricultural Pesticide Use: A Modelling Initiative for Avian Species. Chelsea MI: SETAC Special Publication, Lewis Publisher.
Daniels, R.C. and White, T.W. (1993). Sea-level rise: destruction of threatened and endangered species habitat in South Carolina. Environ. Manag. 17, 373-85.
DeBusk, B.E. (2001). Assessment of organochlorine pesticide residues in Scutes from Morelet's crocodiles (Crocodylus moreletii). MS Thesis, Texas Tech University, Lubbock, Texas.
Delany, M.F., Bell, J.U. and Sundlof, S.F. (1988). Concentrations of contaminants in muscle of the American alligator in Florida. J. Wildl. Dis. 24, 62-6.
Dickerson, R.L., Hooper, M.J., Cobb, G.P., Gard, N.W. and Kendall, R.J. (1994). Toxicological foundations of ecological risk assessment: biomarker development and interpretation based on laboratory and wildlife species. Environ. Health Perspect 102, 65-9. Boca Raton, FL: Lewis Publishers, 457p.
Dunnivant, F.M. (1985). Determination of polychlorinated biphenyl concentrations in selected sediments using a sonication extraction technique. Master's Thesis, Clemson University, Clemson South Carolina, 168pp.
Elliott, J.E., Norstrom, R.J. and Keith, J.A. (1988). Organochlorines and eggshell thinning in Northern Gannets (Sula bassanus) from Eastern Canada, 1968–1984. Environ. Pollut. 52, 81-102.
Elliott, J.E., Whitehead, P.E., Norstrom, R.J., Bandiera, S.M., Hart, L.E., Cheng, K.M. and Bellward, G.D. (1993). Monitoring chlorinated hydrocarbon exposure in great blue herons by using mixed-function oxidases. Marine Environ. Res. 35, 204-5.
Elliott, J.E., Harris, M.L., Wilson, L.K., Whitehead, P.E. and Norstrom, R.J. (2001). Monitoring temporal and spatial trends in polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs) in eggs of great blue heron (Ardea herodias) on the Coast of British Columbia, Canada, 1983–98. AMBIO 30, 416-28.
Fossi, M.C. and Leonzio, C. (1994). Nondestructive Biomarkers in Vertebrates, 345pp. Boca Raton, FL: Lewis Publishers.
Freeman, B.M. and Vince, M.A. (1974). Development of Avian Embryo. New York: John Wiley & Sons.
Friend, M., Haegle, M.A., Meeker, D.L., Hudson, R. and Baer, C.H. (1979). Correlations between residues of dichlorodiphenylethane, polychlorinated biphenyl and dieldrin in the serum and tissues of Mallard ducks (Anas platyrhynchos). In Animals as Monitors of Environmental Pollution, pp. 319-26. Washington DC: National Academy of Sciences.
Groombridge, B. (1987). The distribution and status of World crocodilians. In G.J. Webb, S.C. Manolis, P.J. Whitehead (eds); Wildlife Management: Crocodiles and Alligators, pp. 9-21. Sydney Australia: Surrey Beatty and Sons Pty.
Guillette, L.J., Gross, T.S. and Mason, G.R. (1994). Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ. Health Perspect. 102, 680-8.
Hall, R.J., Kaiser, T.E., Robertson, W.B. and Patty, P.C. (1979). Organochlorine residues in eggs of the endangered American crocodile (Crocodylus actus). Bull Environ. Contam. Toxicol. 23, 87-90.
Hamilton, H.L. (1952). Lillie's Development of the Chick. 624pp. New York: Holt and Company.
Harper, F.D., Waldrop, V.C., Jeffers, R.D., Duncan, C.D. and Cobb, G.P. (1999). Organochlorine and polychlorinated biphenyl contamination in black neck stilt, Himantopus mexicanus, eggs from the savannah and Tybee National Wildlife refuges. Chemosphere 39, 151-63.
Heinz, G.H., Percival, H.F. and Jennings, M.L. (1991). Contaminants in American alligator eggs from lake Apopka, Lake Griffin and Lake Okeechobee, Florida. Environ. Monit. Assess. 16, 277-85.
Henny, C.J. and Meeker, D.L. (1981). An evaluation of blood plasma for monitoring DDE in birds of prey. Environ. Poll. 25, 291-304.
Hebert, C.E. and Keenleyside, K.A. (1995). To normalize or not to normalize? Fat is the question. Environ. Toxicol. Chem. 14, 801-7.
Hooper, M.J., Dietrich, P.J., Weisskopf, C.P. and Wilson, B.W. (1989). Organophosphorous insecticide exposure in hawks inhabiting orchards during winter dormant spraying. Bull. Environ. Contam. Toxicol. 47, 717-24.
Hutchinson, J. and Simmonds, M. (1992). Escalation of threats to marine turtles. Oryx 26, 95-102.
Huggett, R.J., Kimerle, R.P., Mehrle, P.M. and Bergman, H.L. (1992). Biomarkers: Biochemical, Physiological, and Histological Markers of Anthropologenic Stress. 347pp. Boca Raton, FL: Lewis Press.
Jenkins, R.W.G. (1987). The world conservation strategy and CITES: Principle for the management of crocodilians. In G. Webb, S. Manolis and P. Whitehead (eds) Wildlife Management: Crocodiles and Alligators, pp. 27-31. Chipping Norton Australia: Surrey Beatty and Sons.
Klasing, K.C. (1998). Comparative Avian Nutrition. pp. 191-2 Wallingford Oxon, United Kingdom: CAB International.
Kubiak, T.J., Harris, H.J., Smith, L.M., Schwartz, T.R., Stalling, D.L., Trick, J.A., Sileo, L., Docherty, D. and Erdman, T.C. (1989). Microcontaminants and reproductive impairment of the Forster's Tern on Green Bay, Lake Michigan-1983. Arch. Environ. Contam. Toxicol. 18, 706-27.
McCarthy, J.F. and Shugart, L.R. (1990). Biomarkers of Environmental Contamination.457pp.,BocaRaton,FL: LewisPublishers.
McKim, J.M. Jr. and Johnston, K.L. (1983). Polychlorinated biphenyls and p,p-DDE in loggerhead and green postyearling Atlantic Sea turtles. Bull. Environ. Contam. Toxicol. 31, 53-60.
Moul, I.E. (1990). Master's Thesis. 59pp. University of British Columbia.
Mullin, M.D. and Pochini, C.M. (1984). High resolution PCB analysis: synthesis and chromatographic properties of all 209 congeners. Environ. Sci. Technol. 18, 468-76.
Norman, D.M. (1992). Organochlorine pesticides and polychlorinated biphenyl congeners in great blue herons from the Puget Sound ecosystem. Master's Thesis. 248pp. Western Washington University, Bellingham WA
Pastor, D., Ruiz, X., Joyner, L. and Albagiges, J. (1996). The use of chorioallantoic membranes as predictors of egg organochlorine burden. Environ. Toxicol. Chem. 15, 167-71.
Peakall, D.B. (1974). DDE: Its presence in Peregrine eggs in 1948. Science 183, 673-673.
Peakall, D.B., Lew, T.S., Springer, A.M., Walker, W.W., Risebrough, R.W., Monk, J.G., Jarman, W.M., Walton, B.J., Reynolds, L.M., Fyfe, R.W. and Kiff, L.F. (1983). Determination of the DDE and PCB contents of Peregrine Falcon eggs: A comparison of whole egg measurements and estimates derived from eggshell membranes. Arch. Environ. Contam. Toxicol. 12, 523-8.
Peakall, D.B. and Fox, G.A. (1987). Toxicological investigations of pollutant-related effects in Great Lakes gulls. Environ. Health Perspect. 71, 187-93.
Peakall, D.B. (1996). Disrupted patterns of behavior in natural populations as an index of ecotoxicity. Environ. Health Persp. 104(Suppl. 2), 331-51.
Peakall, D. (1992). Animal Biomarkers as Pollution Indicators. Ecotoxicol. Ser., Vol. 1. New York: Chapman and Hall.
Peakall, D.B., Jeffrey, D.A. and Boersma, D. (1987). Mixed-function oxidase activity in seabirds and its relationship to oil pollution. Comp. Biochem. Physiol. C. 88C, 151-4.
Pepper, C.B. (2001). Organochlorine pesticides in the chorioallantoic membrane of Morelet's crocodile eggs. MS Thesis. Texas Tech University: Lubbock TX.
Rainwater, T.R., Adair, B.M., Platt, S.G., Anderson, T.A., Cobb, G.P. and McMurry, S.T. (2002). Mercury in Morelet's crocodile eggs from northern Belize.Arch.Environ.Contam.Toxicol. 42,319-24.
Romanoff, A.L. (1960). The Avian Embryo. New York: The MacMillan Company.
Safe, S. (1994). Polychlorinated biphenyls (PCBs): Environmental impact, biochemical and toxic responses, and implications for risk assessment. Crit. Rev. Toxicol. 24, 87-149.
Sanderson, J.T., Elliott, J.E., Norstrom, R.J., Whitehead, P.E., Hart, L.E., Cheng, K.M. and Bellward, G.D. (1994). Monitoring biological effects of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls in great blue heron chicks (Ardea herodias) in British Columbia. J. Toxicol. Environ. Health 41, 435-50.
SCDHEC (1992). Sampit River Advisory Update. 8pp. South Carolina Department of Health and Environmental Control, Columbia, SC, USA.
Skerfving, S., Svensson, B.-G., Asplund, L. and Hagmar, L. (1994). Exposure to mixtures and congeners of polychlorinated biphenyls. Clin. Chem. 40, 1409-5.
Sparling, D.W., Linder, G.L. and Bishop, C.A. (2000). The Ecotoxicology of Amphibians and Reptiles. 877pp. Pensacola, FL: SETAC Press.
Spiech, S.M., Calambokidas, J., Shea, D.W., Peard, J., Witter, M. and Fry, D.M. (1992). Eggshell thinning and organochlorine contaminants in western washington Waterbirds. Colonial Waterbirds 15, 103-12.
Spotila, J.R. and Reina, R.D. (2000). Pacific leatherback turtles face extinction. Nature 405, 529-30.
Stewart, M.E. and Terepka, A.R. (1969). Transport functions of the chick chorio-allantoic membrane. I. Normal histology and evidence for active electrolyte transport from the allantoic fluid, in vivo. Exp. Cell Res. 8(1), 93-106.
Stone, W.B., Kiviat, E. and Butkas, S.A. (1980). Toxicants in snapping turtles. N.Y. Fish Game J. 27, 39-50.
Tillitt, D.E., Ankley, G.T., Giesy, J.P., Ludwig, J.P., Kurita-Matsuba, H., Weseloh, D.V., Ross, P.R., Bishop, C.A., Sileo, L., Stromborg, K.L., Larson, J. and Kubiak, T.J. (1992). Polychlorinated biphenyl residues and egg mortality in double-crested cormorants from the great Lakes. Environ. Toxicol. Chem. 11, 1281-8.
Wu, T.H., Rainwater, T.R., Platt, S.G., McMurry, S.T. and Anderson, T.A. (2000a). Organochlorine contaminants in Morelet's crocodile (Crocodylus moreletii) eggs from Belize. Chemoshpere 40, 671-8.
Wu, T.H., Rainwater, T.R., Platt, S.G., McMurry, S.T. and Anderson, T.A. (2000b). DDE in eggs of two crocodilian species from Belize. J. Agric. Food Chem. 48, 6416-20.
Yamashita, N., Tanabe, S., Ludwig, J.P., Kurita, H., Ludwig, M.E. and Tatsukawa, R. (1993). Embryonic abnormalities and organochlorine contamination in double-crested Cormorants (Phalacrocorax caspia) and Caspian Terns (Hydroprogne caspia) from the Upper Great Lakes. Environ. Pollut. 79, 163-73.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cobb, G.P., Bargar, T.A., Pepper, C.B. et al. Using Chorioallantoic Membranes for Non-lethal Assessment of Persistent Organic Pollutant Exposure and Effect in Oviparous Wildlife. Ecotoxicology 12, 31–45 (2003). https://doi.org/10.1023/A:1022532711353
Issue Date:
DOI: https://doi.org/10.1023/A:1022532711353