Post-mortems of Peregrines and Lanners with particular reference to organochlorine residues. By D. J. Jefferies and I. Prestt

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1 British Birds Vol. 59 No. 2 FEBRUARY 1966 Postmortems of Peregrines and Lanners with particular reference to organochlorine residues By D. J. Jefferies and I. Prestt Monks Wood Experimental Station, The Nature Conservancy, Huntingdon INTRODUCTION SINCE 1962, when the enquiry into the status of the Peregrine Fako peregrinus was completed (Ratcliffe 1963), there has been widespread concern about the decline of this species in Great Britain. Ratcliffe found strong circumstantial evidence that the persistent organochlorine insecticides were the cause, and the pattern of the decline showed a close correlation, both geographically and in time, with their increasing use in agriculture. Also, both eggs and an adult Peregrine have been proved to contain residues of dieldrin, heptachlor epoxide, isomers of BHC and DDT and metabolites (Ratcliffe 1965; Moore and Ratcliffe 1962). However, the presence of residues in the body of a dead bird does not necessarily mean that they caused its death. Some species of birds may carry considerable quantities of these materials without any external signs of distress (Bernard 1963; Turtle et al. i<)6^; D. J. Jefferies, work in progress). The sensitivity of birds to the various pesticides can be measured by feeding trials similar to those carried out by Bernard (1963) with DDT and House Sparrows Passer domestkus. After chemical analyses these studies provide ranges of internal residues which, if found in a dead bird, allow one to say with a fair degree of confidence that death was due to toxic chemicals. However, it is not always wise to extrapolate from species in one order or family to ones in others, e.g. from the House Sparrow to the Peregrine. The amounts needed to be ingested 49

2 BRITISH BIRDS and the residues of pesticides accumulated in the liver or brain before death are known to vary considerably between individuals (Bernard 1963) and between different orders (DeWitt etal. i960, who demonstrated a seventeenfold difference between the Starling Sturnus vulgaris and the Mallard Anas platyrhynchos with respect to their sensitivities to heptachlor as shown by the lethal dose to 50% otherwise written as L.D.50). There may also be differences due to age and sex (DeWitt et al. i960). To obtain data on the susceptibility of the Peregrine by feeding experiments would be difficult and is not at present being attempted. We must rely, therefore, on other evidence, as in the cases described here. Two Lanners Falco biarmicus, which were being trained for falconry, died suddenly for no obvious reasons and after veterinary examination were sent to the Nature Conservancy for chemical analysis. The presence of substantial residues of organochlorine insecticides and the absence of any other cause of death make it likely that both died from these substances. Thus they provide valuable evidence about the amounts of organochlorine insecticides present as organ residues when one of the large falcons is poisoned and dies. Lanners are of the same genus and about the same weight as Peregrines, and probably have similar susceptibilities. The organ residues and histories of these two Lanners are detailed below and compared with those of four British Peregrines examined in our laboratory and one Peregrine studied in Holland. METHODS Measurements of specimens followed Witherby et al. (193841); the right wing was measured in each case and the bill from cere to tip. The birds were also examined for state of moult as the stress involved may alter susceptibility. The notation used below for feather growth is that of Cornwallis and Smith (1963) (i.e. O signifies an old feather, 1 to 4 stages of growth in ascending order and N a new feather). Both the primaries and secondaries are numbered from the outermost to the innermost, the right wing only being given. The rectrices are numbered dorsally from left to right. On dissection, the liver and in some cases also the brain and breast muscle were removed for analysis of organochlorine insecticide residues. The methods used and the analysts involved are given in the tables. Extractions were carried out by shaking with hexane and cleanup was effected by DMF partition and alumina column chromatography, as described by de Faubert Maunder et al. (1964b). Wherever possible, extracts were examined by gasliquid chromatography with an electron capture detector, following the method of Goodwin et al. (1961) as detailed by de Faubert Maunder et al. (1964a). Residues 5

3 S O cj U U U U U 'S M J 11 _) J J uj ü O O 3 s ts i a l s «js ^o < o o o 0 0 S 0 ^s ü ü ü e> o z w I^ 60 8 & H.5 Q "a Z *> h Vi s g a * s 0 w W * w H I I I S i l 1 «S< s o & < 4 2 jj g" i ix B d 1 s 111 «" o dg 111 l TS "O SM N^Th O M H i, 1 " T "* 1 i JS» 38 o 2 v2 S o «d «o d M d d 0 ~ ' ' ' O C 3 "* «. <.3 C C > 'C rt.jj *o M000 wc^oo q ^ M v O c\ N *? ^ T rpc^l 'ü (T\NM SO*T\N ** «Ä M d M N Ös h h 3^ S 'i «Hu"" W Nfrvrtoooor q q o «^ rr» q. rtcuu h* NMt3 r^mm d «A d ^ d r~ d O ^ M 3 J v 1 rtn 1^ vo * * u " ö C.3 * ö <u v ju o u ««««'S» 'S 3 e a a a Öfcr.S2» H Ü «u e v> H C «h *i!ri h G J g j PQ W ii cq ffi UPQCQ J J 11 hioqm CO M 3 <y ü 1) ü <U u 3 K C J C C G C ^ s? " *1 3rt "C 'G 'C 'u "G C L C H G U u u u *< r / V ««4J U U Ü U h1 ^J fr fr^oifr M. r T" S o M 3 i Sl ' N ^<

4 BRITISH BIRDS determined by gasliquid chromatography were confirmed by paper chromatography and/or thin layer chromatography. Certain analyses were carried out by paper chromatography only, using the procedure described by Evans (1962). FALCONS EXAMINED Specimen 330: Falco biarmicus Biological data. Female; immature; body weight unknown owing to prior veterinary examination, but Woodford (i960) gave the flying weights of the female Lanner as 1 lb. 8 oz. (680 grams) to 2 lb. (907 grams), which is slightly lighter than his figures for the female Peregrine, 1 lb (879 grams) to 2 lb. 2 oz. (964 grams); wing 358 mm.; tail 210 mm.; bill 22 mm.; tarsus 51 mm. State of moult: 1st primary 4, 2nd8th O, 9th! ith N; secondaries N; coverts, extensive moult in progress; tail O; body, extensive moult in progress. History. Taken as a nestling in the Kisumu or Kisii district of Kenya on 21st October Trained for falconry by W. G. Fiske of Saffron Walden, Essex. In December 1963, when it had nearly completed its first moult (having been in moult about six weeks), it went off its food. Force feeding was tried in the final period and, although the bird felt thin, the weight loss was not great. It died later in the month. The body, together with that of Specimen 331, was first sent to Dr. A. R. Jennings of the School of Veterinary Medicine, University of Cambridge, for postmortem examination. He concluded that 'with regard to the two Lanners, neither of these birds showed any evidence of disease. There were no gross lesions indicative of virus, bacterial or parasitic infections.' Because of these negative findings the carcases were sent on to the Nature Conservancy for chemical analysis. The analyses of the breast muscle, liver and brain showed considerable quantities of dieldrin and heptachlor epoxide; isomers of BHC and pp'dde were also present (table 1). Since they came to England the Lanners had been fed on Pheasant Pbasianus colchicus, Hare Lepus europaeus, Mallard Anas platyrhynchos, Moorhen Gallinula chloropus and Woodpigeon Columba palumbus. During December the diet was restricted to Mallard and Moorhen. The food was always gutted, but otherwise muscle, liver, fat and brain were all available and eaten, the birds being fed to repletion. Specimen 331: Falco biarmicus Biological data. Male; immature; body weight unknown owing to prior veterinary examination, but Woodford (i960) gave the flying weight of the male Lanner as 15 oz. (425 grams) to 1 lb. 4 oz. (567 grams), which is lighter than his weights for the male Peregrine, 1 lb. 4 oz. (567 grams) 52

5 POSTMORTEMS OF FALCONS to ilb. 7 oz. (652 grams); wing 307 mm.; tail 180 mm. (in moult); bill 19mm.; tarsus 50 mm. State of moult: 1st primary N, 2nd 2, 3rd}, 4th5th N, 6th8th O, cjthioth N, 1 ith 3; ist8th secondaries N, 9thioth 2, iithi2th O; coverts, not moulted; tail, 5th and 8th N, 4th and 9th 4, 3rd and 10th 3, 1st and 12th 2, 2nd and nth 1, 6th and 7th O; body, extensive moult in progress. The unusual moult may have been a result of being kept in captivity. History. The same as Specimen 330, except that it died two to three weeks earlier. Three other falcons were in Mr. Fiske's mews at the time of the death of the Lanners, though they were kept in buildings separated by 200 yards. These were two Peregrine, a male and a female, and a female Gyr Falcon Falco rusticolus. All were fed on the same diet as the Lanners. The female Peregrine, a young bird in 1963, fell ill at the same time as the Lanners and died shortly after them. Unfortunately it was not analysed for residues, but Dr. Jennings's examination showed that it 'had a very severe infection with Polymorphs boschadis. This is a nematode worm, normally parasitic in water birds, which causes very severe anaemia and emaciation.' Dr. Jennings expressed the opinion that this parasite was the immediate cause of death (but suggested that there was the possibility of chronic poisoning by insecticides as well). The male Peregrine and the Gyr Falcon, both three to four years old at the time, also fell ill during the same period. The Peregrine became very thin and the colour of its feet went pale before it started eating normally. Both of these birds later recovered, though the Peregrine moulted badly. Thus, of the five falcons present, the three young ones died and the two older ones recovered. Specimen 144: Falco peregrinus Biological data. Male; adult; body weight and measurements unknown. History. Found dead on the ledge beside an eyrie on Lundy in the Bristol Channel on 4th June It was discovered by Michael Jones, then Warden of Lundy Field Society, and sent by A. P. Harman to the Nature Conservancy for analysis. The bird was presumed to be the male of a pair from this breeding haunt where no young have been reared since at least i960. On analysis it was found to contain considerable quantities of dieldrin, heptachlor epoxide and pp'dde (table 1). There is a possibility that these levels are artificially high as the body was rather dehydrated. Specimen 581: Falco peregrinus Biological data. Female; adult; body weight 714 grams; wing 340 mm.; tail 162 mm., bill 25 mm.; tarsus 51mm. State of moult: ist5th primaries 0,6th 4,7th! ith N; ist3rd secondaries N, 4th 2,5th6th N, 53

6 BRITISH BIRDS 7th 4, 8th12th O; coverts, four most distal feathers N, rest O; tail, 6th and 7th N, 5th and 8th 2, ist4th and 9thi2th O; body, moult in progress over most parts. History. Picked up on a road in a remote deer forest, apparently unharmed, near Alladale Lodge, central Ross, on 29th August Dr. James Robertson Justice of Spinningdale, Sutherland, who collected it, noted that it showed an inclination to feed but was unable to swallow. It died on the following day, the final collapse being very sudden. A considerable amount of greenishgrey mucus flowed from its beak and nares immediately after death. The body was sent to J. W. Macdonald, of the Veterinary Laboratory of the Ministry of Agriculture, Fisheries and Food, at Lasswade, Midlothian, for examination. He reported that it 'was in poor condition. There was ulceration of the lining membrane of the thoracic portion of the gullet which had perforated to produce pericarditis. Cultural examination of the heart wall showed the presence of the organism Escherichia coli. Although at the time of examination no foreign body could be detected, the ulceration of the oesophagus could be associated with an injury, e.g. by a sharp piece of bone. There were a few large roundworms in the abdominal air sacs.' These were later found to be Serratospiculum sp., probably S. tendo. After postmortem examination the body was sent to the Nature Conservancy for analysis for organochlorine insecticides (table 1). On examination the plumage was found to be in good condition. There was no evidence of severe damage such as may be caused by a bird thrashing about on the ground. The preserved skin is at Monks Wood Experimental Station. Specimen 592: Falco peregrinus biological data. Male; immature; body weight (383 grams); wing 264mm.; tail 144mm.; bill 19mm.; tarsus 50mm. State of moult not known. (From information supplied by J. B. Murray of the Royal Scottish Museum as the skin was not examined by us.) History. Found by C. D. Haddow of Broughton, Biggar, Lanarkshire, on 4th September It was caught up in a hedge and was wearing a leather strap and bells on its leg. It was placed in an outhouse where it took a few pieces of sheep's liver and a very small amount of grouse breast muscle. However, it was dead by 10 a.m. the following day. Mr. Haddow informed us that when alive it 'was quite frisky... but it was very thin and light'. Also that 'several people in this district had seen it and heard the bells during the fortnight prior to our finding the bird'. George Waterston of the Royal Society for the Protection of Birds, Edinburgh, asked the Royal Scottish Museum to send us the body for analysis. The results (table 1) show a relatively small quantity of 54

7 POSTMORTEMS OF FALCONS dieldrin in the liver. Our postmortem examination confirmed the finder's opinion that the bird was light. No fat could be found and the weight of the breast muscles (both pectoralis major and supracoracoideus muscles of right and left sides) was only 10.7% of the total body weight. This is much lower than that'of Specimen 712 below. The gizzard contained only a small quantity of coarse fur and one nematode. Nine nematodes were found in the gut. There was no sign of injury. Specimen 712: Falco peregrinus Biological data. Female; adult; body weight grams; wing 3 5 o mm.; tail 162 mm.; bill 23 mm.; tarsus 50 mm. State of moult: wings, tail and body showed no signs of moult; plumage generally in good condition with little abrasion at the tips of the primaries and tail feathers. History. Found by T. J. Brenton of Trevarrian, near Newquay, Cornwall, on 17th March It was lying dead 'in an open clifftop field about 30 yards from the cliff edge'. Mr. Brenton noted that the area has 'high sheer cliffs with plenty of wild pigeons'. We received the body in fair condition from the Royal Society for the Protection of Birds. Our examination showed that the feathers had apparently been chafed off the projecting humerus/ulna joint, particularly on the upper surface of the wing, leaving exposed skin. The head and mantle had a similar appearance. The right foot and distal joints of its toes were discoloured blue and brown, the toes being stiff and dry. This was in contrast to the left foot which was the usual dull yellow with the toes still soft and supple. When the body was skinned, numerous small contusions were found. Internal examination showed a number of air sac worms apparently lying in the body cavity between the heart and the liver; also a considerable number of amorphous yellow nodules were found on and under the peritoneum. Both nematodes and nodules were sent to J. W. Macdonald for further examination. The air sac worms were later identified as Serratospiculum sp., probably S. tenth (similar to those in Specimen 581), and Mr. Macdonald informed us that he is sure that the severe damage done by these worms interferes with a bird's general health, especially when the heart sac (pericardium) is involved. Microscopic examination of the yellow nodules showed only amorphous material and it was not possible to give an opinion on their nature. The gizzard was found to be empty except for two stems of grass. The preserved skin is now at Monks Wood Experimental Station. Specimen A: Falco peregrinus We are indebted to J. Koeman of Utrecht University for the use of the analysis figures for this specimen (/. Appl. Ecol., in press). The bird 55

8 BRITISH BIRDS Table a. Organochlorine residues in organs of birds of the Residues are expressed in parts per million. Analysts are detail gasliquid chromatography, and PC for paper chromatography. No. of Cause of samples Species Dates obtained death analysed Tissu Mallard Anas platyrhynchos Nov 1963; Mar, Jun shot and 1 unknown Mean of 3 1 Liver Fat Moorhen Gallinula chhropus Aug, Sep, Nov 1962; Mar (3) 1963; Apr road deaths and 2 unknown Mean of 6 Mean of 6 Mean of 2 Liver Breast n Fat Pheasant Pbasianus colchicus Jun 1963 Road death 1 1 Liver Breast n Woodpigeon Columba palumbus Group 1 Jul, Sep (2), Oct 1962; Most found Mean of 3 Liver Jan (2) 1963 dead Mean of 6 Breast 1 Group 2< (b) Jan 1964 Found unable 1 Liver to fly 1 Breast 1 (c, f) Feb (2) 1964 Road death Mean of 2 Liver and found dead Mean of 2 Breast 1 was in captivity at Amersfoort, Netherlands, and died in convulsions in February It was submitted to parasitological and pathological examination, but these were negative. The insecticide content proved to be large (table 1). FOOD SPECIES Birds of the same species as those used by Mr. Fiske to feed his falcons (page 5 2) have been analysed (table 2). The sample available consisted of three Mallards, seven Moorhens, one Pheasant and nine Woodpigeons. The majority were collected in southeast England during and were shot, road casualties or found dead. All three Mallards and the single Pheasant contained very small residues. Only two of the Moorhens possessed detectable residues. The Woodpigeons fell into two groups: six had very small or no residues present in contrast to the other three (b, c and f) which all had high residues. One of the latter (b) was still alive when found, but unable to walk or fly. Mr. Fiske also used a small amount of Hare to feed his falcons. Unfortunately there are no data available on the usual contamination 56

9 POSTMORTEMS OF FALCONS species as those used as food for the Lanners Fako biarmkus in table I ACKNOWLEDGEMENTS on pages GLC is an abbreviation for last three Woodpigeons are referred to in the text by the letters b, c and f Other Heptachlor Gamma BHC pp'dde pp'tde Dieldrin epoxide BHC isomers pp'ddt Endrin Analyst Methoi <I.J 0.01 Shell Shell GLC GLC Nat Cons PC GovChem GLC Nat Cons PC Nat Cons PC o O.I <o.05 Shell Shell GLC GLC Nat Cons Nat Cons PC PC ? <0.2 Nat Cons Nat Cons PC PC O.4O O.OI Nat Cons Nat Cons GLC/P< GLC/P< of this mammal. However, it is unlikely to be any more contaminated than the bird species involved and probably has even lower residues. The residues in experimentally fed mammals are not as great as those in experimentally fed birds. Dale et al. (1962) found that the brains of laboratory rats Rattus sp. which had been given 200 parts per million of pp'ddt in their diet for 90 days contained 6 to 21 p.p.m. (mean 9 p.p.m.) of pp'ddt and no pp'dde. Bernard (1963), on the other hand, after including 200 p.p.m. of DDT in the diet of House Sparrows for 23 to 49 days, found a brain residue of DDT and metabolites amounting to 58 to 200 p.p.m. (mean 129 p.p.m.). ORGAN WEIGHTS As Peregrine 712 had not been examined before our dissection, we removed the organs whole, weighed them and calculated the percentage of total body weight. This allows us to calculate the total pesticide content of a particular organ. The weights and percentages were: breast muscles (both pectoralis major and supracoracoideus muscles of left and right sides), grams (17.5%); liver, grams (3.1%); 57

10 BRITISH BIRDS kidneys, 6.74 grams (0.9%); heart, 9.34 grams (1.2%). These percentages may be low owing to dehydration before examination. If the relationship of organ weights to total body weight is similar in the Peregrine and the Lanner, these percentages can be used to calculate the organ weights of the Lanners for which we were unable to get measurements. In a male Lanner of 496 grams (the mean of the weights given by Woodford i960) the liver would weigh 15 grams and the total breast muscle 87 grams. The organ weights of one Woodpigeon (b) were also measured soon after death. They were breast muscle grams and liver grams. DISCUSSION The presence of considerable residues of organochlorine insecticides and the negative findings of the veterinary examinations make it likely that the two Lanners died of insecticidal poisoning. The fact that two of Mr. Fiske's falcons lived whilst three died does not necessarily invalidate this conclusion. Assuming all five had ingested similar quantities of insecticides, the older ones could have survived because of their greater resistance (DeWitt etal. i960 showed that the sensitivity of Pheasants tended to decrease with age). Their subsequent recovery is in accord with published findings (Ash and Taylor 1963, Bernard 1963) that toxic residues can be eliminated if the birds are changed to an insecticidefree diet. The oneyearold Lanners also had additional stresses imposed by moulting and the young Peregrine by parasites. Of the insecticide residues in the Lanners (table 1), the dieldrin and heptachlor epoxide are by far the most toxic. DeWitt et al. (i960) made comparative tests of the toxicity of 21 insecticides to Bobwhite Quail Colinus virginianus. They found the lethal dose to 50% of the subjects to be 35 milligrams per kilogram for dieldrin, 125 mg./kg. for heptachlor, 200 mg./kg. for gamma BHC and 500 mg./kg. for DDT. Thus dieldrin is respectively about four, six and 14 times more toxic than heptachlor, gamma BHC and DDT. There are no published data on the toxicity of DDE to birds. However, von Oettingen and Sharpless (1946) found it to have onethird of the oral toxicity of DDT to mice. Thus it is probably of little importance in birds when compared with dieldrin. Combining the two most toxic substances, dieldrin and heptachlor epoxide, we see that the amount of the combination present in the liver when death occurred was p.p.m. (dieldrin p.p.m.). The corresponding amount in the breast muscle was p.p.m. (dieldrin p.p.m.). Comparing the organ contents of the wild Peregrines with the above Lanners, we see that Peregrine 144, found dead beside its eyrie, contained a combined residue of dieldrin and heptachlor epoxide of 5.5 p.p.m.; this is in the same range as the captive Lanners. Peregrine

11 POSTMORTEMS OF FALCONS also comes into the same category with a combined content of 5.2 p.p.m.; there is some support for the view that insecticides killed this bird as signs of damage to the body and plumage suggested the typical convulsions with it lying on its back. Peregrine 581 almost certainly died from pericarditis and the ulceration of the oesophagus which would make it difficult for it to feed; the combined residue was very low at 0.8 p.p.m. Peregrine 592 had obviously been taken, probably as a nestling, for falconry; its light condition indicated starvation, either through an inability to catch sufficient food or through being caught up by its jesses; again the combined residue was low at 2.0 p.p.m. Peregrine A almost certainly died of toxic chemical poisoning: the typical convulsions occurred and a veterinary examination could establish no other cause of death; the combined liver residue was high at 9.3 p.p.m. Thus in those cases where there was good presumptive evidence for another cause of death the residues were low, but where the cause of death was otherwise inexplicable the residues were high. Poisoning in the latter birds (i.e. 144, 712 and A) may be logically suspected. We have, therefore, an indication that the quantities of dieldrin and heptachlor epoxide in the livers of large falcons whose deaths may be correlated with apparent insecticidal poisoning lie in the range p.p.m. (dieldrin p.p.m.); the corresponding amounts in the breast muscles are p.p.m. (dieldrin p.p.m.). Peregrines 581 and 592 show that a liver content of p.p.m. dieldrin and heptachlor epoxide (dieldrin p.p.m.) may be carried by living individuals or ones dying from causes other than poisoning by insecticides. It is possible that the mean lethal liver content is higher than the 6.6 p.p.m. shown by the above results and closer to the 9.3 p.p.m. of Peregrine A. First, there is the additional effect of the pp'dde (see below) and isomers of BHC present. Secondly, Peregrines 144 and 712 and Lanners 330 and 331 were under stresses of various kinds: Peregrine 144 was attempting breeding, 712 had a high parasitic load and both Lanners were in moult. This may have increased their susceptibility to toxic chemicals. There is also the indication that young birds are more susceptible than old ones. The high pp'dde contents in the livers of Peregrines 144 and 712 have been ignored in the above analysis as it is very likely that this material was ingested as pp'dde (i.e. detoxication of pp'ddt to pp'dde had occurred before the contaminated food was eaten). If pp'ddt had been ingested one would expect at least a small amount of pp'ddt or pp'tde to have been present in the liver at death (Jefferies and Walker in press). According to the published data (von Oettingen and Sharpless 1946, DeWitt et al. 1960), 70 p.p.m. DDE can only be equivalent to 12 p.p.m. dieldrin. This is supported by the 59

12 BRITISH BIRDS finding that 59.7 p.p.m. pp'dde plus 69.2 p.p.m. pp'ddt in the liver of a Bengalese Finch Lonchura striata not only did not kill the bird but did not prevent it from breeding successfully (D. J. Jefferies, unpublished). The work of Turtle et al. (1963) enables a comparison of the indicated susceptibility of the Peregrine to be made with that of its main prey species, the feral pigeon Columba livia (Ratcliffe 1963 stated that the feral pigeon forms 46% by weight of the Peregrine's diet in England, Wales and southern Scotland and 29% by weight in all British regions). Pigeons dying after being fed experimentally with dieldrin contained p.p.m. in the breast muscle; those surviving contained p.p.m. at sacrifice. Those dying after being fed with aldrin and heptachlor contained respectively p.p.m. (as the metabolite dieldrin) and p.p.m. (as the metabolite heptachlor epoxide) in the breast muscle. Thus we see that the large falcons are probably some four times more sensitive to organochlorine insecticides than these pigeons. In the case of the Lanners the food species ingested were known and thus an idea of the rate of organochlorine intake may be estimated and compared with the content of the falcons. The insecticides present dieldrin, heptachlor and gamma BHC are most likely to have come from the commonly used cereal seed dressings via the four bird species used as food, i.e. Mallard, Moorhen, Pheasant and Woodpigeon. Analysis of a sample of twenty specimens of these four species obtained mainly in southeast England during (table 2) showed that in most cases the organochlorine content was very low. The Moorhens and most of the Woodpigeons were found to contain no dieldrin or heptachlor epoxide in the liver or breast muscle. Both the Mallards and the Pheasant had small residues of dieldrin in the liver, but there was none in the breast muscle of the Pheasant. Three of the Woodpigeons, however, contained organochlorines in amounts vastly greater (800 times) than that which may be taken as the normal background level for these four species. Ignoring these three birds at present, one can calculate the dose level of dieldrin and heptachlor fed to the Lanners, assuming they were given equal weights of the four bird species containing the normal background contamination. This level is found to be 0.01 micrograms (jug) per gram of liver and none in the breast muscle. This must only be considered an approximation, however, as some inaccuracies will arise from the unsatisfactory but unavoidable combination of paper chromatography and gasliquid chromatography results, paper chromatography being less sensitive. We have already noted that a male Lanner weighing 496 grams would have a total breast muscle of 87 grams and a liver of 15 grams. 60

13 POSTMORTEMS OF FALCONS If one takes these as being the organ weights of the male Lanner 331 and uses the residues from table 1, one can calculate that a total of 335 I^S f dieldrin and 73 /xg of heptachlor epoxide (408 /xg in all) were present in the breast muscle plus liver. As the age of Lanner 331 is known (420 days), one can calculate the dose level of dieldrin and heptachlor in the food that this represents, assuming a complete accumulation of every /xg ingested. Woodford (i960) noted that 'the daily ration for a Peregrine falcon will be about 5 oz. and for a tiercel rather under 4 oz.' As a male Lanner is smaller than both, a daily consumption of 3 J oz. (99.22 grams) is probable. Thus food eaten at the rate of grams per day for 420 days would have to be contaminated to an extent of 0.01 /xg per gram (p.p.m.) to produce the residue level in the Lanner under the above conditions. However, as normal background contamination of the usual food amounted to only 0.01 p.p.m. dieldrin in the liver and o p.p.m. in the breast muscle, we can see that a lethal residue of dieldrin could accumulate only if (a) the bird were fed completely on liver (b) all the insecticide accumulated were concentrated in the liver and breast muscle of the falcon and (c) there were complete assimilation of every /xg of dieldrin ingested. These conditions make it improbable that the residue found arose from the normal background contamination of the food since (a) falcons are fed mainly on breast muscle (b) the liver plus breast muscle contents represent only a fraction, perhaps a half or twothirds, of the total insecticide content of the Lanner and (c) it is very unlikely that every /xg of insecticide ingested will be stored in the bird(stickel eta/ showed that only 16.3% to 20.0% of the heptachlor consumed via contaminated earthworms was absorbed by American Woodcock Philohela minor). The most likely way, therefore, in which the lethal concentrations present could have been accumulated is by the consumption of a few highly contaminated birds such as the three Woodpigeons (b, c and f) containing levels 800 times more than the background (two of these were still alive at the time of being taken). Using the organ weights detailed above, it may be calculated that the first of these Woodpigeons (b) contained a total of 1,273 MS f dieldrin in the breast muscle (1,126 /xg) and liver (147 /xg). Even allowing that only 20% of the dieldrin is absorbed by the falcon, the liver and breast muscle content of Lanner 331 could have been absorbed by consuming the breast muscle of only two such pigeons. Assuming that these organs held twothirds to a half of the total content of the falcon, three or four such heavily contaminated pigeons could prove lethal (Turtle et al showed that feral pigeons may accumulate as much as 13.5 p.p.m. of dieldrin in the breast muscle and still survive, so it is possible that even these small numbers could be further reduced). 61

14 BRITISH BIRDS If these remarks are extrapolated to cover wild Peregrines, one mayspeculate that it was not so much a slow accumulation of toxic chemicals which produced the initial decrease in the British population, but a rapid buildup causing the death of a large number of individual Peregrines during the period when dressed seed was available to pigeons (Murton and Vizoso 1963 showed that Woodpigeons can pick up an L.D.50 dose of dieldrin from dressed grain in less than five hours of feeding). It is possible that the effects of toxic chemicals are likely to be at their most obvious in a small population of a slow breeding species, such as the Peregrine, which is sensitive to small organochlorine residues and whose main prey species, the feral pigeon, is most resistant. This situation is probably made worse by the Peregrine taking the weaker and probably more heavily contaminated birds from out of the flock (Eutermoser 1961, Saar 1961). Similar results have been found with the Fox Vulpes vulpes, many of which died during i960 and 1961, apparently from insecticide poisoning. Blackmore (1963) showed that the Fox is extremely sensitive to dieldrin, noting that insecticide poisoning can be suspected if more than 1 p.p.m. of dieldrin and more than 4 p.p.m. of heptachlor epoxide are found in the flesh. He attributed the deaths to Foxes eating the carcases of Woodpigeons which had died after feeding on dressed cereal seeds (deaths occurred in experimental Foxes after consumption of three to six wild Woodpigeons found dead in the field). Ratcliffe (1963) also showed that, as well as a 40% decline in the Peregrine population by 1961, only onethird of the survivors were breeding successfully. Thus there is also the possibility that sublethal residues, obtained from prey possessing low residues or from one or two prey with high residues, may also be affecting the population. (Some evidence that sublethal amounts of organochlorines can affect breeding success has already been shown for other species DeWitt 1956, Post 1951; and Jefferies, work in progress.) Thus, if these sublethal residues did not, as has been suggested, cause the initial sudden decline in numbers, they could delay a recovery in the population. These conclusions are unfortunately based on limited information, but the Peregrine is a bird of remote places and only very rarely are bodies obtained in a condition to allow detailed veterinary and chemical examinations. ACKNOWLEDGEMENTS We should like to thank all those people who helped to obtain the specimens in particular W. G. Fiske who also went to considerable lengths to provide details of the history of his birds. We are also grateful to Dr. A. R. Jennings and J. W. Macdonald, specialists in avian diseases; and to H. Egan and J. O'G. Tatton of the Laboratory 62

15 POSTMORTEMS OF FALCONS of the Government Chemist, A. Richardson of the Shell Chemical Company, J. Koeman of Utrecht and C, H. Walker of the Nature Conservancy, the analysts concerned, for allowing us to use their unpublished data. Dr. D. A. Ratcliffe, Dr. N. W. Moore, R. Wagstaffe and C. H. Walker read the manuscript and provided valuable comment. SUMMARY An examination was made of the results available to date from analyses of a small number of wild Peregrines Falco peregrinus and some trained Peregrines and Lanners F. biarmicus. Three died in circumstances making it probable that organochlorine insecticides were responsible, two others from other known causes and two more from unknown causes. The residues present in those dying from other known causes was very much lower than in all the rest. It was concluded that all but these two may have died from organochlorine poisoning probably from the effects of the combined residues of dieldrin and heptachlor epoxide, the two most toxic present. If this is correct, the lethal range is indicated by a residue of parts per million (p.p.m.) in the liver. An examination of the residues in wild individuals of the bird species fed to two trained Lanners considered to have died from organochlorine poisoning showed most to contain extremely small residues. However, a few Woodpigeons Columba palwnbus contained very high levels, A theoretical calculation suggests that lethal residues could be obtained by the falcons ingesting a few highly contaminated prey rather than a large number of prey with small residues. Using figures available from toxicological experiments on feral pigeons C. livia (the principal diet of wild Peregrines), it appears that death could result from eating only three or four heavily contaminated birds. If this is correct, the sudden decline of the British Peregrine population might be explained to a large extent by individual falcons having taken a few pigeons which contained high residues, probably as a result of feeding on seed corn treated with organochlorines. REFERENCES ASH, J. S., and TAYLOR, A. (1963): 'Trials to measure the effects of a normal mercury/ gamma BHC seeddressing on breeding Pheasants: interim report'. Game Research Ass, Ann. Rep., 1963: BERNARD, R. F. (1963): 'Studies on the effects of DDT on birds'. Publications of the Museum, Michigan State University Biological Series, 2: BLACKMORE, D. K. (1963): 'The toxicity of some chlorinated hydrocarbon insecticides to British wild Foxes {Vulpes vulpes)'. J. Comp, Path., 73: CORNWAIXIS, R. K., and SMITH, A. E. (1963): The Bird in the Hand. Oxford, p. 35. DALE, W. E., GAINES, T. B., and HAYES, W. J. (1962): 'Storage and excretion of DDT in starved Rats'. Toxic. Appl. Pharmac, 4: DE FAUBERT MAUNDER, M. J., EGAN, H., and ROBURN, J. (1964a): 'Some practical aspects of the determination of chlorinated pesticides by electroncapture gas chromatography. Analyst, 89: DE FAUBERT MAUNDER, M. J., EGAN, H., GODLY, E. W., HAMMOND, E. W., ROBURN, J., and THOMSON, J. (1964b): 'Cleanup of animal fats and dairy products for the analysis of chlorinated pesticide residues'. Analyst, 89: DEWITT, J. B. (1956): 'Chronic toxicity to quail and pheasants of some chlorinated insecticides.' /. Agric. FoodChem., 4:

16 BRITISH BIRDS DEWITT, J. B., MENZIE, C. M., ADOMAITIS, V. A., and REICHEL, W. L. (i960): 'Pesticidal residues in animal tissues'. Trans. Twentyfifth North Amer. Wildlife Conf., EUTERMOSER, G. (1961): 'Erlauterungen zur Krahenstatistik'. Deutscher Falkenorden, 6: EVANS, W. H. (1962): 'The paperchromatographic separation and determination of chlorinated insecticide residues'. Analyst, 87: GOODWIN, E. S., GOULDEN, R., and REYNOLDS, J. G. (1961): 'Rapid identification and determination of residues of chlorinated pesticides in crops by gasliquid chromatography'. Analyst, 86: JEFFERIES, D. J., and WALKER, C. H. (in press): 'The uptake of pp'ddt and its postmortem breakdown in the avian liver'. MOORE, N. W., and RATCLIFFE, D. A. (1962): 'Chlorinated hydrocarbon residues in the egg of a Peregrine Falcon {Falco peregrinus) from Perthshire'. Bird Study, 9: MURTON, R. K., and Vizoso, M. (1963): 'Dressed cereal seed as a hazard to Woodpigeons'. Ann. Appl.BioL, 52: POST, G. (1951): 'A study of aldrin insecticide, its effect on birds and other wildlife' Wyoming WildLife, 15: RATCLIFFE, D. A. (1963): 'The status of the Peregrine in Great Britain'. Bird Study 10: (1965): 'The Peregrine situation in Great Britain '. Bird Study, 12: SAAR, C. (1961): 'Der Krahenfalke "Mara" '. Deutscher Falkenorden, 6: STICKEL, W. H., HAYNE, D. W., and STICKEL, L. F. (1965): 'Effects of heptachlorcontaminated earthworms on Woodcocks'. /. Wildlife Management, 29 (1): TURTLE, E. E., TAYLOR, A., WRIGHT, E. N., THEARLE, R. J. P., EGAN, H., EVANS, W. H., and SOUTAR, N. M. (1963): 'The effects on birds of certain chlorinated insecticides used as seed dressings'. /. Sci. Fd. Agric, 14: VON OETTINGEN, W. F., and SHARPLESS, N. E. (1946): 'The toxicity and toxic manifestations of 2,2Bis(pchlorophenyl)i,i,itrichloroethane (DDT) as influenced by chemical changes in the molecule. A contribution to the relation between chemical constitution and toxicological action'. J. Pharmacol., 88 (4): WITHERBY, H. F., JOURDAIN, F. C. R., TICEHURST, N. F., and TUCKER, B. W. (1938): The Handbook of British Birds. London, vol. 1, p. xxxiv. WOODFORD, M. H. (i960): A Manual of Falconry. London, pp. 127, 188,

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