Document 0LqvE1boRg91ZLbmqLOZVZveJ

oe> rda- v 1 Chlorinated Hydrocarbons and Eggshell Changes in ' * { Raptorial and Fish-Eating Birds (9\. Analyses were conducted on a j;as chromatograph (Karher Coleman, model GC 5000, and Jarrcll-Ash. model 28- 7(H)) with cleciron-capmre detectors. Abstract. Catastrophic declines of three raptorial species In the United Slates The glass column (0.6 cm by 1.2 m) was lure been accompanied hv decreases in eggshell thickness that began in 1947, packed with 5 percent IX' 200 (I2.S0O) ht\r aniounietl to 19 percent or more, and were Identical to phenomena >n Cromporl XXX. The column tem 2 reported in Britain. In 1967, shell thickness in herring gull eggs from five states perature was 2I0C, and the nitrogen 3 decreased with increases in chlorinated hydrocarbon residues. (low rate was 75 cm 7 min. F.ach por S 2 tion of the ground and dried samples 1 New perspectives on the role of chlo declining populations; golden eagles was extracted for 8 hours or more in a rinated hydrocarbon insecticides in our (Aquila chrysaeetos), red-tailed hawks Soxhlct apparatus with a mixture of I environment have come into focus in recent years. Successive discoveries have 720, | demonstrated that these compounds are (Buteo famaicensis), and great horned owls (Bubo vlrginianus) were selected as representative of reasonably station ether and petroleum ether (70:170). Portions of the extracts were further purified by putting them through a e of I systematically concentrated in the upper ary populations that may be slowly de Florisil column. a the | inop- I d 19 I orted u in trophic layers of animal pyramids (/). Raptorial bird populations have simul taneously suffered severe population crashes in the United States and Western Hurope (2, 3, 4). These involve repro ductive failures which, at least in Brit clining as their habitats are gradually destroyed by man, but for which wide spread reproductive failures are cur rently unknown. In addition, 57 eggs of the herring gull (Lotus argentatus) were collected from five colonies in In California, where the peregrine falcon population is in "a serious con dition" (10), a change of 18.8 percent in shell weight occurred from 1947 to 1952. Ratcliffe (6) found a correspond ing decrease of 18.9 percent in Britain. ain, are characterized by changes in can calcium metabolism and by a decrease only m eggshell thickness resulting in the (the parent birds' breaking and eating their ; tur- own eggs (4, 5, 6). Such a derangement 1 > in J of calcium metabolism or mobilization rcijon perhaps could result from breakdown of irity. vtcroids by hepatic microsomal enzymes trrent induced by exposure to low dietary y arc levels of chlorinated hydrocarbons (7). 1967. The shells of these were dried at room temperature for 4 months before being measured, and residues of the en tire egg contents were analyzed by the Wisconsin Alumni Research Foundation for chlorinated hydrocarbons but not for polychlorinated biphenyls. Analyti cal procedure followed that outlined by the U.S. Food and Drug Administration The change in California involved a de crease in shell thickness and had no precedent in the previous 57-ycar re corded history of the peregrine in that state (Fig. 1). In the eastern United States, where the nesting population of peregrines has now been wiped out (3), fragmentary data indicate that the same change took place (Table 1). Broken r plot hown conrhaps at ion cont one (crinj rough been Kay* erinff. 21 We have examined the possibility that the eggshell changes reported in Britain (6) have also occurred in the United States and that the raptor population crashes in Europe and North America may have had a common physiological mechanism. The population change?, arc without parallel in the recent history of bird populations (8). They include the pending extirpation of the peregrine falcon (Ftdco peregrinus) in northwest ern Europe, the complete extirpation of the nesting population of this species in ihe eastern half of the United States, jrtd simultaneous declines among other Table 1. Weight* of raptor eggshells in museum and private collection*. Citations (23-23) refer to the data for the population trend; S.E., standard error of the mean. Region Period No. Weight (!) Mean S.E. Chango (%) Population trend (or reproduc tion) Calif. (33) Calif. (33) Brevard Co, Fla. 18X5-1937 1943--44 1953-67 1889-1939 1940-46 1947-65 1886-1939 1947-62 Retl-tatled hawk 386 6.32 0.032 6 6.09 0.237 8 6.49 0.214 Golden eagle 278 13.03 0.083 28 12,70 0.161 33 13.41 0.232 Bald eagle (24a) 56 12.15 0.127 12 9.96 0.280 - 3.6 + 2.7 - 2.5 -1- 2.9 -- 18.0 Stationary Stationary Stationary Stationary Declining bird- and fish-eating raptors on both sides of the Atlantic. !J). We examined 1729 blown eggs in 39 (19*41. . museum and private collections. Shells : E. a (19*2); wen weighed to the nearest hundredth of a gram. In 29 percent of these, we cre able to insert a micrometer FluU Univ.. through the hole drilled by (he collector rt-Hcny. iuafurd i.-. Si* d SU I than), rlfiwni a the girth of the sliell and to lake four measurements of thickness 7 mm from he edge of the blow hole; these were then averaged to the nearest 0.01 mm lor each shell. Thickness in each case then represented the shell itself plus the dried egg membranes. Peregrine falcons, Co0* Md eagles (llallaeetus leucocepitalus), `d ospreys (1`undion ludiaelus) were se Osceola Co,, Fla. M<L-Va. NJ. B.C. ;1 1 Calif. (23) NX. to NJ.* Vt Maaa. NJ. Calif. (23) 1901-44 1959-62 1890-1938 1940-46 1955 1880-1938 1957 1915--37 1947--53 1895-1939 1940-46 1947-52 1888-1932 1946 1947 1950 1886-1936 1948-50 25 12.32 0.240 8 9.88 0.140 Osprey (24b) 152 7.05 0.054 21 6.91 0.164 3 6.85 117 7.08 0.069 6 5.30 0.446 Peregrine (23) 4.24 0.061 15 4.18 0.081 235 4.20 0.031 49 4.07 0.038 31 3.41 0.084 56 4.38 0.034 3 4.30 3 3.47 3 3.24 Great homed awl 134 4.50 04)33 12 462 0.119 - 19.8 Declining - 2.0 -M -25.1 Stationary Stationary Declining - 1.4 - 3.1 - 18.8 - 1.8 - 20.8 -26.0 St iilionary No data Declining Stationary Extirpated Extirpated + 2.4 Stationary lected as having one or more regionally M- 1C II OCTOBEK 19M * ladudtae Vermont and Mamertmaett*. 271 332232 STLCOPCB4078808 eyrie were observed for the first lime in 1947 by J. A. Hagar 60 miles (9.6 km) from the Massachusetts eyrie cited in this table (//). They were nest inferred in Quebec in 1948 when egg-eating was observed at the same site in 1949 (12), and were observed in Pennsylvania in 1949 and 1950 (IS). Chlorinated hydro* carbon data for this now-extinct region al population are completely absent. For nine surviving adult peregrines in Cana da's Northwest Territories in 1966, the data are reported to have averaged 369 parts per million (ppm) (fresh weight) in fat (14). For four adults in another migratory population in northern Alas ka, values were even higher (IS). Fig. 1. Measurements of 614 California peregrine eggshells collected since 1891. The dotted horizontal line is the midpoint between the 95 percent confidence limits for 1947-52 and the lowest of any pre ceding group. Solid horizontal bars are means; rectangles, 95 percent confidence limits; heavy vertical lines, standard devia tions; narrow vertical lines, range in sam ple. The thickness index, calculated as ten times the weight divided by the product of the length and breadth (in mm) of earn egg, was devised by Ratcliffe (6) for the study of museum eggs and appears here to be a meaningful statistic. The sizes of samples for measurement of weight and of thickness index for the periods were 71, 49, 36, 85, 155, 30, and 31, respectively; and the sizes of the tamplea for measurement of thickness were 24, 31, 29, 23, 37, 7, and 6. 171 have studied, the data do not permit a precise delineation of the onset of the change in calcium metabolism or mobi lization, but the decrease (Tabic 1) in shell weight (and hcncc thickness) has involved only declining populations and not stationary ones. Change in shell thickness occurs in poultry as a result of dietary deficiencies and age (16, 17). This phenomenon would probably not occur simultaneously on two continents 1 year after the chlorinated hydro carbon insecticides came into general usage. Other chemicals affect shell thickness in poultry (17), but the find ing of high concentrations of chlori nated hydrocarbons in the eggs of wild populations of raptors and the time correlation of shell changes with the introduction of DDT (1,1,1-trichloro-2,2-bis (p-chlorophenyl) ethane] tend strongly to suggest that chlorinated hydrocarbons are the major contributing cause, although it is not unlikely that other chemicals could be contributory. In order to test the hypothesis that these recent changes of thickness in raptor eggshells were the result of dif ferences in exposure to chlorinated hydrocarbons we analyzed 10 to 14 eggs taken in 1967 from each of five colonies of the herring gull (Larus arRentatus). Mean shell weight and thick ness in 55 eggs collected in the same five states prior to 1947 disclosed no geo graphic gradients or significant differ ences. The 1967 mean thicknesses for each colony were therefore compared to mean levels of residual DDE [1,1dichloro-2,2-bis (p-chlorophenyl) ethyl ene] on a fresh-weight basis, with the result shown in Fig. 2, the r value being significant, with P = .001. The residues of polychlorinated biphenyls (18) have not been studied in these ecosystems, but DDE has been consistently high in the Lake Michigan birds, averaging (fresh weight) 1925 ppm (S.E. 274) in the fat of 12 healthy adults collected in 1963-64 (19). Reproduction in these gull colonies was generally normal in 1967 except perhaps in Wisconsin. At the latter colony where an 11 percent mean de crease in shell thickness occurred, some egg breakage and shell flaking was evi dent in 1967, although not at the fre quency seen in previous years. Excessive reproductive failure occurred at this site in 1964 when about 18 percent of the eggs lost about one-third of the shell due to flaking, when dutch size decreased and embryonic mortality was high, and when DDE residues averaged Fig. 2. Variation in shell thickness )nj DDE concentrations in the eggs of herringulls in 1967. The eggs were taken c* Block Island, R.I.; Green Island in PenoK scot Bay, Me.: Rogers City, Mich, <y Lake Huron; near Knife River, Minn, <*. Lake Superior; and the Sister Islands i; Green Bay, Wis. Some polychlorinauj biphenyls probably occurred in these e^ but they have not yet been identified. 202 ppm (S.E. 34) in nine or. (20). (If linear extrapolation of the IV values is carried out to 202 ppm, shell thickness in 1964 could he mated as having decreased by about percent.) The effectiveness of DDE : the enzymatic metabolism of aminof. rine has been reported by Hart ar Fouts (21), and our data suggest ik this compound, because of its pro. lence, has played a major role in ind,. ing the hepatic microsomal mctahol. of steroids that in turn resulted in r. eggshell changes we have encounter, in museum collections. Without do.'DDE is the commonest insecticide > insecticide analog now being found avian tissues (22). In 1966, it was foe. to average 284 ppm (S.E. 62) in the of nine arctic-breeding peregrine f. cons (14) and about 414 ppm in f.others on a wet-weight basis (IS). Co centrations of this compound and oi:' chlorinated, hydrocarbons in the per grine populations that crashed fan" south can be assumed to have bent. high--and they may have been u'higher. From the above evidence and i accumulated by others (2, 4, 6, S), have reached these conclusions; i many of the recent and spectar. raptor population crashes in both : United States and Western Europe h. had a common physiological bask eggshell breakage has been widesprbut largely overlooked in North Ar ica; (iii) significant decreases in ` . thickness and weight are character, pf the unprecedented reproductive; urcs of raptor populations in cere science, vot DSW 332233 set of I the intr carbons random sisting c insidiou1 birds a ccosystc: Departn Universi 1. E. G dame Prstlciv of Wi 24H-2M 2. C. Den Mnkol P. Lint ibid. 23 HO (I9< frrrnce national 1964), \ 3. D. D. (iambic. Their B (Univ. < P. 165. 4. IV A. K 6. ------ . 7. IV II. P Una. K. Arpl. Pi iu\v. Phi Ktipfcr. <. H. J. J. Hit tiiHt.i; Ti : W|>con>i?. 4. V.S. Pixv' tide A mu ' Health. F Publ. (I* to. B. Gladir 11. J. A. Ha 12. Ci. H. Ha IV J. N. Ric U. J. H. En 7i. 149 (1 IV T. J. Ctd< P. 170. 1A. A. L. Ro A vian Eg 154-157. 17. T. G. Tay Phyiiology Press, Iiha I* D. C. Hoj: ton. Natur 1*. J. J. Hicke: Ecol. 3 (si. V J. A. Kelt N966). L. G. Hat Ptifhoi. Ph<i -- E. H. Dus Vtr, Ai>fon L B. Dixoi V Harrivo munication. ,4. A. Spruni. Nh- W. A. Stic :v P^cpt for in populati* 1- Beebe ( v,P>fTord (oi Mjssjchusci V.r New Je bi-search cai Bureau of S nd Wildlife " H. Drur ruwtded kuI fx>n, w. c facj|i 'Ik-Ms. Wc (i ihrouphout (i July IVfc# 11 OCTOBER 11 STLCOPCB4078809 OMX L less and i 1 herrin.' I tken of j t Penoh- t ich., on | linn., on I lands in j lorinatcd > ne eggs, l Iked. ! rI * cF"' ; he 19ti7 j pm, the 1 be csti- I bout 32 DDE in I minop)- | lart and | test that ' s prcv.i. j n induetabolism j d in the J ountersJ 1 at doubt ' ticidc or J found ir, : as founJ n the f->: rine fuli in four 5). Conaid other h. e pure1 farther - j ! i i been ai en mueh and that 6, S), vc ons: (i> ectacu!-' both t1 ope h..'basis: idespts th Am i in '1 -actons; rtive u n cert- j ! . , ! ^ VOl i " ^i of the calcium change 1 year aficr ihe introduction of chlorinated hydrocjrhons into general usage was not a rindoni circumstance; and (v) these per sisting compounds arc having a serious insiJious effect on certain species of birds at the tops of contaminated ecosystems. Joseph J. Hickey Daniel W. Anderson Department of Wildlife Ecology, University of Wisconsin. Madison Rrferoirr* mm4 Nolen |. P. Ci, Hum and A. I. Bitchoff, Cal//. Fhh tiame 46, 91 (1*60); review In R. L, Rudd, Potuldts arid the Lltlng Landscape (Unlv. p( Wisconitn Presi, Madison, 1964), pp. 1 C Demandt, Ornithol. Mitt. 7. 3 (1933); P. I mknta, Suomrn Lrusnlo IS. 3, 34 (1939); p linkoli, thld. 19. 20 (I960); P. Llnkola, ihid. 23. 3 (19641; K. KlctiuOtuber, Falke IS, ml (1963); C. Kruyfhooft, in tVorhlng Conlmnce on Birds e/ Frey and Owis (Inter, njiinnal Council Bird Protection, London, JW4), p. 70; J.-F. Terraaae, Udd., p. 73. ). r>. D. Berper. C. R. Slndelar, Jr., K. E. ii.mbie, in Frregrlna Falcon Populations: Their Biology and Decline, J. J. Hickey, Ed. (l.'ni*. of Wiiconain Preu, Madiion, 196S), - 165. 4 I) A. Ralclifte. Bird Study IS, 36 (1963). s -------- , Bril. Birds SI. 23 (195S). r-------- . Nature 215 . 20* (1967). 7 I) B. Penkad. Ibid. 216. 305 (1967): L. O. tljii. R. W. Shullica, J. R. Fntiti, Toxicol. Appt. Pharmacol. S. 371 (1963); A. H. Con wy. Pharmacol. Rev. 19, 317 (1967); D. kupfcr. Residue Rev. 19, II (1967). i. i J. Hickey, Ed., Peregrine Falcon Fopulahum: Their Biology and Decline (Unfa, of Wisconsin Press. Madiaon, 1968). * i: S Food and Drug AdmlniMratlcm, Bestt iJr Analytical Manual, vol. 1 (U.S. Dept, of llcjlih. Education, and Welfare. FDA Adm. I'uN. (1963, revised 1964 and 1965)]. ' H Glading, in Hickey (8), p. 96. ) A. Hspar. in Hickey (8), p. 123. (> II Hall. Brit. Birds 51, 402 (1958). ' J N. Rice, in Hickey (8), p. 155. * J H. Enderton and D. D. Berger, Condor 71. 149 (1968). * r J. Cade. C. M. White, J. R. Haugh, ibid., r no. .* a I.. RomanofT and A. J. Romanoff, The (.m Egg (Wiley, New York, 1949), pp. i 54-157. ' T (i. Taylor and D. A. Stringer, -n Avian fhuiotngy, P. D. Sturkic, Ed. (Cornell Univ. Iros. Ithaca, N.Y., ed. 2. 1965), p. 486. '* I> C. Holme*, I. H. Simmons, J. 0*0. Tat- Mature 216, 227 (1967). * 1 i. Hickey. J. A. Keith, F. B. Coon. /. Appl. J fsuppl.), 141 (1966). 1 A. Keith. J. Appl. Ecot. 3 (svppl.), 57 Iv6h). 1 ( Ci. Hart and J. R. Fouts. Arch. Exp. r.uhol. Fharmakol. 249, 486 (1965). I II.Dustman and L.'F. Stickel. Amor. w. Agron. Spec. Fubt. 8, 109 (1966). J 8. Disnn. B. Gliding. W. C. Hanna, E. N liarriNon, S. B. Peyton, personal commkation. 1 V. Sprunt. IV, personal communication. - V A. Stickel, in Hickey (8), p. 337. ' > wept fur the California data (23) the data trends are given tn (8) by F. l Ikche for British Columbia; by W. R.. S:,'fi`6rU for Vermont; by J. A. Hagar for `l4".Khuiens; and by D. D. Berger et at. ' * New Jersey. ' ' "ih carried out under contract with the '-' "i oi Sport Fisheries and Wild'ife, Fish i Wildlife Service, U.S, Dept, of Interior. -v ll Drury, J. T. Emkn. and M. E. Slate `"kd gull cpgi for analysis. E. N. HarW. c. Hanna, and many other oologiata J,lv facilitated ow measurexNenta at egg ' A We thank D. A. RatciilCe for advice j-'iig-hout the entire study. > IV6* lOBF.R 1968 Phagocytosis by Polymorphonuclear fxriikocylcs Abstract. In vitro, the hitman polymor/ihomu leap leukocyte curt recognize and ingest the free forms of I'l.ismodium lalciparum. Digestive vacuoles form about the engulfed organisms. Neither the polymorphonuclear leukocyte nor the monocyte can recognize the parasitized red cell. 1`hagocytosis of normal or parasitized red cells was not observed. Both cellular and humoral elements and events arc involved in malaria im munity. The presence of pigment and red cells in the reticuloendothelial cells of the spleen and bone marrow led in vestigators to consider phagocytosis a most important factor in removing parasites from the blood (/). Hull and Wcathcrby (2) first observed phagocy tosis of a free schizont of avian malaria Fig. 1. Sequence of frames is from top down and from left to right. Arrow points to parasitized red cell. In the left column, a monocyte passes the parasitized red cell. In the remaining frames a polymorphonuclear leukocyte moves by the cell. Neither white cell recognizes the diseased red cell (abou( X 1000). ---- ---------1 l i Fig. 2. Sequence of frames is from top down and from left to right. In the (op frame (left column) the meimoiUA i-scapc from lysing red cell (arrow) and immedi ately attract the polymorph.m.. ..r leukocyte which cncutfs and digests them (about X 1000). DSW 332234 STLCOPCB4078810