Ecotoxicology 1, 31-44 (1992)
Mortality from the pesticides aldrin and dieldrin in British Sparrowhawks and Kestrels I. N E W T O N * , I. W Y L L I E a n d A. A S H E R
Institute of TerrestrialEcology, Monks Wood Experimental Station, Abbots Ripton, Huntingdon, PE17 2LS, UK Received 27 February 1992; accepted 31 March 1992 Among 1029 dead Sparrowhawks and 1055 dead Kestrels from various parts of Britain that were examined over the period 1963-90, the main causes of death were (a) collisions of various kinds (b) starvation or disease and (c) organochlorine poisoning. The main chemical which caused poisoning was HEOD, derived from the insecticides aldrin and dieldrin. Other deaths were attributed to poisoning by DDE (the main metabolite of the insecticide DDT) and by HE (heptachlor epoxide, derived from the insecticide heptachlor). Sparrowhawks whose deaths were attributed to HEOD poisoning contained 5-85 ¢tg g-1 HEOD in their livers (wet weight), while Kestrels contained 6-99 ¢tg g-1 HEOD. Such birds were typically lighter in weight than collision victims, but heavier than starved or diseased birds. In the period 1963-75, HEOD probably accounted for about 50% of all recorded Sparrowhawk deaths and 39% of all recorded Kestrel deaths in eastern arable districts, but a smaller proportion elsewhere. Geographical variation in the proportion of deaths attributed to HEOD paralleled variation in the proportion of land devoted to arable crops on which aldrin and dieldrin were mainly used. It also paralleled variation in the extent of population decline in these species. Moreover, the proportion of deaths attributed to HEOD declined between 1963-75 and 1976-86, following a marked reduction in aldrin-dieldrin use, and fell to nil in 1987-90, when aldrin and dieldrin were withdrawn altogether. Over this period, the populations of both species recovered from a decline which occurred in the late 1950s, when aldrin-dieldrin were first introduced.
Keywords: Accipter nisus; aldrin; dieldrin; Falco tinnunculus; heptachlor; kestrel; mortality; pesticide; sparrowhawk Introduction In this paper we examine the incidence of aldrin-dieldrin poisoning in British Sparrowhawks, Accipiter nisus, and Kestrels, Falco tinnunculus, during the period 1963-90. The paper is based on necropsies and chemical analyses of birds found dead and sent for examination to Monks Wood Experimental Station. The findings form part of the evidence implicating organochlorine pesticides in the population changes of these and other raptors which have occurred in the past forty years. Following the introduction of organochlorines, the numbers of Sparrowhawks, Kestrels and other raptors in Britain declined in the late 1950s, only to recover again following successive reductions in the use of organochlorines which occurred d u r i n g 1963-86 (Ratcliffe, 1980; Newton, 1986; Newton and WyUie, 1992). Similar changes in raptor populations occurred elsewhere in Europe and in North America (Newton, 1979; Opdam et al., 1987; Cade et al., 1988). *To whom correspondence should be addressed. 0960-9292 © 1992 Chapman & Hall
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Decline in the Sparrowhawk population was evident over almost the whole of Britain, but was most marked in eastern regions, where the proportion of arable land, and associated pesticide use, was greatest (Newton and Haas, 1984). Decline in the Kestrel population was much less marked and mainly restricted to eastern arable areas. Two types of chemicals were implicated in these declines: cyclodienes (notably aldrin and dieldrin), which are highly toxic and poison birds directly, thus increasing mortality above the natural level; and DDT-derivatives (notably DDE), which are much less toxic to birds but at sublethal levels can cause eggshell-thinning and egg-breakage, thus reducing the breeding rate. Only at much higher levels (see later) do DDT-type chemicals cause direct mortality. Although both these mechanisms, of enhanced mortality and depressed reproduction, are thought to have contributed to population declines in British raptors, changes in mortality from aldrin-dieldrin use seem to have played the major role (Newton, 1986; Nisbet, 1988). The same may not be true in other countries, however, where usage patterns differed (Risebrough and Peakall, 1988). In Britain, aldrin and dieldrin were used mainly as seed-treatments to protect cereal grains and other seeds against insect attack. At times of sowing, in autumn or spring, such seeds were often eaten by birds and rodents, from which they reached various predators, including Sparrowhawks and Kestrels. The two chemicals were most widely used during 1956-62, after which (because of large-scale spring mortality of seed-eating birds) they were restricted to use on autumn-sown grain. Then, from 1976, they were totally withdrawn from use on cereals and remained only for relatively minor uses, before being banned altogether by statutory control from 1986. The residue monitoring programme, on which this paper is based, was started in 1963 after the peak period of aldrin-dieldrin use, and has continued to the present, during a period of progressively declining use. Some findings from the programme to 1977 were reviewed by Cooke et al. (1982), while trends in mean residues in Sparrowhawks to 1982 were given by Newton and Haas (1984) and in Sparrowhawks and Kestrels to 1990 by Newton et al. (1992). In addition, the necropsy findings from the two species to 1979 were summarized by Newton et al. (1982a). In this paper, we focus on those mortality incidents in the two species that could be attributed to aldrin-dieldrin and examine how such incidents have varied across the country and over the years in relation to changing aldrin-dieldrin use. Materials and methods
The specimens for analysis came from most parts of Britain in response to regular advertisements placed in ornithological magazines and journals asking for birds found dead. All birds were requested, regardless of the cause of death. In the event, most were accident victims, while others appeared to have died of food shortage or disease; only a small proportion seemed to have died of pesticide poisoning (Newton et al., 1982a). On receipt, each carcass was weighed, marked and then stored at - 2 0 °C until it could be examined, up to several months later. For necropsy, the unfrozen carcass was opened up and examined for body condition, any obvious parasites, lesions or other abnormalities. The findings were used, along with information from the sender, to allocate each bird to one of three main categories (following Cooke et al., 1982)), according to whether it had apparently died of: (1) collision, shooting or other trauma; (2) starvation or disease; or (3) pesticide poisoning or other nonobvious causes. Most specimens (93% of Sparrowhawks and 95% of Kestrels) could be allocated to one of these three categories,
Sparrowhawk and Kestrel mortality from pesticides
33
even though within each category the precise cause of death was not always obvious. The remaining ones could not be allocated because only part of the carcass (often the liver only) was received for analysis. These latter birds are omitted from further consideration, leaving a total of 1029 Sparrowhawks and 1085 Kestrels. However, other types of information (for example, body weight or month of death) was also missing from some specimens, leading to variation in the numbers available for different analyses (see Tables 1 and 2, Figs 1-3). Typically, collision casualties had extensive bruising and broken bones, and many were found at roadsides, indicating that they were traffic victims. Shot birds contained lead pellets or had pellet wounds. Assignment of other traumatic mortality causes, such as drowning, was dependent mainly on information from the sender, together with the lack of any conflicting evidence from necropsy. Starved birds were low in weight, with wasted breast muscles, no body fat, no fat on the heart and empty blackish or greenish intestines. Diseased birds were very few in number, but also in poor body condition ("thin") and showed obvious lesions, particularly on liver, kidneys or lungs, or contained large numbers of helminth parasites. The deaths of all or most of the remaining birds could be attributed to pesticide poisoning. Verification of apparent pesticide victims was dependent mainly on chemical analysis (see below), together with the tack of any other obvious mortality cause. Many supposed organochlorine victims also showed signs of haemorrhaging around certain internal organs, including brain, lungs, heart and foregut (Newton et al., 1982a,b). This was quite distinct from the heavier, more superficial and local haemorrhaging found at the point of impact in accident victims. In addition, some apparent pesticide victims were found alive, but reported by the sender to die in spasms, while other birds found dead showed signs of a similar death as their wings and tail were spread or their feet were firmly clenched, clutching grass or leaves. Birds which had died from other obvious causes showed none of these symptoms. After necropsy, a piece of liver was removed from each specimen and analysed for organochlorine residues of D D E and TDE (from the insecticide DDT), H E O D (from the insecticides aldrin and dieldrin) and H E (from the insecticide heptachlor), using gasliquid chromatography. The limit of detection was about 0.01/~g per g wet weight. To achieve consistency over the years, analytical results were continually checked against standards of known concentration (for full analytical procedure, see Newton et al., 1992). All carcasses were sampled, regardless of cause of death, and residues are presented here on a fresh weight basis. Diagnosis of pesticide victims, largely on the basis of residue levels in tissues, was inevitably somewhat arbitrary, as it was based partly on comparative data from other species deliberately dosed to the point of death with the relevant chemicals. The considerable variation in sensitivity, both between and within species, meant that a given level might be lethal to one bird but not to another. Furthermore, because organochlorines accumulate in body fat, when a bird loses weight, residues released from metabolised fat redistribute themselves within the body, rising in concentration in other tissues, such as liver (Jefferies and Davis, 1968; Stickel et al., 1969; Porter and Wiemeyer, 1972; Bogan and Newton, 1977). There is thus an interaction between a bird's nutritional state and the organochlorine levels in different tissues, and it is sometimes difficult to separate starvation from poisoning as the primary cause of death. After considering the available data, Moore (1965) and Cooke et al. (1982) concluded for various birds that a concentration in liver of 10/~g g-* or more of H E O D (in wet weight) or 100 ~g g-1 or more of
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Newton, Wyllie and Asher
DDE could be taken as indicative of lethal organochlorine poisoning, but these figures were intended only as a rough guide. Some specific information on HEOD is available for Kestrels and Sparrowhawks, in that Jefferies found HEOD concentrations of 12/zg g-1 and 19/zg g-1 in the livers of two Kestrels that had been experimentally poisoned with dieldrin (in Prestt et al., 1968), while Koeman et al. (1969) found 16, 24 and 19 pg g-~ of H E O D in the livers of two wild Kestrels and a Sparrowhawk whose deaths were attributed to dieldrin poisoning in the Netherlands. Little information is available for heptachlor, but DeWitt et at. (1960) found 6-20#g g-1 HE in tissues of various birds poisoned by this chemical, and Turtle et at. (1963) found 19-53 pg g-i in the muscle of ten experimentally poisoned pigeons, compared with 5-23 #g g-1 in seven survivors. As mentioned above, organochlorine victims often showed other symptoms, however, such as internal haemorrhaging (Cooke et al., 1982; Keymer et al., 1982; Newton et aI., 1982a,b) and usually died with muscle tremors or convulsions. For examination of geographical variation in apparent organochlorine mortality, the country was divided into four zones, where the proportion of tilled land in 1960 was less than 10%, 11-30%, 31-60% and more than 60%, respectively (see Newton and Haas (1984) for map). The proportion of tilled land was assumed to reflect regional variation in pesticide use. It was lowest in the north and west of the country and highest in the south and east. In all four zones the proportion of tilled land increased slightly during the study, but not sufficiently to warrant redrawing the boundaries of the different zones. Throughout the commonest arable crops were cereals, which occupied about 90% of all tilled land. For examination of temporal variation in apparent organochlorine mortality, the period of study (1963-90) was divided into three sub-periods: 1963-75, when aldrindieldrin were permitted for use on autumn-sown cereals as well as on other minor crops; 1976-86 when aldrin-dieldrin were permitted for use on minor crops only; and 1987-90, when they were banned altogether. The pesticide heptachlor had been fairly widely used on cereals up to 1963 but was then quickly phased out, while DDT was used throughout the period 1963-86 but in progressively decreasing quantities. Results
Of 1029 Sparrowhawks from the period 1963-90, the deaths of 727 (70.7%) were attributed to accidents (including shooting), of 266 (25.9%) to starvation (including disease) and of 36 (3.5%) to organochlorine poisoning (including 25 (2.4%) attributed to HEOD, 10 (0.8%) to DDE/TDE and one (0.1%) to HE). Of 1085 Kestrels from the same period, the deaths of 409 (37.7%) were attributed to accidents, of 563 (51.9%) to starvation and 113 (10.4%) to organochlorine poisoning (including 88 (8.1%) attributed to HEOD, 23 (2.1%) to DDE/TDE and two (0.2%) to HE). The frequency of these three main mortality classes differed significantly between the species (u 2 = 233.9, p < 0.001). Mortality from H E O D In both species, the proportion of apparent HEOD victims varied greatly between the four agricultural zones and also declined over time (Table 1). In the period 1963-75, when aldrin and dieldrin were still widely used on autumn-sown cereals, H E O D victims of both species were received from all four agricultural zones; but they formed a significantly higher proportion of carcasses from the eastern zone (50% of Sparrowhawks
0.001 < 0.05 Cp < 0.01
•pp
250
~
I 'm
~
100
150
~
~
200 Grams
Fig. 3, Body weights of Sparrowhawks and Kestrels whose deaths were attributed to different causes, October-April only.
~
}
3250
40
.Newton, Wyllie and Asher
figures for Kestrels were 160 g for most males and 170 g for most females. In both sexes of both species, birds classed as H E O D victims were generally intermediate in weight between accident and starvation casualties, possibly because most had become immobilized some time before their death.
Mortality from other organochlorines Compared with H E O D , fewer deaths were attributed to DDE. Like deaths from H E O D , however, deaths from D D E were initially widespread but found mostly in the eastern region. Apart from one Sparrowhawk, they were all prior to 1987, when the ban on all organochlorines came into effect. The levels of D D E found in 10 Sparrowhawks whose deaths were attributed to this chemical were in the range 140-251 #g g-l, apart from two with 55 #g g-1 and 40 /~g g-1 which also had 35 and 48 #g g-1 TDE, respectively. These last two birds had only traces of other organochlorines but died of convulsions with internal haemorrhaging typical of organochlorine victims. The equivalent D D E levels in 23 Kestrels were mostly in the range 110-812 ppm, with two outliers at 1474 (1982) and 1500 ppm (1978). The carcasses of both these Kestrels were in good physical condition and were found in an area of intensive fruit-growing (Kent) where D D T use was especially high. The deaths of three birds were attributed to HE, namely two Kestrels with 10 and 15 #g g-l, and one Sparrowhawk with 10 #g g-1. In these birds, residues of all other organochlorines were well below supposed lethal levels. Some birds had supposed lethal levels of more than one chemical. Thus, one Sparrowhawk with 17 #g g-1 H E O D also contained 340 #g g-~ of DDE, while five Kestrels whose deaths were arbitrarily attributed to H E O D also contained 17 and 40 pg g-1 of H E and 110, 150 and 260jzg g-1 of DDE, respectively. In addition, H E levels exceeding 10#g g-1 were found in one Sparrowhawk and one Kestrel which died of collisions, while D D E levels exceeding 100 were found in seven Sparrowhawks and one Kestrel which died of collisions, and in five Sparrowhawks which had apparently starved. Discussion
The carcasses received for analysis probably did not represent a random cross-section of Sparrowhawk or Kestrel deaths but were biased towards those forms of mortality most readily detected by people. This may account for the high proportion of collision victims: many of the Kestrels had been hit by vehicles and were found at roadsides, while many of the Sparrowhawks had collided with windows. Despite this likely bias, however, carcasses were obtained in the same way throughout the study, so that changes in the proportions of different mortality causes should reflect the changes occurring in nature. Moreover, with such obvious causes of mortality, our allocation of carcasses into three main classes is unlikely to have been subject to any more than minor error and could certainly be done in a consistent manner throughout. The analytical and other findings lent support to the view that most (or all) of the birds that were not classed on necropsy as victims of accidents or starvation-disease were indeed casualties of organochlorine use. They gave only a minimal estimate of the likely organochlorine casualties, however, because some of the birds classed as collision or starvation victims also contained potentially lethal organochlorine levels, which may have predisposed their deaths. Our monitoring programme was not started until 1963, when Sparrowhawks and
Sparrowhawk and Kestrel mortality from pesticides
41
Kestrels had already declined in numbers and when the first restrictions in the use of aldrin and dieldrin had already been introduced. Nonetheless, chemical analyses implied that H E O D accounted for a large proportion of recorded Sparrowhawk (50%) and Kestrel (39%) mortality in southeastern Britain during 1963-75, declining thereafter. Indeed, both geographical and temporal variation in H E O D deaths fitted the patterns in aldrin-dieldrin use. The increasing trend in apparent H E O D deaths from the north and west to the south and east paralleled-the increasing proportion of land under arable crops, and the decrease in H E O D deaths over time followed the declining use of aldrin and dieldrin over the study period. These changes in the incidence of apparent H E O D deaths were in turn associated with changes in population levels. In both species, population decline was most marked in the south and east (see above), and during the whole study period (but especially after 1975) populations were in the process of recovery (Newton, 1979, 1986; Newton and Wyllie, 1992). The fact that, among the samples received for analysis, a greater proportion of Kestrel than Sparrowhawk deaths were attributed to H E O D poisoning cannot be taken to imply that Kestrels were more vulnerable to this form of mortality. In the early years, when H E O D victims were most common, there was a marked geographical difference in the finding localities of the two species. Population decline was much more marked in Sparrowhawks than Kestrels, with the result that Sparrowhawks had almost disappeared from the eastern most arable zone by 1963, while Kestrels remained in reasonable numbers. As a result, there was a much greater opportunity for HEOD-poisoned Kestrels to be found, compared with HEOD-poisoned Sparrowhawks. This was reflected in the relative numbers of the two species received from the different zones. In the period 1963-75, in the most arable zone, Kestrels outnumbered Sparrowhawks by 10.2 to one, but, in the least arable zone, Sparrowhawks outnumbered Kestrels by 2.2 to one. By 1986-90, however, when organochlorine use had ceased and populations had largely recovered, Sparrowhawks outnumbered Kestrels in the samples from all four zones (Table 1). In fact, biochemical findings suggest that Sparrowhawks may be somewhat more vulnerable to organochlorine poisoning than Kestrels, as judged by the activity of the mono-oxygenase enzymes which are involved in the metabolic breakdown of these chemicals (Walker et al., 1987). Differences in the other forms of mortality recorded in the two species fit their respective lifestyles and hunting methods. The Sparrowhawk chases small birds at high speed through cover, so would be expected to have frequent collisions; Kestrels, however, which feed mainly on small rodents, would be less prone to collisions but perhaps more vulnerable to starvation, especially during snow periods when their prey are largely hidden or in years when vole numbers are low. Although most aldrin- and dieldrin-treated cereal seed was sown in OctoberNovember, most deaths from H E O D poisoning did not occur until January-April. One possible explanation of this time lag is that H E O D took some weeks to work up the food chain and accumulate to lethal levels in the raptors. This seems not to be the whole explanation, however, for other organochlorine pesticides (notably DDE) and PCBs also reach peak concentration in liver during the same months (Cooke et al., 1982), even though exposure to these chemicals would have followed different seasonal patterns. Almost certainly, then, the peaks in organochlorine concentrations and mortality, which occurred in January-April, were partly a consequence of the physiological condition of the birds at that time of year, perhaps including a greater tendency to accumulate fat reserves, than at other seasons. The fact that many HEOD-induced raptor deaths occurred in late winter and early spring meant that they would have been additive to
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Newton, Wyllie and Asher
most natural mortality, which occurs earlier. This would have enhanced the ability of these pesticides to cause population declines. The main route by which aldrin and dieldrin could have reached the raptors would have been via small rodents (notably Wood Mouse Apodemus sylvaticus) and small seedeating birds to Kestrels, and via seed-eating birds to Sparrowhawks. Contamination of rodents was confirmed in a study in southeast England where Wood Mice, live-trapped in a field for up to 13 days after dieldrin-treated wheat had been drilled, contained an average of 10.1 _ 1.2 Hg g-1 HEOD in their whole bodies (wet weight). In another field, Wood Mice trapped two months after drilling contained 0.7 + 0.5 #g g-1 HEOD (Jefferies and French, 1976). Contamination of seed-eating birds was evident from the many thousands that were found dead and dying around recently sown fields in the years around 1960, and the chemical analyses which revealed HEOD residues in various species (Turtle et al., 1963, Prestt and Ratcliffe, 1972). Disabled birds on the field surface wonld have been particularly attractive to raptors. The involvement of a seed-eating species was the most direct means through which raptors are likely to have acquired HEOD. However, other less direct routes were also involved, as is evident from the general occurrence of HEOD residues in a wide range of bird and mammal species, not only seed-eaters (Prestt and Ratcliffe, 1972). Such general contamination of the prey-base would have ensured a steady uptake of HEOD by the raptors throughout the year. Not all birds which died of HEOD poisoning would be expected to have similar concentrations of HEOD in their livers, but the range of variation found among our apparent H E O D victims was considerable, 5-85 #g g- i in Sparrowhawks and 6-99/~g g- i in Kestrels. The highest concentrations may have resulted from a combination of a recent high intake, a continuing accumulation of residues in the liver in the period between intake and death and possibly also shrinkage of the liver itself. A bird might continue to absorb residues long after its fate was sealed by previously absorbed residues. Whatever the cause of such variation, a wide range of liver residues (13-46 #g g-l) was also found in 22 owls of various species that were analysed from among 55 which died of H E O D poisoning in the London Zoo (Jones et at., 1978). The deaths of these owls were traced to high H E O D levels in the mice that they were fed, the mice having been kept on sawdustbedding derived from dieldrin-treated timber. Another wide range of HEOD values (644 ktg g-l) was found in the livers of wild Barn Owls, Tyro alba, whose deaths were attributed to HEOD poisoning (Newton et al., 1991). Like the raptors in the present study, these birds came mainly from eastern England in the period 1963-75. Clearly, a wide range of tissue concentrations is to be expected in poisoned birds and has also been noted in various experimental studies of H E O D and other organochlorine poisoning (e.g., Turtle et al., 1963; Stickel et aI., 1969). The only comparable long-term study known to us concerns the Bald Eagle, Haliaetus leucocephalus, in the United States. In this species, the proportion of deaths attributed to aldrin-dieldrin also declined over the years, associated with reduced usage. Thus, the deaths of 11.5% of 69 birds in 1966-68 were attributed to HEOD (Mulhern et al., 1970), compared with 15.4% of 39 birds in 1969-70 (Belisle et al., 1972), 10.8% of 37 birds in 1971-72 (Cromartie et al., 1975), 4.7% of 86 birds in 1973-74 (Prouty et al., 1977), 3.0% of 168 birds in 1975-77 (Kaiser et al., 1980) and 1.7% of 293 birds in 1978-83 (Reichel et al., 1984). In our study, we could not exclude the possibility that some recorded deaths were due to other pesticides, such as carbamates and organophosphate compounds, which
Sparrowhawk and Kestrel mortality from pesticides
43
replaced the organochlorines in agricultural use. However, since the proportion of nonobvious deaths declined almost to nil over the years, in line with reduced organochlorine use, any influence of other chemicals could at most have been negligible. The results of this study help to confirm that aldrin and dieldrin played a key role in the regional and temporal changes in Sparrowhawk and Kestrel populations which have occurred in Britain during the past 40 years. We have argued elsewhere that the changes in mortality resulting from aldrin-dieldrin use had more influence on the population changes of these British raptors than did the effects of DDE (Newton, 1986; Newton and Wyllie, 1992).
Acknowledgements This work was funded by the Natural Environment Research Council and the Nature Conservancy Council. We are grateful to all the observers, too numerous to mention individually, who sent in carcasses over the years, and to chemists at the laboratory of the Government Chemist and Monks Wood Experimental Station for chemical analyses.
References Belisle, A.A., Reichel, W.L., Locke, L.N., Lamont, T.G., Muthern, B.N., Prouty, R.M., DeWolf, R.B. and Cromartie, E. (1972) Residues of organochlorine pesticides, potychlorinated biphenyls and mercury, and autopsy data for Bald Eagles, 1969 and 1970. Pesticide Monitor. J. 6, 133-8. Bogan, J. and Newton, I. (1977) Redistribution of DDE in Sparrowhawks during starvation. Bull. Environ. Contamin. Toxicol. 18,317-21. Cade, T.J., Enderson, J.H., Thelander, C.G. and White, C.M. (1988) Peregrine Falcon Populations: Their Management and Recovery. Boise: The Peregrine Fund. Cooke, A.S., Bell, A.A. and Haas, M.B. (1982) Predatory Birds, Pesticides and Pollution. Cambridge: Institute of Terrestrial Ecology. Cromartie, E., Reichel, W.L., Locke, L,N., Belisle, A.A., Kaiser, T.E., Lamont, T.G., Mulhern, B.M., Prouty, R.M. and Swineford, D.M. (1975) Residues of organochlorine pesticides and polychlorinated biphenyls and autopsy data for Bald Eagles, 1971-72. PesticideMonitor. J. 9, 1t-4. DeWitt, J.B., Menzie, C.M., Adomaitis, V.A. and Reichell, W.L. (1960) Pesticidal residues in animal tissues. Trans. North Amer. Wildlife Conf. 25, 277-85. Jefferies, D.J. and Davis, B.N.K. (1968) Dynamics of dieldrin in soil, earthworms, and Song Thrushes. J. Wildlife Management 32, 441-56. Jefferies, D.J. and French, M.C. (1976) Mercury, cadmium, zinc, copper and organochlorine insecticide levels in small mammals trapped in a wheat field. Environ. PoUut. 10, 175-82. Jones, D.M., Bennett, D. and Elgar, K.E. (1978) Deaths of owls traced to insecticide-treated timber. Nature 272, 52. Kaiser, T.E., Reichel, W.L., Locke, L.N., Cromartie, E., Krynitsky, A.J., Lamont, T.G., Mulhern, B.M., Prouty, R.M., Stafford, C.J. and Swineford, D.M. (1980) Organochlorine pesticide, PCB, and PBB residues and necropsy data for Bald Eagles from 29 states - 197577. Pesticide Monitor. J. 13, 145-9. Keymer, I.F., Fletcher, M.R. and Stanley, P.I. (1982) Mortality of Sparrowhawks and Kestrels. Brit. Birds 75, 424-5. Koeman, J.H., Vink, J.A.J. and De Goeij, J.J.M. (1969) Causes of mortality in birds of prey and owls in the Netherlands in the winter of 1968-1969. Ardea 57, 67-76. Moore, N.W. (1965) Pesticides and birds-a review of the situation in Great Britain in 1965. Bird study 12, 222-51.
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Mulhern, B,M., Reichel, W.L., Locke, L.N., Lamont, T.G., Belisle, A., Bronartie, E., Bagley, G.E. and Proaty, R.M. (1990) Organochlorine residues and autopsy data from Bald Eagles 1966-68. Pesticide Monitor. J. 4, 141-4. Newton, I. (1979) Population Ecology of Raptors. Berkhamsted: Poyser. Newton, I. and Haas, M.B. (1984) The return of the Sparrowhawk. Brit. Birds 77, 47-70. Newton, I. and WyUie, I. (1992) Recovery of a Sparrowhawk population in relation to declining pesticide contamination. J. Appl. Ecol., in press. Newton, I. (1986) The Sparrowhawk. Calton: Poyser. Newton, I., Bell, A.A. and Wyllie, I. (1982a) Mortality of Sparrowhawks and Kestrels. Brit. Birds 75, 195-204. Newton, I., Bell, A.A. and Wyllie, I. (1982b) Mortality of Sparrowhawks and Kestrels. Brit. Birds 75,425. Newton, I., Wyllie, I. and Asher, A. (1991) Mortality causes in British Barn Owls Tyto alba, with a discussion of aldrin-dieldrin poisoning. Ibis 133, 162-9. Newton, I., Wyllie, I. and Asher, A. (1992) Long-term trends in organochlorine and mercury residues in some predatory birds in Britain. Environ. PolIut., in press. Nisbet, I.C.T. (1988) The relative importance of DDE and dieldrin in the decline of Peregrine Falcon popttlations. In Peregrine Falcon Populations. Their Management and Recovery (Cade, T.J., Enderson, J.H., Thelander, C.G. and White, C.M., eds) pp. 351-75, Boise: The Peregrine Fund. Opdam, P., Burgers, J. and Miiskens, G. (1987) Population trend, reproduction, and pesticides in Dutch Sparrowhawks following the ban on DDT. Ardea 75, 205-12. Porter, R.D. and Wiemeyer, S.N. (1972) DDE at low dietary levels kills captive American Kestrels. Bull. Environ. Contain. Toxicol. 8, 193-9. Prestt, I., Jeffries, D.J, and Macdonald, J.W. (1968) Post-mortem examinations of four RoughLegged Buzzards. Brit. Birds 61, 45-65. Prestt, I. and Ratcliffe, D.A. (1972) Effects of organochlorine insecticides on European birdlife. Proc. Int. Ornithological Congr. 15, 407-27. Prouty, R.M., Reichel, W.L., Locke, L.N., Belisle, A.A., Cromartie, E., Kaiser, T.E., Lamont, T.G., Mulhern, B.M. and Swineford, D.M. (1977) Residues o f organochlorine pesticides and polychlorinated biphenyls and autopsy data for Bald Eagles, 1973-74. Pesticide Monitor. J. 11, 134-7. Ratcliffe, D.A. (1980) The Peregrine Falcon. Calton: Poyser. Reichel, W.L., Schmeling, S.K., Cromartie, E., Kaiser, T.E., Krynitsky, A.J., Lamont, T.G., Mulhern, B.M., Prouty, R.M., Stafford, C.J. and Swineford, D.M. (1984) Pesticide, PCB, and lead residues and necropsy data for Bald Eagles from 31 States - 1978-1981. Environ. Monitor. Assess. 4, 395-403. Risebrough, R.W. and Peakall, D.B. (1988) The relative importance of the several organochlorines in the decline of Peregrine Falcon populations. In Peregrine Falcon Populations: Their Management and Recovery (Cade, T.J., Enderson, J.H., Thelander, C.G. and White, C.M., eds) pp. 449-62. Boise: The Peregrine Fund. Stiekel, W.H., Stickel, L.F. and Spann, J.W. (1969) Tissue residues of dieldrin in relation to mortality in birds and mammals. In Chemical Fallout (Miller, M.W. and Berg, G.G., eds) pp. 174-204. Springfield: C.C. Thomas. Turtle, E.E., Taylor, A., Wright, E.N., Thearte, 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. J. Sci. Food Agric. 14, 567-77. Village, A. (1990) The Kestrel. Calton: Poyser. Walker, C.H., Newton, I., Hallam, S.D. and Ronis, M.J.J. (1987) Activities and toxicological significance of hepatic microsomal enzymes of the Kestrel (Falco tinnunculus) and Sparrowhawk (Accipiter nisus). Comp. Biochem. Physiol (C) 86, 379-82.
Mortality from the pesticides aldrin and dieldrin in British Sparrowhawks and Kestrels I. N E W T O N * , I. W Y L L I E a n d A. A S H E R
Institute of TerrestrialEcology, Monks Wood Experimental Station, Abbots Ripton, Huntingdon, PE17 2LS, UK Received 27 February 1992; accepted 31 March 1992 Among 1029 dead Sparrowhawks and 1055 dead Kestrels from various parts of Britain that were examined over the period 1963-90, the main causes of death were (a) collisions of various kinds (b) starvation or disease and (c) organochlorine poisoning. The main chemical which caused poisoning was HEOD, derived from the insecticides aldrin and dieldrin. Other deaths were attributed to poisoning by DDE (the main metabolite of the insecticide DDT) and by HE (heptachlor epoxide, derived from the insecticide heptachlor). Sparrowhawks whose deaths were attributed to HEOD poisoning contained 5-85 ¢tg g-1 HEOD in their livers (wet weight), while Kestrels contained 6-99 ¢tg g-1 HEOD. Such birds were typically lighter in weight than collision victims, but heavier than starved or diseased birds. In the period 1963-75, HEOD probably accounted for about 50% of all recorded Sparrowhawk deaths and 39% of all recorded Kestrel deaths in eastern arable districts, but a smaller proportion elsewhere. Geographical variation in the proportion of deaths attributed to HEOD paralleled variation in the proportion of land devoted to arable crops on which aldrin and dieldrin were mainly used. It also paralleled variation in the extent of population decline in these species. Moreover, the proportion of deaths attributed to HEOD declined between 1963-75 and 1976-86, following a marked reduction in aldrin-dieldrin use, and fell to nil in 1987-90, when aldrin and dieldrin were withdrawn altogether. Over this period, the populations of both species recovered from a decline which occurred in the late 1950s, when aldrin-dieldrin were first introduced.
Keywords: Accipter nisus; aldrin; dieldrin; Falco tinnunculus; heptachlor; kestrel; mortality; pesticide; sparrowhawk Introduction In this paper we examine the incidence of aldrin-dieldrin poisoning in British Sparrowhawks, Accipiter nisus, and Kestrels, Falco tinnunculus, during the period 1963-90. The paper is based on necropsies and chemical analyses of birds found dead and sent for examination to Monks Wood Experimental Station. The findings form part of the evidence implicating organochlorine pesticides in the population changes of these and other raptors which have occurred in the past forty years. Following the introduction of organochlorines, the numbers of Sparrowhawks, Kestrels and other raptors in Britain declined in the late 1950s, only to recover again following successive reductions in the use of organochlorines which occurred d u r i n g 1963-86 (Ratcliffe, 1980; Newton, 1986; Newton and WyUie, 1992). Similar changes in raptor populations occurred elsewhere in Europe and in North America (Newton, 1979; Opdam et al., 1987; Cade et al., 1988). *To whom correspondence should be addressed. 0960-9292 © 1992 Chapman & Hall
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Newton, Wyllie and Asher
Decline in the Sparrowhawk population was evident over almost the whole of Britain, but was most marked in eastern regions, where the proportion of arable land, and associated pesticide use, was greatest (Newton and Haas, 1984). Decline in the Kestrel population was much less marked and mainly restricted to eastern arable areas. Two types of chemicals were implicated in these declines: cyclodienes (notably aldrin and dieldrin), which are highly toxic and poison birds directly, thus increasing mortality above the natural level; and DDT-derivatives (notably DDE), which are much less toxic to birds but at sublethal levels can cause eggshell-thinning and egg-breakage, thus reducing the breeding rate. Only at much higher levels (see later) do DDT-type chemicals cause direct mortality. Although both these mechanisms, of enhanced mortality and depressed reproduction, are thought to have contributed to population declines in British raptors, changes in mortality from aldrin-dieldrin use seem to have played the major role (Newton, 1986; Nisbet, 1988). The same may not be true in other countries, however, where usage patterns differed (Risebrough and Peakall, 1988). In Britain, aldrin and dieldrin were used mainly as seed-treatments to protect cereal grains and other seeds against insect attack. At times of sowing, in autumn or spring, such seeds were often eaten by birds and rodents, from which they reached various predators, including Sparrowhawks and Kestrels. The two chemicals were most widely used during 1956-62, after which (because of large-scale spring mortality of seed-eating birds) they were restricted to use on autumn-sown grain. Then, from 1976, they were totally withdrawn from use on cereals and remained only for relatively minor uses, before being banned altogether by statutory control from 1986. The residue monitoring programme, on which this paper is based, was started in 1963 after the peak period of aldrin-dieldrin use, and has continued to the present, during a period of progressively declining use. Some findings from the programme to 1977 were reviewed by Cooke et al. (1982), while trends in mean residues in Sparrowhawks to 1982 were given by Newton and Haas (1984) and in Sparrowhawks and Kestrels to 1990 by Newton et al. (1992). In addition, the necropsy findings from the two species to 1979 were summarized by Newton et al. (1982a). In this paper, we focus on those mortality incidents in the two species that could be attributed to aldrin-dieldrin and examine how such incidents have varied across the country and over the years in relation to changing aldrin-dieldrin use. Materials and methods
The specimens for analysis came from most parts of Britain in response to regular advertisements placed in ornithological magazines and journals asking for birds found dead. All birds were requested, regardless of the cause of death. In the event, most were accident victims, while others appeared to have died of food shortage or disease; only a small proportion seemed to have died of pesticide poisoning (Newton et al., 1982a). On receipt, each carcass was weighed, marked and then stored at - 2 0 °C until it could be examined, up to several months later. For necropsy, the unfrozen carcass was opened up and examined for body condition, any obvious parasites, lesions or other abnormalities. The findings were used, along with information from the sender, to allocate each bird to one of three main categories (following Cooke et al., 1982)), according to whether it had apparently died of: (1) collision, shooting or other trauma; (2) starvation or disease; or (3) pesticide poisoning or other nonobvious causes. Most specimens (93% of Sparrowhawks and 95% of Kestrels) could be allocated to one of these three categories,
Sparrowhawk and Kestrel mortality from pesticides
33
even though within each category the precise cause of death was not always obvious. The remaining ones could not be allocated because only part of the carcass (often the liver only) was received for analysis. These latter birds are omitted from further consideration, leaving a total of 1029 Sparrowhawks and 1085 Kestrels. However, other types of information (for example, body weight or month of death) was also missing from some specimens, leading to variation in the numbers available for different analyses (see Tables 1 and 2, Figs 1-3). Typically, collision casualties had extensive bruising and broken bones, and many were found at roadsides, indicating that they were traffic victims. Shot birds contained lead pellets or had pellet wounds. Assignment of other traumatic mortality causes, such as drowning, was dependent mainly on information from the sender, together with the lack of any conflicting evidence from necropsy. Starved birds were low in weight, with wasted breast muscles, no body fat, no fat on the heart and empty blackish or greenish intestines. Diseased birds were very few in number, but also in poor body condition ("thin") and showed obvious lesions, particularly on liver, kidneys or lungs, or contained large numbers of helminth parasites. The deaths of all or most of the remaining birds could be attributed to pesticide poisoning. Verification of apparent pesticide victims was dependent mainly on chemical analysis (see below), together with the tack of any other obvious mortality cause. Many supposed organochlorine victims also showed signs of haemorrhaging around certain internal organs, including brain, lungs, heart and foregut (Newton et al., 1982a,b). This was quite distinct from the heavier, more superficial and local haemorrhaging found at the point of impact in accident victims. In addition, some apparent pesticide victims were found alive, but reported by the sender to die in spasms, while other birds found dead showed signs of a similar death as their wings and tail were spread or their feet were firmly clenched, clutching grass or leaves. Birds which had died from other obvious causes showed none of these symptoms. After necropsy, a piece of liver was removed from each specimen and analysed for organochlorine residues of D D E and TDE (from the insecticide DDT), H E O D (from the insecticides aldrin and dieldrin) and H E (from the insecticide heptachlor), using gasliquid chromatography. The limit of detection was about 0.01/~g per g wet weight. To achieve consistency over the years, analytical results were continually checked against standards of known concentration (for full analytical procedure, see Newton et al., 1992). All carcasses were sampled, regardless of cause of death, and residues are presented here on a fresh weight basis. Diagnosis of pesticide victims, largely on the basis of residue levels in tissues, was inevitably somewhat arbitrary, as it was based partly on comparative data from other species deliberately dosed to the point of death with the relevant chemicals. The considerable variation in sensitivity, both between and within species, meant that a given level might be lethal to one bird but not to another. Furthermore, because organochlorines accumulate in body fat, when a bird loses weight, residues released from metabolised fat redistribute themselves within the body, rising in concentration in other tissues, such as liver (Jefferies and Davis, 1968; Stickel et al., 1969; Porter and Wiemeyer, 1972; Bogan and Newton, 1977). There is thus an interaction between a bird's nutritional state and the organochlorine levels in different tissues, and it is sometimes difficult to separate starvation from poisoning as the primary cause of death. After considering the available data, Moore (1965) and Cooke et al. (1982) concluded for various birds that a concentration in liver of 10/~g g-* or more of H E O D (in wet weight) or 100 ~g g-1 or more of
34
Newton, Wyllie and Asher
DDE could be taken as indicative of lethal organochlorine poisoning, but these figures were intended only as a rough guide. Some specific information on HEOD is available for Kestrels and Sparrowhawks, in that Jefferies found HEOD concentrations of 12/zg g-1 and 19/zg g-1 in the livers of two Kestrels that had been experimentally poisoned with dieldrin (in Prestt et al., 1968), while Koeman et al. (1969) found 16, 24 and 19 pg g-~ of H E O D in the livers of two wild Kestrels and a Sparrowhawk whose deaths were attributed to dieldrin poisoning in the Netherlands. Little information is available for heptachlor, but DeWitt et at. (1960) found 6-20#g g-1 HE in tissues of various birds poisoned by this chemical, and Turtle et at. (1963) found 19-53 pg g-i in the muscle of ten experimentally poisoned pigeons, compared with 5-23 #g g-1 in seven survivors. As mentioned above, organochlorine victims often showed other symptoms, however, such as internal haemorrhaging (Cooke et al., 1982; Keymer et al., 1982; Newton et aI., 1982a,b) and usually died with muscle tremors or convulsions. For examination of geographical variation in apparent organochlorine mortality, the country was divided into four zones, where the proportion of tilled land in 1960 was less than 10%, 11-30%, 31-60% and more than 60%, respectively (see Newton and Haas (1984) for map). The proportion of tilled land was assumed to reflect regional variation in pesticide use. It was lowest in the north and west of the country and highest in the south and east. In all four zones the proportion of tilled land increased slightly during the study, but not sufficiently to warrant redrawing the boundaries of the different zones. Throughout the commonest arable crops were cereals, which occupied about 90% of all tilled land. For examination of temporal variation in apparent organochlorine mortality, the period of study (1963-90) was divided into three sub-periods: 1963-75, when aldrindieldrin were permitted for use on autumn-sown cereals as well as on other minor crops; 1976-86 when aldrin-dieldrin were permitted for use on minor crops only; and 1987-90, when they were banned altogether. The pesticide heptachlor had been fairly widely used on cereals up to 1963 but was then quickly phased out, while DDT was used throughout the period 1963-86 but in progressively decreasing quantities. Results
Of 1029 Sparrowhawks from the period 1963-90, the deaths of 727 (70.7%) were attributed to accidents (including shooting), of 266 (25.9%) to starvation (including disease) and of 36 (3.5%) to organochlorine poisoning (including 25 (2.4%) attributed to HEOD, 10 (0.8%) to DDE/TDE and one (0.1%) to HE). Of 1085 Kestrels from the same period, the deaths of 409 (37.7%) were attributed to accidents, of 563 (51.9%) to starvation and 113 (10.4%) to organochlorine poisoning (including 88 (8.1%) attributed to HEOD, 23 (2.1%) to DDE/TDE and two (0.2%) to HE). The frequency of these three main mortality classes differed significantly between the species (u 2 = 233.9, p < 0.001). Mortality from H E O D In both species, the proportion of apparent HEOD victims varied greatly between the four agricultural zones and also declined over time (Table 1). In the period 1963-75, when aldrin and dieldrin were still widely used on autumn-sown cereals, H E O D victims of both species were received from all four agricultural zones; but they formed a significantly higher proportion of carcasses from the eastern zone (50% of Sparrowhawks
0.001 < 0.05 Cp < 0.01
•pp
250
~
I 'm
~
100
150
~
~
200 Grams
Fig. 3, Body weights of Sparrowhawks and Kestrels whose deaths were attributed to different causes, October-April only.
~
}
3250
40
.Newton, Wyllie and Asher
figures for Kestrels were 160 g for most males and 170 g for most females. In both sexes of both species, birds classed as H E O D victims were generally intermediate in weight between accident and starvation casualties, possibly because most had become immobilized some time before their death.
Mortality from other organochlorines Compared with H E O D , fewer deaths were attributed to DDE. Like deaths from H E O D , however, deaths from D D E were initially widespread but found mostly in the eastern region. Apart from one Sparrowhawk, they were all prior to 1987, when the ban on all organochlorines came into effect. The levels of D D E found in 10 Sparrowhawks whose deaths were attributed to this chemical were in the range 140-251 #g g-l, apart from two with 55 #g g-1 and 40 /~g g-1 which also had 35 and 48 #g g-1 TDE, respectively. These last two birds had only traces of other organochlorines but died of convulsions with internal haemorrhaging typical of organochlorine victims. The equivalent D D E levels in 23 Kestrels were mostly in the range 110-812 ppm, with two outliers at 1474 (1982) and 1500 ppm (1978). The carcasses of both these Kestrels were in good physical condition and were found in an area of intensive fruit-growing (Kent) where D D T use was especially high. The deaths of three birds were attributed to HE, namely two Kestrels with 10 and 15 #g g-l, and one Sparrowhawk with 10 #g g-1. In these birds, residues of all other organochlorines were well below supposed lethal levels. Some birds had supposed lethal levels of more than one chemical. Thus, one Sparrowhawk with 17 #g g-1 H E O D also contained 340 #g g-~ of DDE, while five Kestrels whose deaths were arbitrarily attributed to H E O D also contained 17 and 40 pg g-1 of H E and 110, 150 and 260jzg g-1 of DDE, respectively. In addition, H E levels exceeding 10#g g-1 were found in one Sparrowhawk and one Kestrel which died of collisions, while D D E levels exceeding 100 were found in seven Sparrowhawks and one Kestrel which died of collisions, and in five Sparrowhawks which had apparently starved. Discussion
The carcasses received for analysis probably did not represent a random cross-section of Sparrowhawk or Kestrel deaths but were biased towards those forms of mortality most readily detected by people. This may account for the high proportion of collision victims: many of the Kestrels had been hit by vehicles and were found at roadsides, while many of the Sparrowhawks had collided with windows. Despite this likely bias, however, carcasses were obtained in the same way throughout the study, so that changes in the proportions of different mortality causes should reflect the changes occurring in nature. Moreover, with such obvious causes of mortality, our allocation of carcasses into three main classes is unlikely to have been subject to any more than minor error and could certainly be done in a consistent manner throughout. The analytical and other findings lent support to the view that most (or all) of the birds that were not classed on necropsy as victims of accidents or starvation-disease were indeed casualties of organochlorine use. They gave only a minimal estimate of the likely organochlorine casualties, however, because some of the birds classed as collision or starvation victims also contained potentially lethal organochlorine levels, which may have predisposed their deaths. Our monitoring programme was not started until 1963, when Sparrowhawks and
Sparrowhawk and Kestrel mortality from pesticides
41
Kestrels had already declined in numbers and when the first restrictions in the use of aldrin and dieldrin had already been introduced. Nonetheless, chemical analyses implied that H E O D accounted for a large proportion of recorded Sparrowhawk (50%) and Kestrel (39%) mortality in southeastern Britain during 1963-75, declining thereafter. Indeed, both geographical and temporal variation in H E O D deaths fitted the patterns in aldrin-dieldrin use. The increasing trend in apparent H E O D deaths from the north and west to the south and east paralleled-the increasing proportion of land under arable crops, and the decrease in H E O D deaths over time followed the declining use of aldrin and dieldrin over the study period. These changes in the incidence of apparent H E O D deaths were in turn associated with changes in population levels. In both species, population decline was most marked in the south and east (see above), and during the whole study period (but especially after 1975) populations were in the process of recovery (Newton, 1979, 1986; Newton and Wyllie, 1992). The fact that, among the samples received for analysis, a greater proportion of Kestrel than Sparrowhawk deaths were attributed to H E O D poisoning cannot be taken to imply that Kestrels were more vulnerable to this form of mortality. In the early years, when H E O D victims were most common, there was a marked geographical difference in the finding localities of the two species. Population decline was much more marked in Sparrowhawks than Kestrels, with the result that Sparrowhawks had almost disappeared from the eastern most arable zone by 1963, while Kestrels remained in reasonable numbers. As a result, there was a much greater opportunity for HEOD-poisoned Kestrels to be found, compared with HEOD-poisoned Sparrowhawks. This was reflected in the relative numbers of the two species received from the different zones. In the period 1963-75, in the most arable zone, Kestrels outnumbered Sparrowhawks by 10.2 to one, but, in the least arable zone, Sparrowhawks outnumbered Kestrels by 2.2 to one. By 1986-90, however, when organochlorine use had ceased and populations had largely recovered, Sparrowhawks outnumbered Kestrels in the samples from all four zones (Table 1). In fact, biochemical findings suggest that Sparrowhawks may be somewhat more vulnerable to organochlorine poisoning than Kestrels, as judged by the activity of the mono-oxygenase enzymes which are involved in the metabolic breakdown of these chemicals (Walker et al., 1987). Differences in the other forms of mortality recorded in the two species fit their respective lifestyles and hunting methods. The Sparrowhawk chases small birds at high speed through cover, so would be expected to have frequent collisions; Kestrels, however, which feed mainly on small rodents, would be less prone to collisions but perhaps more vulnerable to starvation, especially during snow periods when their prey are largely hidden or in years when vole numbers are low. Although most aldrin- and dieldrin-treated cereal seed was sown in OctoberNovember, most deaths from H E O D poisoning did not occur until January-April. One possible explanation of this time lag is that H E O D took some weeks to work up the food chain and accumulate to lethal levels in the raptors. This seems not to be the whole explanation, however, for other organochlorine pesticides (notably DDE) and PCBs also reach peak concentration in liver during the same months (Cooke et al., 1982), even though exposure to these chemicals would have followed different seasonal patterns. Almost certainly, then, the peaks in organochlorine concentrations and mortality, which occurred in January-April, were partly a consequence of the physiological condition of the birds at that time of year, perhaps including a greater tendency to accumulate fat reserves, than at other seasons. The fact that many HEOD-induced raptor deaths occurred in late winter and early spring meant that they would have been additive to
42
Newton, Wyllie and Asher
most natural mortality, which occurs earlier. This would have enhanced the ability of these pesticides to cause population declines. The main route by which aldrin and dieldrin could have reached the raptors would have been via small rodents (notably Wood Mouse Apodemus sylvaticus) and small seedeating birds to Kestrels, and via seed-eating birds to Sparrowhawks. Contamination of rodents was confirmed in a study in southeast England where Wood Mice, live-trapped in a field for up to 13 days after dieldrin-treated wheat had been drilled, contained an average of 10.1 _ 1.2 Hg g-1 HEOD in their whole bodies (wet weight). In another field, Wood Mice trapped two months after drilling contained 0.7 + 0.5 #g g-1 HEOD (Jefferies and French, 1976). Contamination of seed-eating birds was evident from the many thousands that were found dead and dying around recently sown fields in the years around 1960, and the chemical analyses which revealed HEOD residues in various species (Turtle et al., 1963, Prestt and Ratcliffe, 1972). Disabled birds on the field surface wonld have been particularly attractive to raptors. The involvement of a seed-eating species was the most direct means through which raptors are likely to have acquired HEOD. However, other less direct routes were also involved, as is evident from the general occurrence of HEOD residues in a wide range of bird and mammal species, not only seed-eaters (Prestt and Ratcliffe, 1972). Such general contamination of the prey-base would have ensured a steady uptake of HEOD by the raptors throughout the year. Not all birds which died of HEOD poisoning would be expected to have similar concentrations of HEOD in their livers, but the range of variation found among our apparent H E O D victims was considerable, 5-85 #g g- i in Sparrowhawks and 6-99/~g g- i in Kestrels. The highest concentrations may have resulted from a combination of a recent high intake, a continuing accumulation of residues in the liver in the period between intake and death and possibly also shrinkage of the liver itself. A bird might continue to absorb residues long after its fate was sealed by previously absorbed residues. Whatever the cause of such variation, a wide range of liver residues (13-46 #g g-l) was also found in 22 owls of various species that were analysed from among 55 which died of H E O D poisoning in the London Zoo (Jones et at., 1978). The deaths of these owls were traced to high H E O D levels in the mice that they were fed, the mice having been kept on sawdustbedding derived from dieldrin-treated timber. Another wide range of HEOD values (644 ktg g-l) was found in the livers of wild Barn Owls, Tyro alba, whose deaths were attributed to HEOD poisoning (Newton et al., 1991). Like the raptors in the present study, these birds came mainly from eastern England in the period 1963-75. Clearly, a wide range of tissue concentrations is to be expected in poisoned birds and has also been noted in various experimental studies of H E O D and other organochlorine poisoning (e.g., Turtle et al., 1963; Stickel et aI., 1969). The only comparable long-term study known to us concerns the Bald Eagle, Haliaetus leucocephalus, in the United States. In this species, the proportion of deaths attributed to aldrin-dieldrin also declined over the years, associated with reduced usage. Thus, the deaths of 11.5% of 69 birds in 1966-68 were attributed to HEOD (Mulhern et al., 1970), compared with 15.4% of 39 birds in 1969-70 (Belisle et al., 1972), 10.8% of 37 birds in 1971-72 (Cromartie et al., 1975), 4.7% of 86 birds in 1973-74 (Prouty et al., 1977), 3.0% of 168 birds in 1975-77 (Kaiser et al., 1980) and 1.7% of 293 birds in 1978-83 (Reichel et al., 1984). In our study, we could not exclude the possibility that some recorded deaths were due to other pesticides, such as carbamates and organophosphate compounds, which
Sparrowhawk and Kestrel mortality from pesticides
43
replaced the organochlorines in agricultural use. However, since the proportion of nonobvious deaths declined almost to nil over the years, in line with reduced organochlorine use, any influence of other chemicals could at most have been negligible. The results of this study help to confirm that aldrin and dieldrin played a key role in the regional and temporal changes in Sparrowhawk and Kestrel populations which have occurred in Britain during the past 40 years. We have argued elsewhere that the changes in mortality resulting from aldrin-dieldrin use had more influence on the population changes of these British raptors than did the effects of DDE (Newton, 1986; Newton and Wyllie, 1992).
Acknowledgements This work was funded by the Natural Environment Research Council and the Nature Conservancy Council. We are grateful to all the observers, too numerous to mention individually, who sent in carcasses over the years, and to chemists at the laboratory of the Government Chemist and Monks Wood Experimental Station for chemical analyses.
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