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Response to Comment on “Ammunition is the Principal Source of Lead Accumulated by California Condors Re-Introduced to the Wild” Don Saba of Sierra Bioresearch raises two issues in criticism of our paper (1, 2), first that the isotopic signature of background environmental lead in California is more variable than the values we reported from the published literature, and second that the isotopic signature of lead in ammunition is more variable than the values we measured and reported in our study. He concludes that these issues undermine the conclusions we reached in our study that incidental ingestion of lead ammunition by California Condors is the principle source of elevated lead exposures in condors re-introduced to central California. Saba makes erroneous assumptions in his arguments that, in our professional opinion, invalidate his criticisms. We strongly disagree with his conclusions, and believe that the results and conclusions of our study stand as published. Saba argues that the stable isotope signature of background environmental lead is more variable than the values we reported from the published literature. First, and perhaps most important, this criticism is irrelevant to the major conclusions reached in our study, which do not rely on the background lead values cited in our paper. Those conclusions, which are supported by the two-endmember mixing model we present, rely on the fact that the blood lead concentrations and stable isotopic composition of condors prior to release into the wild are significantly different than the blood lead values of released free-flying condors; this is clearly demonstrated by our data. Further, the fact that the prerelease condor blood lead concentrations and isotopic signatures are so similar to each other directly contradicts Saba’s assertion that they are exposed to background dietary lead spanning a very large isotopic range. The fact that the blood lead isotopic signatures also closely resemble the isotopic signatures in representative diet items containing background lead concentrations that we measured, and that the lead isotopic signature in those representative diet items resembles the isotopic signatures of some environmental lead values published in the literature is also consistent with our conclusions. At the basis of Saba’s misguided argument is the failure to distinguish between the whole universe of lead isotope values that one may find in California materials, ranging from rocks, sediments, soils, flora, fauna, etc., and the range of isotopic values of lead bioavailable to Condors through their diet. He erroneously assumes that condor dietary items will “contain background lead that will have the isotopic composition of the environment, which has been shown to have 207Pb:206Pb ratios ranging from 0.7541 to 0.8453”. This assumption seems to consider that all of the environmental lead samples published in those studies, including unfiltered stream runoff, soil, and hydraulic mine tailing samples that likely contain significant fractions of lead derived from local or regional soil and rock formations, are reflective of biologically available environmental lead that may enter the condor’s food web. However, numerous studies, most notably by Patterson, Flegal, and colleagues (3–13) have demonstrated that biologically available “background” environmental lead has been dominated over past decades by atmospheric lead deposition from the cumulative combustion of leaded gasoline, and that this environmental lead is not readily transported or biologically accumulated up the food web. In the study of Erel et al. (14), we believe that background 10.1021/es702174r CCC: $40.75
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environmental lead was best represented by the cited isotopic values of dry atmospheric deposition (Table 5c) and snowfed lake water (Table 5d), while in Dunlap et al. (15) this was best reflected in the cited values from filtered Sacramento and San Joaquin River water (Table 1). Notably, Saba neglected to note that the environmental lead values we cited from these two studies also agree quite well with our own prior studies in which we have estimated the lead isotopic composition of biologically assimilated background environmental lead in central California (11, 16). Saba provides a long list of food items that have been recorded in condor diets in the past before the few birds remaining in the wild were taken into captivity. This list is now hardly relevant. Food with very low concentrations of lead, principally in the form of stillborn dairy calves, is available to the condors at all times; carbon isotope analyses have shown that the carcasses of corn-fed animals such as dairy cattle (or their stillborn progeny) constitutes about 50% of the current diet (17). Moreover, during their first year in the wild released condors feed principally on this food source and accumulate very little lead (18). The second issue that Saba raises in criticism of our study (2) is that the lead isotopic compositions of the ammunition that we measured do not reflect the possible range in isotopic compositions of ammunition available to hunters across the United States, using data of a study we cite (19) to support this suggestion. He then goes on to state that “. . . It is therefore virtually certain that ammunition having a wide isotopic range is used to take game in areas where condors forage. Therefore, the authors’ assumption, that only ammunition of a very narrow isotopic range is available in central California, is strongly contradicted by the evidence”. While Saba is technically correct that the isotopic composition of lead ammunition across the United States can be more variable than the values we measured, he provides no data on ammunition sold in central California to support his assertion. Moreover, Saba makes a significant error in assuming that the possible variability in 207Pb/206Pb ratios of ammunition in the United States precludes the use of lead isotope methods to evaluate lead ammunition as a source of exposure. We collected ammunition from retail stores and private hunters in the central California region, following the plausible assumption that these stores represent a reasonable source of ammunition to hunters in central California condor habitat, and hence represent a plausible source of spent ammunition to the condors in central California. We did not attempt to estimate the 207Pb/206Pb ratios of ammunition in central California from published sources, as did Saba, because we believed that those samples of shot pellets reported by Scheuhammer and Templeton (19, obtained prior to 1998 in Canada but including shot produced by the major U.S. manufacturers) were not reasonably linked via a plausible exposure pathway to condors in central California. The very fact that the 207Pb/ 206Pb ratios of the brands and calibers of ammunition that we sampled across several different counties and retail outlets clustered as they did fully supports our assumptions and our conclusions. Numerous studies over the past 25 years have established the utility of stable lead isotopic techniques for determining the biogeochemical cycling of lead, including exposure pathways to humans and wildlife (3, 5, 9–11, 13, 16, 19–28). These studies fully support the scientific approach and application of stable lead isotope tracer methods used in our condor study (2), which relied upon (i) knowledge of the VOL. 42, NO. 5, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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plausible sources of lead exposure to the condors, including lead concentrations and lead loadings in those sources; (ii) the measured isotopic ratios of those plausible lead sources within the condor’s environment; and (iii) information about behavioral feeding habits of condors, including consideration of plausible exposure pathways. Saba states that “there is ample evidence that condors consume a variety of diet items that have far higher levels of lead than the narrow diet reported by the authors. For example, a study of lead in carcasses within condor range (7, 29) reported lead levels ranging from 1 to 17.5 ppm in the muscle tissue of 3 out of 19 deer carcasses examined”. If these deer were killed by hunters, which we consider likely, this is precisely our point. Most of the ammunition we sampled consisted of high-speed copper-jacketed lead bullets commonly used to hunt deer. The lead in these bullets often fragments into many small particles upon impact (30). We believe that these small fragments in deer and other animals killed by ammunition are in fact the principal source of the lead accumulated by condors in central California that matches so closely the local ammunition sold to local hunters. Finally, Saba refers to blood lead levels up to 37 µg/dL in captive condors in the 1980s. Before the creation of a captive flock, only one condor was in captivity and was the bird with this elevated blood lead level. This bird, Topa-topa (Studbook #1), is still alive and continues to sire offspring. His diet, however, is now much more carefully controlled. In our paper we report data on lead concentrations in the blood of eight prerelease condors, with an average of 2.8 µg/dL. Unpublished data from the condor program on lead in the blood of other young condors from the zoos are comparable. In summary, we believe that Saba’s criticisms of our work are without scientific merit. We stand by our conclusions that incidental ingestion of lead ammunition by California Condors is the principle source of elevated lead exposures in condors reintroduced to central California.
Literature Cited (1) Saba, D. Comment on “Ammunition is the principal source of lead accumulated by California Condors re-introduced to the wild”. Environ. Sci. Technol. 2008, 42, 1807–1808. (2) Church, M.; Gwiazda, R.; Risebrough, R. W.; Sorenson, K.; Chamberlain, C. P.; Heinrich, W.; Rideout, B.; Smith, D. R. Ammunition is the principal source of lead accumulated by California Condors re-introduced to the wild. Environ. Sci. Technol. 2006, 40, 6143. (3) Chow, T. J.; Johnstone, M. S. Lead Isotopes in Gasoline and aerosols of Los Angeles Basin, California. Science 1965, 147, 502. (4) Ericson, J. E.; Shirahata, H.; Patterson, C. C. Skeletal concentrations of lead in ancient Peruvians. N. Engl. J. Med. 1979, 300, 946. (5) Flegal, A. R.; Nriagu, J. O.; Niemeyer, S.; Coale, K. H. Isotopic tracers of lead contamination in the Great Lakes. Nature (London) 1989, 339, 455. (6) Manea-Krichten, M.; Patterson, C. C.; Miller, G. E.; Settle, D. M.; Erel, Y. Comparative increases of lead and barium with age in human tooth enamel, rib and ulna. Sci. Total Environ. 1991, 107, 179. (7) National Research Council. Measuring Lead Exposure in Infants, Children, and Other Sensitive Populations; National Academy Press: Washington, DC, 1993. (8) Settle, D. M.; Patterson, C. C. Lead in albacore: guide to lead pollution in Americans. Science (Washington D.C.) 1980, 207 (4436), 167. (9) Shirahata, H.; Elias, R. W.; Patterson, C. C.; Koide, M. Chronological variations in concentrations and isotopic compositions of anthropogenic atmospheric lead in sediments of a remote subalpine pond. Geochim. Cosmochim. Acta 1980, 44, 149. (10) Smith, D. R.; Niemeyer, S.; Estes, J.; Flegal, A. R. Stable lead isotopes evidence anthropogenic contamination in Alaskan Sea Otters. Environ. Sci. Technol. 1990, 24, 517. 1810
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(11) Smith, D. R.; Osterloh, J. D.; Niemeyer, S.; Flegal, A. R. Lead sources to California sea otters: Industrial inputs circumvent natural lead biodepletion mechanisms. Environ. Res. 1992, 57, 190. (12) Stukas, V. J.; Wong, C. S. Stable Lead Isotopes as a Tracer in Coastal Waters. Science (Washington, D.C.) 1981, 211 (4489), 1424. (13) Sturges, W. T.; Barrie, L. A. Lead 206/207 isotope ratios in the atmosphere of North America as tracers of US and Canadian emissions. Nature (London) 1987, 329, 144. (14) Erel, Y.; Morgan, J. J.; Patterson, C. C. Natural levels of lead and cadmium in a remote mountain stream. Geochim. Cosmochim. Acta 1991, 55 (3), 707. (15) Dunlap, C. E.; Bouse, R.; Flegal, A. R. Past Leaded Gasoline Emissions as a Nonpoint Source Tracer in Riparian Systems: A Study of River Inputs to San Francisco Bay. Environ. Sci. Technol. 2000, 34 (7), 1211. (16) Smith, D. R.; Osterloh, J. D.; Flegal, A. R. The use of endogenous stable lead isotopes to determine the release of lead from the skeleton. Environ. Health Perspect. 1996, 104, 60. (17) Chamberlain, C. P.; Waldbauer, J. R.; Fox-Dobbs, K.; Newsome, S.; Koch, P.; Smith, D. R.; Church, M.; Chamberlain, S.; Sorenson, K.; Risebrough, R. Pleistocene to recent dietary shifts in California condors. PNAS 2005, 102, 16707. (18) Sorenson, K. J.; Burnett, L. J. Lead concentrations in the blood of Big Sur California Condors. In press, Special Publication of the American Ornithologists’ Union and Nuttall Ornithological Club; Mee, A.; Hall, L. S., Eds.; 2007. (19) Scheuhammer, A. M.; Templeton, D. M. Use of stable isotope ratios to distinguish sources of lead exposure in wild birds. Ecotoxicology 1998, 7, 37. (20) Finklestein, M.; Gwiazda, R.; Smith, D. Lead poisoning of seabirds: Environmental risks from leaded paint at a decommissioned military base. Environ. Sci. Technol. 2003, 37, 3256. (21) Gulson, B. L.; Davis, J. J.; Bawden-Smith, J. Paint as a source of recontamination of houses in urban environments and its role in maintaining elevated blood leads in children. Sci. Total Environ. 1995, 164, 221. (22) Gwiazda, R. H.; Smith, D. R. Lead Isotopes as a Supplementary Tool in the Routine Evaluation of Household Lead Hazards. Environ. Health Perspect. 2000, 108, 1091. (23) Gwiazda, R.; Campbell, C.; Smith, D. R. A non-invasive approach to estimate the bone lead contribution to blood in children: Implications for assessing the efficacy of lead abatement. Environ. Health Perspect. 2005, 113, 104. (24) Maddaloni, M.; Lolacono, N.; Manton, W.; Blum, C.; Drexler, J.; Graziano, J. Bioavailability of soilborne lead in adults, by stable isotope dilution. Environ. Health Perspect. 1998, 106 (6), 1589. (25) Outridge, P. M.; Evans, R. D.; Wagemann, R.; Stewart, R. E. A. Historical trends of heavy metals and stable lead isotopes in beluga (Delphinapterus leucas) and walrus (Odobenus rosmarus rosmarus) in the Canadian Arctic. Sci. Total Environ. 1997, 203, 209. (26) Outridge, P. M.; Stewart, R. E. A. Stock discrimination of Atlantic walrus (Odobenus rosmarus rosmarus) in the eastern Canadian Arctic using lead isotope and element signatures in teeth. Can. J. Fish. Aquat. Sci. 1999, 56, 105. (27) Scheuhammer, A. M.; Bond, D. E.; Burgess, N. M.; Rodrigue, J. Lead and stable lead isotope ratios in soil, earthworms, and bones of American woodcock (Scolopax minor) from eastern Canada. Environ. Toxicol. Chem. 2003, 22 (11), 2585. (28) Yaffe, Y.; Flessel, C. P.; Wesolowski, J. J.; del Rosario, A.; Guirguis, G. N.; Matias, V; Gramlich, J. W.; Kelly, W. R.; Degarmo, T. E.; Coleman, G. C. Identification of lead sources in California children using the stable isotope ratio technique. Arch. Environ. Health 1983, 38 (4), 237. (29) Wiemeyer, S. N.; Jurek, R. M.; Moore, J. F. Environmental contaminants in surrogates, food, and feathers of California condors (Gymnogyps californianus). Environ. Monit. Assess. 1986, 6, 91–111. (30) Hunt, W. G.; Burnham, W.; Parish, C. N.; Burnham, K. K.; Mutch, B.; Oaks, J. L. Bullet fragments in deer remains: implications for lead exposure in avian scavengers. Wildl. Soc. Bull. 2006, 34, 167.
Molly E. Church University of Pennsylvania, School of Veterinary Medicine, Rosenthal Building, 3800 Spruce Street, Philadelphia, Pennsylvania 19104
Roberto Gwiazda and Donald R. Smith Department of Environmental Toxicology University of California Santa Cruz, California 95064
Sean Farry Arizona Game and Fish Department P. O. Box 856 Alpine, Arizona 85920
Robert W. Risebrough Bodega Bay Institue 2711 Piedmont Avenue Berkeley, California 94705
Kelly Sorenson Ventana Wildlife Society 19045 Portola Drive, Suite F-1 Salinas, California 93924
C. Page Chamberlain Department of Geological and Environmental Science Stanford University Stanford, California 94305
William Heinrich The Peregrine Fund World Center for Birds of Prey 5668 W. Flying Hawk Lane Boise, Idaho 83709
Bruce A. Rideout Zoological Society of San Diego P. O. Box 120551 San Diego, California 92112 ES702174R
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