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Organochlorine Pollutants in Peregrines and Merlins Migrating through Wisconsin RoiH.KV \V. ktSIllROUGIl Department of Nutritional Sciences InMhuic of Mnnnc Resources University of C: lifornia Berkeley, Califo ma y*4720 ' Gkix.okv I.. 1 f 1KX NI l.nBoratoi \ *f O, rornrjf U'nivfi. iiliK i. New Vork Uanii.i. D. R :.rgi:r 1328 N. JeflTerso i Milwaukee. Wis<<>n\in 5J202 T he discovery that tire Peregrines (i'ako pcrcgrinus) breedii g in the eastern Arctic arc laying thin-shelled eggs and arc showing symptoms of reproductive f; ilurc (Berger cl al, this issue) suggests that this population is beginning to be alTcclcd by tli: same extinction process that Iras resulted in the extirpation of breeding Pere grines in man ' areas of North America and Kuropc (Hickey,1969; RatclilTc. 1970). The Peregrines of the eastern United States disap peared before the nature of the extinction pro cess was evident, but subsequent research showed that eggshell thinning had been asso ciated with the population decline (Mickey and Anderson, 1968). In Great Britain there was a considerable amount of evidence that exces sive mortality of adult birds had been a major reason for the rapid decline that began around 1955, coinciding with the introduction of highly toxic insecticides such as dieldrin into agricul tural use (Ratcliflc, 1963; Jefferies and Prcstl, 1966). The surviving birds, however, exper ienced reproductive failures that were charactcrized by shell thinning, egg breakage, and eat ing of the eggs by the adult birds (RatclilTc. 1967; Ratcliflc, 1970). Although embryonic mortality may be contributing to the decline in reproductive capacity of the Ungnva Pcrcgrjnes (Berger c( al, this issue) the pattern of egg breakage associated with shell thinning now observed in this population appears to be iden tical to the symptoms noted previously in south- cm Canada (Mall, this issue), the United States (Mic1 cy and Anderson, 1968) and Grett Britain (Ratcliflc, 1970). At the conference convened in Madison. Wisconsin, by J. J. Hickey in 1965 to examine the c; uses of disappearance of the Peregrine from the eastern United States, all conccisablc factors were considered in detail. Among these, only environmental pollution was consistent will) the pattern of extinction observed in Peregrine populations in both Europe and North Anieiicii (Mickey. iy69). Since rcpioduclive failure now appears to threaten the survival of the Arctic populations, it has be come imperative to determine more precisely the particular pollutants responsible. In addition to the evidence relating excessive adult mortality to the use of several of the more toxic of the chlorinated hydrocarbon insecti cides, RatclifTc (1970) has accumulated a con siderable amount of data relating the shell thinning among British birds of prey to the ienvironmental distribution of organochlorine pollutants, including both insecticides w ith their iderivatives and industrial compounds. The latter consist primarily__of--polychlorinated^ Jbiphenyls which have become widespread and ' ,locaUyabuffdant pollutants (Jensen cl al. 1969; Koeman cl al., 1969; Risebrough ci al. 1968). Other pollutants that might be contribu ting to the decline of the North American iPeregrines include mercury and lead. Mercury' 247 DSW 026513 STLCOPCB4010474 248 Tut Canadian Ficdd-Nas urai.ist Vo!. 84 is mofc widespread in lire environment than was previously suspected (l-'iinrcitc ct at., this issue). Waterfowl may accumulate, lend--front months old. Seven were biopsied in 1968 and three in 1969. All of the Merlin samples were obtained in 1969. Three wxrc adult males, one ingested shotgun pellets (Bnglcy and Locke, "T967) Tirvtt Peregrines preying ti[ion them might acquire dangerous concentrations. There is as an adult female, and the remaining three were immatuics of the year. . The biopsy technique has been described yet, however, no evidence that links either metal at environment; I concentrations to the shell thinning phenom -non. Proof is rapidly accumu previously (Fnderson and Berger, 1968). There have bran no indications that this procedure harms tic birds in any way. Biopsy samples lating, however, hat one or more of the chlor have b.cn obtained from Harriers (Circus inated hydrocarbons, particularly the DDT cyanens) that have been observed for many compound DDL. may induce sjtclMihjaning,.. months afterwards (Frances Hamcr.strom, perunder both env rohuTCTTCal and" experimental sonal communication). conditions (Micky and Anderson, 1968; Porter The adipose tissue biopsy samples were and Wiemeyer, 1969; Heath rr at., 1969; frozen, either in acetone-washed glass sials Anderson ct at.. 1969). Very small concentra capped with aluminum foil, or in sterile packets tions of DDF. a e associated with significant lined internally with aluminum foil which arc changes in shell laickncss in eggs of the Brown used in medicine for antiseptic gauzes. 7 he Pelican (Veteran is occidcntalis) (Risebrough, samples were weighed in the laboratory to obAnderson and Sthreiber, unpublished observa tain wet weights and then ground in a Waring tions). The role )f DDF and of other chlorin blcndor with anhydrous sodium sulfate. Lipids ated hydrocaibous found in the environment were obtained by soxhlct extraction for at least such as dicldrin and the polychlorinated bi six hours with a hot mixture of tsvo parts of phenyls in producing additional sublethal clTects hexane ; nd one part of acetone. T he organic that might interfere with reproduction is as yet solvents were removed by evaporation. When unclear. Delayed breeding or abnormalities in small amounts of sodium sulfate were carried behaviour could be associated with the high over into the extract, the lipid was dissolved in rate of steroid degradation caused by the liver petroleum ether and washed with water. enzymes induced ny these compounds f Jefferies, 1 he biopsy samples w-lT*. mhuIj. The iVic- 1967; Peakall, 1970). The volume that emerged from the 1965 coifcrcncc in Madison (Hickey, 1969) concludes with the statement by Hickey grille samples averaged 0.49 grams, with a range from 0.0496 to 0.983 gm. and the Merlins averaged 0.162 gm, with a range from 0.0497 to and Rocllc "How much industrial pollutants like 0.5608 gm. Some samples were found to consist the polychlorinated biphenyls have also contri mainly of connective tissue rather than lipid. buted to some of these phenomena promises to The Peregrine samples consisted of an average be an absorbing chapter in the research of the of 699c by weight of extractable lipid, with a ' immediate future" (Hickey and Rocllc, 1969). range from 3 I 57 to 9157. One Merlin sample /The present paper reports on the polychlorina- consisted of only 59?. lipid, the average percent ted biphenyls and other chlorinated hydro lipid among the Merlin samples was 35 57. and carbons in fat biopsy samples obtained from ten (Pcrcgiincs and seven Merlins (Pigeon Hawk, Valeo cotnrnbarins) trapped at the Cedar Grove Ornithological Station on the western shore of Lake Michigan during the fall migrations of 1968 and 1969. Materials and Methods the highest value was 685c. The lipid extracts wxrc diicd at 65c for 8-12 hours, weighed in the beakers, dissolved in hexane and divided into one or more aliquots. The aliquot analysed for the DDT and PCB compounds was passed through a modified Davidow column (Stanley and LeFavoure. 1965). This column, consisting of eelite, sul- All of the Peregrines were immature birds of furic acid and fuming sulfuric acid, permits the year and therefore approximately three rapid cleanup with quantitative rccov- I 1 | : , ! * j ' I J | , 1 1 ! t j { ; I ! | j , i i , , , ! 1 j 1 ; 'i j j J j ! j 1 ^ j i 0SW 026514 i I 1 ' V STLCOPCB4010475 1970 Riseiirough et. al.: Pollutants in Peregrines ano Merlins 249 cries of ihc DDT compounds and PCB. of the polychlorinated biphenyls encountered in Allhough not an important factor for the environmental samples. DDE frequently con present study, it permits much larger amounts stitutes 90% or more of the DDT compounds of lipid material to he treated at one lime than present in wildlife. The electron capture re docs the flor'sil method. This procedure, how sponse of DDE is considerably greater than ever destroys dieldrin and to determine this that of PCB, and although one of the PCB compound another method must be employed. compounds emerges at approximately the sa nc Another aliq lot of the lipid extract, in hexane, lime as DDE, the error introduced in the D )E was partitioned twice with acetonitrile, the determination is less than experimental cr or combined acetonitrile fractions were evaporated even when the total PCB concentration is up to l.r divness. redissolvcd in j'clrolcum ether, and five times that of the DDE. Vermeer and Ri y- applied to a llofiui column. The column was nolcls (1970) have commented upon the diifi- rinsed first with 200 ml of petroleum ether and cully in separating the DDT compounds p. 200 ml of 6% ethyl ether in petroleum ether. DDD and p,p'-DDT from PCB. On the DC-2 X) Dieldrin was eluted by passing 200 ml of 15% column, both DDT compounds emerge at ethyl ether in petroleum ether through the col approximately the same time as a PCB pc ik umn. Control., had indicated that 90% or more (Anderson et al., 1969). On the QF-1 colun n, of the dieldrin applied to a florisil column eluted however, there is no interference between p.p'- in this (racin'n. DD f and any of the polychlorinated biplicn Is Blank samples consisting of redistilled petro usually encountered in environmental sample . leum ether analysed througli the entire proce I Although many different chlorinated biphcryl dure showed no substances that might interfere //compounds arc released into the environmet t, with the determination of any of the chlorinated relatively few persist iq ||)r- higher |pwlt f0(jCJ hydrocarbons reported here. l(chains. Moreover, these arc found in appro) i- The extracts were analysed with a Microtek gas chromatograph equipped with a tritium and a nickcl-63 electron capture detector. Glass columns were used containing 3% OF-1, or a mixture of 3% QF-1 and 10% DC-200, on Chromosorb W, 80-100 mesh, acid washed and HMDS treated. Other laboratories (Reynolds, 1969; Armour and Burke, 1970) have developed methods for separating the polychlorinated biphenyls from some or nil of the chlorinated hydrocarbons of insecticide origin. The polychlorinated biphenyl mntely the same proportions in environment ll samples over wide areas of the world. Ti c chromatograms of the PCB compounds in the Peregrines analysed in the present study ate therefore similar to the chromatograms of Petegrine extracts from Mexico. California, and Amchitka Island (Risebrough, unpublished re sults). Moreover, the chromatograms arc similar to those obtained from extracts of Brown Pelican eggs from several areas in both North and South America (Risebrough, unpublished results). It is frequently possible, therefore, to compounds emerge at different times from the treat the PCB mixture as a single compound gas chromatograph and occasionally a peak may and to obtain accurate relative concentrations coincide or interfere with the peak produced of PCB using any one of the several peaks. T he by one of the insecticides. We have found it peak emerging at the same time as p.p'-DDD possible, however, to quantify PCB, DDE, on the QF-1 column is almost always of the p,p'-DDD, p,p'-DDT, dieldrin and endrin on same height as two of the other peaks. It is the basis of the procedure outlined above, with therefore possible to obtain a crude estimate of out any attempt at separating the PCB. Dieldrin the DDD present without initial separation of and DDE emerge at exactly the same time on the PCB. This assumption may be tested and the the DC-200 column, but on the QF-1 column identification of p,p'-DDT and p,p'-DDD con there is no significant interference between firmed by saponification (Anderson et al., 1969; dieldrin and DDE, or between dieldrin and any Risebrough et al., 1969). An aliquot of the DSM 026515 STLCOPCB4010476 250 The Canadian Fielo-Naturalist Vol. 84 extract, in hexane or petroleum ether, is re fluxed in 5% KOH in ethyl alcohol. The hexane is then separated front the alcohol and potassium hydroxide by the addition of water and a sample injected into the pas chromatograph. The pro cedure converts both DDT and DDD to their respective ethylene derivatives, DDE and DDMU, but leaves the PCB profile of the chromatograms unchanged. Since the profile of ihc PCB peaks was similar, but not identical to the profile observed in chromatograms of the commercial prepara tion Aroclor 1254, PCB was quantified by comparing the total area of the PCB peaks emerging after DDE with the areas of the same peaks in chromatograms of standard Aroclor 1254. The procedure is therefore arbitrary, but permits the deter nination of relative. amounts of PCB within the correct order of magnitude of absolute amounts. Moreover, the values ob tained can be readjusted as methodology is improved. Results and Discussion Enderson and Berger (1968) have previously reported on the chlorinated hydrocarbon resi dues found in biopsy (at samples from immature Peregrines that were also trapped during fail migration at Cedar Grove, Wisconsin. These samples, analysed by the' Wisconsin Aiuntni Research Foundation in Madison, Wisconsin, contained an average concentration of 19.4 ppnt of DDE on a lipid basis. DDE concentra tions in the fat of females at Ihc Arctic breeding grounds arc much higher, in the order of 300 ppm or higher (Berger et al., this issue). The ten Peregrine samples analysed in the present study contained 17.9 12.3 ppm DDE, 0.23 0.34 ppm p,p'-DDD, 0.71 0.68 ppm p,p'-DDT, 18.8 i 12.5 ppm total DDT (DDE -j- p,p'-DDD + p.p'-DDT), and 52.2 32.3 ppm PCB. Seven samples were analysed for dicldrin, which averaged 0.40 0.64 ppnt. AJI residues are expressed on an extractable lipid basis, with the 95% confidence limits of the standard error of the mean. The values for p,p'-DDD and p,p'-DDT arc lower than those previously reported by WARF, Inc., presum ably a result of interference by PCB in the earlier determinations (Anderson et al., 1969). The dicldrin values are equivalent to those previously reported and there is no significant difference in the DDE concentrations. On a lipid basis, the average values reported by WARF. Inc. were 19.3 ppm DDE, 0.8 ppm DDD, 1.2 ppnt p.p'-DDT and 0.3 ppm dicldrin (Enderson and Berjer, 1968). First year immature Peregrines migrating from the Arctic have therefore low residues of DDE. Unfortunately little is known about the relationships among dietary levels of DDE and PCB, equilibrium concentrations of these com pounds in various tissues, and the limes required to achieve an equilibrium concentration. The low concentrations found in these Peregrines presumably reflect therefore both the age of the birds, which possibly has not permitted them to accumuhle the high concentrations found in adults, and lower levels of contamination found in some )f the prey species. An understanding of the pharmacodynamics of DDE and PCB in birds is one of the conspicuous deficiencies in our knov ledge in the field of pollution ecology. Within several ecosystems so far studied, the concentrations of DDE in birds tends to parallel the concentrations of PCB. The ratio may be approximately one to one, as in San Francisco Bay (Risebrough el al., 1968). DDE is several times more abundant than PCB in several Pacific marine ecosystems (Risebrough et al., 1968), but in Florida, PCB is approximately three limes as abundant as DDE in the Brown Pelicans (Risebrough, Gress. Anderson and Schrcibcr, unpublished manuscript). The cor relation coefficient between the DDE and PCB concentrations is frequently highly significant. These observations have suggested that the ratios observed reflect the local fallout pattern of the DDT and PCB compounds, and that the DDE and PCB show similar patterns of accu mulation, concentration and excretion in the birds and possibly other members of the ecosys tem. Among the 10 Peregrine samples analysed, PCB was more abundant than DDE by approximatcly three times. 1 tie correlation ct>- 0SW 026516 i i i i i i \ f I J I ii i i \ i i f j i I ) i ii i i l i STLCOPCB4010477 14 1970 RistnRoucii et. ae.: Pollutants in Peregrines and Merlins 25 if ! efficient is 0.8897, which is significant at the shell thinning associated with egg breakage, ) 0.001 level. Although it is not known from disappearance of (lie eggs, and eating of the NC ; which area of the Arclic these hints have conic, eggs by the adult birds (Ralclilfc, 1 970), In the !n! i ihe results suggest that over a considerable area Ungava population (if Peregrines in the eastern lid 1 of ihe tundra ecosystems occupies! by the Pcrc- Arctic, shell thinning and eg); breakage are nov i grilles, this ralio reflects the local fallout pattern contributing to reproductive failures (Bereer c 2 l ; of DDLs and PCB. al.. Ibis issue). The evidence available to dan in j The four adult Merlins averaged 302 ppm suggests, however, thnTTCB is not'a cause m DDE (1 39-704 ) in the lipid fraction, This value tire's] ell Thinning observed in many population . I may be compared with an average conccntra- oTEOr NrTcor rein tion bet ween Thinning a n i1 of | tion of 392 ppm in the lipid of 9 breeding PCB vas round in the eggs of the White Pelican " ilic I Peregrines from the Mackenzie River region JTelcranus eryllirorhyncfibs) (Anderson cl al., nd j (Enderson and Berger, 1968), 725 ppm in 1969> or in eggs of the Great Blue Heron ' the fat of four adult Peregrines from Alaska (Ant-a Werodtax) fVcTmccr and Rcynolcfs. fd i (Cade et al., 1968) and 334 ppm in the lipid of 1970'. An analysis of approximately 200 eggs he ! 9 adult Peregrines from Ungava (Berger et al., of tli: Brown Pelican from both eastern anu U'S i this issue). Merlins therefore may possess al western North Amcrica.Jias shown that DDE he I most the sam level of contamination as the rathe- than PCB is associated with the slid to , . , Peregrines anc might therefore be expected to thinn ng rRTschrnugh, Gross. Anderson an I in 1 show symptoms of shell thinning. The conccn- 'Sclirc ber, unpublished ms.) Whenever corre nd tralions of total DDE in the adult Merlins lations between PCB and shell thinning haw np I averaged 314 ppm. 96C8 of the DDT residues been observed, as in Double-Crested Cormor in | in these Merlins therefore consisted of DDE. ants 1 Phalacrocora.r auritus), PCB is also cor in | The PCB concentrations averaged 196 ppm related with DDE (Anderson et al.. 1969). 'V- I (44-467). The samples were not analysed for Pc ikall (1970) has reported that p.p'-DDT lie dicldrin. - delays egg laying in the Ringdove (Sircpto/<elit< del In the three immaturcs. DDE averaged 49.3 risoria) and that the delay is associated with he , ppm (10.8, 18.6 and 119.3), total DDT aver- lower concentrations of estradiol in the blood ro j aged 50.3 ppm, and PCB averaged 28.6 ppm carly in the breeding cycle. Peakall had entiicr ml I (5.7, 29.0 and 51.2). With the exception of one reported (in Risebrough et al., 1968) th.i ml j' immature Merlin that contained 18.6 ppm DDE technical DDT. p.p'-DDE. and PCB induce the nL, i and 51.2 ppm PCB, a ralio similar to that found synthesis of liver enzymes that degrade estradiol, ely j in the Peregrines, all other Merlins contained and that PCB is a more potent enzyme inducer wn | more DDE than PCB. With the one immature than is DDE. Delayed breeding may therefore md I excepted, TCB was significantly correlated with be one of the environmental effects of PCB, an or- l DDE (r -- 0.9820, p less than 0.001, four effect that could be critical to Arctic-breeding CB J degrees of freedom), Most of the Merlins, birds which must complete their reproductive ml. therefore, appear to be comtiTg from a region oP cycle within a restricted period of time. the j the boreal forest where the polfuTanTTnllout A recent investigation in Japan of (lie cm j -pattern is different from th.it in~THe~ tundra' "Yusho" or Rice Oil Disease has traced the the I ecosystem occupied, by__tlic_ Peregrine. ' cause to rice oil contaminated by chlorinated cu- T When PCB was found to be present in Pcrc- biphenyls (Kntsuki, 1969). Both the contamin thc grilles, occasionally in high concentrations, it ated rice oil and the Japanese commercial I'CB ys- seemed likely that these pollutants were con produce symptoms when fed to chicks similar tributing to the reproductive failures associated to those observed in the "chick edema" syn -cd, with population decline (Risebrough et al., drome (Goto et al., 1969). This disease of np- . 1968). The dominant symptom of reproductive chicks was first observed in the United States co- failures of the Peregrines in Britain has been in 1957, and among the symptoms were accu- I i t rrr DSW 026517 STLCOPCB4010478 252 The Canadian Fiei.d-Natukai.ist Vo!. 81 mnlntion of Unit! in the pericardial sac and in the abdominal cavity, subcutaneous edema, and liver and kidney damage (Verrett, 1970). Chlorinated tlibcnzo-p-dioxins have been shown to be one of the groups of chlorinated synthetic compounds that produce this disease (Higgin botham n. til.. 1968). These compounds have also been shown to be present in the herbicide 2,4,5-T and induce both mortality and embry onic deformities in chicks at very low concen trations (Vcti.it. 1970). A similar group of compounds. iiic chlorinated dibenzofurans, are / almost as toxic (Schulz, 1970). These resemble / the chlorinated biphenyls in structure~and might I be derived from them. ^Whether they arc now I present in the environment and pose a threat I to wildlife promises to be "an absorbing chapter /in the research of the immediate future" / (Hickey and koclle, 1969). Acknowledgement The research was supported by the National Science Foundation grants GB 6362 and GB 11649. , Literature Cited Anderson, D. W., Hickey, J. J., Risebrouglt, K. W,, Hughes, l). I'., and Christensen, K. E. 1969. Sig nificance of chlorinated hydrocarbon residues to breeding pelicans amt cutmuianis. Canadian EieldNaturalisl 83(2): 91-112. Armour, J. A. and Iturkc, J. A. 1970. 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M., Snkagtichl, K.. and Ogai, K. 1969, Hydropericardium assay of rice oil which caused Yusho and of Kancchlor 400 in Chickens (in Jap anese with English abstract). Fukuoka Acta Medica 60: 5 33-538. Hall, G. II. 1955. Great moments in action: 7 h story o( the Sun Lite Falcons. Mercury Press. Montreal (Reprinted in the Canadian Eicld-Naluralist ;4 ( 3 ): 213-2 30. Mcalf, It. G,, Spann, J. 'V,, and Kreitzer, J. F. 196r. M;ii fed DUE impairment of Mallard reproduction in c intruded studies. Nature 224: 47-48. Ilickc; , J. J,, editor. 1969. Peregrine Falcon Pop ilations: Their Biology and Decline. UnivcrsiE' o( Wisconsin Tress. Madison. 596 pp. Ilickc;, J. J. and Anderson, D. W, 1968. Chlorin ated hydrocarbons and eggshell changes in raptorial and fish cating birds. Science 162: 271-27) Hicke; , J. J. and Roelle, J. E. 1969. Conference summary and conclusions, in Peregrine I'alcor Populations: Their Biology and Decline. J. J. Hicl ey, cd. University o( Wisconsin Press. Madison pp. 553-567. 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B, 1970. p.p'-DDT: EITect on calcium metabolism and concentration of estradiol in the blood. Science 168: 592-594. Porter, R. D. and Wlcmcyer, S. N, 1969. Dieldrin and DDT: Effects on Sparrow Hawk eggshells and reproduction. Science 165: 199-200. Ratcliffe, D. A. 1963. The status of the Peregrine in Great Britain. Bird Study 10: 56-90. RalclifTr, D. A. 1967. Decrease in eggshell weight in certain birds of prey. Nature 215: 208-210. Ratcliffe, D. A. 1970. Changes attributable to pesli cides in egg breakage frequency and eggshell thick ness in some British birds. Journal of Applied Ecology 7: 67-115. DSW 026518 STLCOPCB4010479 1970 Riseurough et. al.; Pollutants in Peregrines and Merlins 253 Reynolds, L. M. 1969. Polychlorobiphcnyls (PCIJ's) au<J ihcir interference with pesticide residue analysis. Journal of Environmental Contamination and Toxicology. 4: 128-143. Kisebrough, K. W., Ketehr, P., Pcnkflll, D. HM Herman, S. G* and Kirvrn, M. N. 1968. Polychlorinated biphenyls in the global ecosystem. Nature 220: 1098 V 1102. Rist-brough, JL W.t Krichc, P., and Olcolf, II. S. 1969. Current Progress in the determination of the polychlorinated biphenyls. bulletin of Environ mental Contamination and Toxicology. 4; 192-201. ScliuU, K. II. 1970. Clinical picture and etiology of chloracnc. Reprinted in: Effects of 2,4,5,-T on Man and the Environment. Hearings before the Subcommittee on Energy, Natural Resources, and Ihe Environment of the Comrpiitee on Commerce, United Stales Senate. Serial 91-60. U.S. Govern ment Printing Office. Washington. D.C. Stanley, II. I.. and l^eFavoure, J|. T. 1965. Rapid digestion and clcan-up of animal tissues for pesticide residue analysis. Journal of the Association of Offici;i! Analytical Chemists. 4R: 666-667. Vtrmttr, K. and Reynolds L. M. 1970. Orga 10* cl lorinc residues in aquatic birds in the Canad an Prairie Provinces. Canadian Field-Naturalist 84: I '7-130. Venett, J. 1970. Statement before the Subcomm ttee on Energy. Natural Resources, and \hc Environment. In: Effects of 2,4.5-T on Man and the Ei vironment. Serial 91-60. U.S. Government Prill ing Office, Washington, D.C. Received October, 1970 Accepted October, 1970 ' f DSW 026519