S18.1: Raptor poisonings and current insecticide use: What do isolated kill reports mean to populations?

Charles J. Henny1, Pierre Mineau2, John E. Elliott3 & Brian Woodbridge4

1USGS Forest & Rangeland Ecosystem Science Center, 3200 SW Jefferson Way, Corvallis, OR 97331, USA, e-mail hennyc@fsl.orst.edu, fax 541 757-4845; 2Canadian Wildlife Service, Environment Canada, 100 Gamelin, Hull, PQ K1A 0H3, Canada, e-mail pierre.mineau@ec.gc.ca; 3Canadian Wildlife Service, Environment Canada, 5421 Robertson Road, RR1, Delta, BC V4K 3N2, Canada, e-mail john.elliot@ec.gc.ca; 4USDA Forest Service, Klamath National Forest, 1312 Fairlane Road, Yreka, CA 96097, USA, woodbrdg@snowcrest.net

Henny, C.J., Mineau, P., Elliott, J.E., & Woodbridge, B. 1999. Raptor poisonings and current insecticide use: What do isolated kill reports mean to populations? In: Adams, N.J. & Slotow, R.H. (eds) Proc. 22 Int. Ornithol. Congr., Durban: 1020-1032. Johannesburg: BirdLife South Africa.

Raptors killed by organophosphorus (OP) and carbamate (CB) pesticides were evaluated on three spatial scales: (1) continental (isolated kill reports, all species in United States), (2) a single species and its world-wide distribution, and (3) a regional population. Isolated kill reports of raptors from the United States (l985-94) were used to evaluate species vulnerability. Incidents were categorised into abuse (gross label violations), labelled use (normal agricultural practice) and use unknown. Main exposure routes for labelled use were: (1) consumption of contaminated invertebrates (usually sprays, sometimes granules), (2) secondary poisoning through consumption of vertebrates (usually granules, sometimes sprays with other special cases including avicides and topical livestock treatment with pour-ons), and (3) dermal exposure (dormant oil sprays). Swainson’s Hawks Buteo swainsoni wintering in Argentina (exposed by eating insects), and a local population of Bald Eagles Haliaeetus leucocephalus in British Columbia (exposed by eating waterfowl contaminated by granular insecticides) were evaluated in more detail when an estimated 2-5% of each population was killed by OPs or CBs. Data available provided no evidence of adverse long-term population effects (i.e., reduced numbers) related to the pesticide incidents. We conclude from our review that poisonings are likely and frequent under current pesticide use practices, and that there are potential population impacts where raptors congregate in agricultural areas. This mortality is preventable when less toxic alternative pesticides are available. Only a few products or formulations were responsible for most of the problems. More studies are needed to further evaluate raptor exposure to OPs and CBs and to determine effects on individuals and populations.

 

INTRODUCTION

Bald Eagle, Peregrine Falcon Falco peregrinus, and Osprey Pandion haliaetus populations all increased during the last two decades (Millar l995, Cade et al. 1988, Houghton and Ryman l997) with the first two species now being delisted from Endangered Species status; the latter was never listed although its population declined throughout most of North America. These species declined primarily because of DDT and perhaps other organochlorine (OC) insecticides, and responded positively after the products were banned in the l970s. The three species shared two characteristics: (l) they were top of the food chain predators, and (2) their diets included either fish or birds that bioaccumulated OC insecticides. The mammal-eating and insect-eating hawks and owls were not exposed to high concentrations of OC insecticides (Moore l966, Keith l969).

The use of organophosphorus (OP) and carbamate (CB) insecticides, which are both anti-cholinesterase compounds (anti-ChEs), began in the l950s and became more widespread as replacements for banned OCs in the l970s and l980s.These replacement chemicals were not persistent (especially when compared to OCs) and did not bioaccumulate in food chains like the OCs; however, the tradeoff was that manyOPs and CBs were extremely toxic for varying periods of time, e.g., for famphur up to 100 days (Henny et al. 1985). Raptor mortality from anti-ChEs was first reported in the l970s (Mills l973, Mendelssohn and Paz l977), and continued into the l980s and l990s (e.g., Balcomb l983, Henny et al. 1985, 1987, Tarboton l987, Meinzingen et al. l989, Woodbridge et al. 1995, Elliott et al. 1996, l997). Some reports involved hundreds of poisoned raptors. Raptors that died from these products were not necessarily those that ate fish or birds, but included almost all species. Therefore, criteria other than diet becomes important in understanding the distribution and magnitude of the raptor deaths. The species vulnerability issue may be as simple as being at the wrong place (sprayed field) at the wrong time (within a certain number of days of spray event) and eating exposed prey, having dermal contact with the spray or inhaling the spray. The vulnerability question may become, ‘Which species most closely associate with agricultural land?’ Other questions often asked include, ‘Do deaths from anti-ChEs have an affect on the size of raptor populations, i.e., a population effect?’, and, ‘Which species are most likely killed and what circumstances or special species traits make them vulnerable to anti-ChEs ?’ The importance of these mortality incidents to conservation of raptor populations is often debated, and the debate is usually based upon minimal data.

Traditionally, contaminant studies (including anti-ChEs) have used the individual-based approach, i.e., a dead bird with the cause of death usually determined by several diagnostic criteria. These criteria for OPs and CBs have been the combination of 50% brain ChE inhibition, and the presence of identifiable chemical residues in the digestive tract (Hill and Fleming 1982). This contrasts considerably with a population-based approach. It is important to recognise that much additional information is needed to evaluate potential population effects. To evaluate population effects, there must be linkages or an integration between ecology, population dynamics, and toxicology, since many factors influence population size. Therefore, the approach must be multi-disciplined. Population parameters of special concern include: population size, change in population size over time, population turnover (i.e., mortality rates); and other population characteristics of equal importance include: productivity rates, age at sexual maturity, natal dispersal, and fidelity to breeding or wintering localities. Prey availability and weather can also influence population numbers and distribution. Much of this information is seldom available for a raptor species or local raptor populations, and many biologists believe that it is nearly impossible to document contaminant-related population effects on raptors on any spatial scale, and they usually point to many decades of research evaluating the effects of hunting on waterfowl and upland game bird populations. To address the population effect of hunting game species (contaminants could be viewed in the same context as harvesting or taking), detailed population surveys are made annually, harvest or take information is obtained by annual surveys, recruitment information is obtained annually and related to habitat characteristics (food, water, etc.), and many birds are banded annually to estimate annual survival rates. Collectively over many years, with large data collection regimes and with hunting regulations modified to change the harvest or take, changes in survival rates from given harvest rates may be discerned for a few key waterfowl species (e.g., see Nichols 1991).

With this perhaps somewhat pessimistic introduction on evaluating population effects, we now review three data sets to address the issue of raptor poisonings by anti-ChEs on three spatial scales. First, we present all documented raptor poisoning incidents that we could find from the United States for the period l985-94 (isolated kill reports). Then, we present a case study of Swainson’s Hawk mortality in Argentina resulting from the use of monocrotophos for grasshopper control (species issue). Then, another case study of wintering Bald Eagle mortality in the Fraser River delta of British Columbia which is an area of intensive agriculture (population or regional issue). Patterns derived from isolated kill reports provide clues regarding species vulnerability and the circumstances. Findings from the two case studies provide a framework to discuss population effects and circumstances resulting in large numbers of each species being poisoned.

RESULTS AND DISCUSSION

Raptor poisonings in the United States, 1985-94

Our source of information for this section was incidents involving raptors reported to authorities in the United States. Those cases from 1985-94 were originally compiled by Mineau et al. (in press) from records held by the U.S. Fish and Wildlife Service (USFWS), the U.S. Environmental Protection Agency (USEPA), and the Biological Resources Division of the U.S. Geological Survey (USGS) at the National Wildlife Health Center. Mineau et al. (in press) ascribed a ‘certainty index’ to each and used best scientific judgement to categorise incidents and recognised that information available might be judged inadequate by legal standards.

Following their extensive work on famphur, Henny et al. (1985) suggested that: ‘The lack of OP secondary poisoning reports for birds of prey in North America may be due to the limited number of dead raptors being analysed for ChE depression and OP residues.’ As a result the dates 1985-94 correspond to a general increased effort made in the United Sates to document raptor mortality following poisoning with anti-ChEs. Mineau et al. (in press) also pointed out a number of biases and limitations in their data set including: (1) the information was only a subset of the incidents and actually only a subset of the documented incidents (not all authorities were contacted), (2) a systematic bias existed toward Bald and Golden Eagles Aquila chrysaetos which were more likely fully investigated for legal reasons, (3) the insecticides diazinon and carbofuran were subjected to special reviews by the USEPA during the time period which perhaps placed more focus on them, and (4) large bodied birds which flock have a higher probability of being discovered. Mineau et al. (in press) also tried to distinguish malicious poisoning of birds and other gross pesticide label violations (abuse) from incidents resulting from normal agricultural practice (labelled use). Cases where labels were not necessarily followed to the letter were either ascribed to abuse or to labelled use depending on the apparent severity of the infraction. Cases where interpretation was difficult were simply left as use unknown.

Mineau et al. (in press) believed cases of pesticide abuse were more likely reported because: (1) birds killed by highly concentrated baits do not go far from the site of intoxication, and birds which fly away from the site of exposure are less likely to be analysed for anti-ChEs, and (2) abuse cases are considered less sensitive, i.e., they do not reflect poorly on a jurisdiction’s agricultural operations or pesticide regulatory system, and (3) pesticide users may be reluctant to report problems if they believe the pesticide implicated is essential to their livelihood.

The Incidents

Between 1985 and 1994, there were 255 incidents reported involving 734 dead raptors. Fewer incidents were reported in 1985, but 21-33 incidents were reported annually between 1986 and 1994. The incidents were tallied by chemical and type of incident (Table 1) and also by species (Table 2).

Mineau et al. (in press) reported 73 abuse and 63 labelled use incidents for raptors between 1985 and 1994, (Table 1). Furthermore, circumstances surrounding many of the incidents in the unknown category were suggestive of labelled use. Where ChE inhibitors were concerned, dead raptors reported from the United States were at least as likely killed from labelled use as wilful attempts to poison them or some other vertebrate.

Not all species are as likely to suffer the brunt of pesticide abuse. The Golden Eagle was almost always killed by abuse (Table 2). This is explained by the species absence from much cropland. Most kills were recorded in the western states in association with attempts to kill eagles, and/or wolves Canis lupus, or coyotes Canis latrans. The Red-tailed Hawk Buteo jamaicensis is one of several species equally likely to be killed following abuse or labelled use. Many other species, especially those less prone to scavenging and therefore taking baits, were more frequently killed by labelled uses. This is most notably the case for accipiters, as well as most owl, falcon and kite species. Pesticides employed in abuse cases undoubtedly reflect availability as well as toxicity. Carbofuran is widely available in several formulations and registered for a large number of crops. This single pesticide accounted for 75% of all known abuse cases during the study period (Table 1).

Main Routes of Exposure from Labelled Use

Consumption of Contaminated Invertebrates: Insectivory is important to a large number of raptor species. The most obvious exposure situation is where recently sprayed insects were consumed directly by raptors (see later, Swainson’s Hawk in Argentina). Few incidents clearly result from the direct ingestion of invertebrates contaminated by pesticide formulations other than sprays; however, Balcomb (1983) noted granules of carbofuran adhering directly to earthworms.

Secondary Poisoning through Consumption of Vertebrates: Secondary poisoning in its strictest definition refers to the passing of residues assimilated into one animal tissue (usually not exclusively vertebrate) into another animal. The USEPA refers to secondary poisoning as residues being passed from vertebrate to vertebrate without regard to the exact location of these residues. This is the most practical definition and the one used here. It is likely that most cases of ‘secondary poisoning’ involving OPs and CBs do not involve residues assimilated in the tissues of the primary kill. In most cases, residues are transferred to a predator or scavenger when the gut contents are ingested or when surface residues are ingested or transferred during prey handling.

The most common form of secondary poisoning in raptors is seen following the use of granular insecticides. Granular insecticides are highly concentrated forms of pesticides which are often implicated in kills of songbirds, shorebirds, and waterfowl as well as small mammals and other vertebrates. Granular insecticides are particularly attractive to songbirds, either as grit or as food. Typically, secondary kills which appear to result from contaminated songbirds occur at, or soon after insecticide application (often at seeding). Several incidents were documented in corn, grapes, winter wheat, and tree farms. Bald Eagles, Buteo hawks, harriers, and accipiters were poisoned. Another less commonly recognised route of exposure to granular insecticides is ‘passive uptake’ generally involving waterfowl species. Typically, waterfowl are exposed to granular insecticides when they sift sediments and crop residues in puddles or waterlogged soils (see later, Bald Eagles in British Columbia).

Insecticides need not be present as concentrated granular material to secondarily affect raptors. Several incidents were recorded in vineyards following application of carbofuran to drip irrigation water when songbirds were attracted to the irrigation water for drinking and were then captured or scavenged. The primary vertebrate kills, especially small birds or mammals, can carry an appreciable load of residues on their fur or feathers from being in contact with an aerosol or entering a freshly sprayed area. It is difficult to conclude whether secondary poisoning is a result of consuming viscera or surface residues or both.

Some bird control (avicide) programs use ChE inhibitors, and it is not surprising that raptors attracted to the easy source of food are killed. In North America, the main use of anti-ChEs for bird control has been the Rid-A-BirdTM perch. It consists of a hollow mesh perch into which sits a wick soaked in a solution of 11% fenthion. The perches are labelled for the control of Starlings Sturnus vulgaris, House Sparrows Passer domesticus, and Rock Doves Columbia livia. Hunt et al. (1991, 1992) experimentally demonstrated the risk of secondary poisoning from the use of fenthion in Rid-A-BirdTM perches. A single contaminated sparrow proved lethal to 9 of 10 American Kestrels Falco sparverius. Furthermore, exposed sparrows were 16-fold more likely captured by kestrels than their unexposed flock mates. Mineau et al. (in press) summarised 20 fenthion poisoning cases involving 71 raptors (including 6 Peregrine Falcons) believed to result from Rid-A-BirdTM perches. In March 1998, the manufacturer applied for a voluntary cancellation of the product in the U.S. with one year to use existing stock. Also, fenthion has been one of the main avicides used in the control of Red-Billed Quelea Quelea quelea in several African countries, a use pattern reviewed by Keith and Bruggers (1998).

The topical treatment of livestock with the OP famphur poured on the back to systemically control warble fly larva has resulted in secondary poisoning of raptors. Ranchers reported kills of magpies associated with the use of famphur as early as 1973, shortly after its introduction to the U.S. market (Henny et al. 1985). Henny et al. (1985, 1987) and Franson et al. (1985) described secondary poisoning of raptors associated with primary kills of Black-billed Magpies Pica pica and Starlings. They found that magpies were poisoned when they ingested hair from topically treated cattle. Scavengers (notably Red-tailed Hawks) died when exposed to the magpies and those authors even documented tertiary poisoning of a Great Horned Owl Bubo virginianus scavenging one of the dead hawks. In the early years, it was not known that famphur could persist on hair of treated cattle for >100 days. Therefore, eagles that died weeks or months after cattle treatment were automatically assumed to be abuse cases. Fewer cases were recorded with fenthion used as a ‘pour on’, but this may simply reflect the extent of use.

Dermal Exposure in Treated Areas: Dermal exposure of raptors is important in almond and stone fruit orchards in California, where insecticides are applied in dormant oil sprays.  Fry et al. (1998) used radio telemetry and pesticide use data correlated with foot wash residues and blood ChE to assess the relative contributions of a number of OP pesticides to the ‘effective’ exposure in Red-tailed and Red-shouldered Hawks Buteo lineatus using the orchards. Of the pesticides studied (ethyl parathion, diazinon, methidathion and chlorpyrifos), parathion contributed the most to the measured level of ChE inhibition in the hawks. Parathion use in dormant oil sprays was cancelled in 1991. Most birds did not appear to die from toxicosis; usually, trauma such as electrocution, entanglement or impact was diagnosed as the proximate cause of death. Based upon inhibited ChE as well as pesticide residues extracted from feathers or foot washes, pesticides were ascribed only a contributing role. The role that ingestion of contaminated prey may be playing in these incidents was not assessed.

Risk factors contributing to raptor poisoning

Several risk factors were discussed in the context of exposure routes. Significant factors resulting in raptor poisonings included: insectivory; opportunistic taking of debilitated prey; scavenging, especially if GI tracts were consumed; presence in agricultural areas; perceived status as a pest species; and flocking or other gregarious behaviour at some part of their life cycle, e.g., a geographically-restricted breeding, migration or wintering area. Other factors include the toxicity of the pesticide in use and the relative sensitivity of the raptor species to the pesticides. Also, limited information exists to assess the sensitivity of birds of prey relative to other bird species.

Conservation aspects of raptor poisoning

The magnitude and relative importance of raptor mortality from anti-ChEs in North America is difficult to estimate. Although kills are frequent, they generally involve small numbers of birds, widely dispersed on their breeding range. Large kills of the Swainson’s Hawk have been reported from the use of monocrotophos on wintering grounds in Argentina (Woodbridge et al. 1995a, Goldstein et al. 1996, Canavelli et al. 1996), and pesticide poisoning resulting from apparently normal use of soil insecticides is an important cause of death among wintering Bald Eagles in the lower Fraser River delta of British Columbia, Canada (Elliott et al. 1996, 1997). We probe into these two case histories, which have drawn considerable attention, to evaluate possible adverse effects at the population level.

Swainson’s Hawk in Argentina

Possible adverse effects of anti-ChEs on wintering grounds of Swainson’s Hawks in Argentina was mentioned by Risebrough et al. (1989) although it was only a suspicion. It was not until the winter of 1994-95 that over 700 dead Swainson’s Hawks were found in Argentina while biologists were locating satellite-transmitted hawks from California (Woodbridge et al. 1995a). The hawks died after consuming grasshoppers which were sprayed with an unknown pesticide. The symptoms suggested anti-ChE poisoning. Although the initial report was an isolated event, discussions with biologists and ranchers in Argentina lead the authors to suspect that the event was not unusual. Recent changes on the pampas to more intensive agricultural cultivation of alfalfa and sunflowers has resulted in more pesticide use, although the timing of the agricultural change was not precisely known.

In a follow up study the next winter (1995-96), Goldstein et al. (1996) recorded four major incidents of mortality with 4,100 dead hawks. Two incidents involved monocrotophos applications in alfalfa fields for grasshopper control (982 dead Swainson’s Hawks). In the third incident, 103 dead hawks were found after dimethoate was apparently sprayed on alfalfa for grasshopper control, although the presence of that OP was not confirmed chemically. In the largest incident, an estimated 3,024 hawks were killed after a 120 ha alfalfa field was sprayed with monocrotophos (Goldstein 1997). Canavelli et al. (1996) recorded at least 18 incidents (including those above) in 1995-96 for a total of 5,093 dead Swainson’s Hawks. Based on an extrapolation of the area searched for kills and assuming all kills were located in the searched area (an unlikely assumption which provides a conservative estimate), it was estimated that more than 20,000 Swainson’s Hawks died. Using an earlier world population estimate of 450,000 birds, Goldstein et al. (1996) estimated that pesticide-related mortality may well exceed 5% of the world’s population, 1% of which was recorded. More recent (1995 and 1996) Swainson’s Hawk fall counts in Veracruz, Mexico (at a migration bottleneck) provided estimates of 845,485 and 541,663 respectively (data base, Hawk Mountain Sanctuary). These counts were believed underestimates of total migrants (L. Goodrich pers. comm.) for two reasons: (1) only 2 counting sites were used, but migration corridor was about 30 km wide, and (2) some birds fly too high to observe. The flight lanes used and the altitude of the migration varies from year to year, therefore, year-to-year comparisons require caution and should not be made. However, the above percentage of the world population killed in Argentina in the winter of 1995-96 may be over-estimated, because of higher population counts.

Goldstein (1997) recorded the age (adult:juvenile) of dead hawks at four locations in Argentina (1464 birds aged, 266 not aged). Of those aged, hawks at two locations showed about a 50:50 ratio (42:39 and 165:163), while two locations strongly favoured adults (354:127 and 332:242). Woodbridge et al. (1995a) noted some wintering flocks dominated by adults. What should the age ratio be in the wintering population and can it be estimated with available data? Using a 22-year average of 1.91 young per successful nest in Canada (Houston and Schmutz 1995a) and the minimum failure rate (29.6%), the maximum number of young fledged per nesting attempt would be 1.34 young. Or, we could use the 10-year average of 1.53 young fledged per nesting attempt from California (Woodbridge et al. 1995b). If two adults produced 1.34 or 1.53 young, the age ratios at fledging would be 60:40 or 57:43. However, we know these adult ratios are biased low because: (1) not all adults breed, Schmutz et al. (unpublished ms., Univ. Saskatchewan, Saskatoon) reported in high prey years, the average age of first encountered breeding was 2.9 years, and (2) young after fledging do not survive as well as adults during their first few months of life. These biases all favor more adults in the population, therefore, the expected adult:juvenile ratio on the wintering grounds should be considerably higher. Although the overall ratio of dead hawks in Argentina was only slightly higher (61:39), age ratios from the four incidents varied considerably (74:26, 58:42, 52:48, and 50:50). The hawks probably died in ratios approximating their presence in various flocks. Although the age ratios of the dead hawks in Argentina do not seem different from the age ratios in the flocks, it should be noted that the normal mortality pattern for a long-lived raptor would be more age-specific and biased toward juveniles and subadults.

Banded hawks killed in Argentina were from throughout the breeding range in North America, although most came from Saskatchewan and Alberta (Woodbridge et al. 1995a, Goldstein 1997). More Swainson’s Hawks have been banded in the two prairie provinces of Canada than anywhere else in North America (Houston and Schmutz 1995b), therefore, the distribution of bands actually reflects banding effort. However, we believe the wintering population exposed to pesticides in Argentina represents the North American breeding population. Therefore, with several long-term Swainson’s Hawk breeding population studies underway, it was logical to review the data to evaluate possible population changes--especially following the winters of 1994-95, and 1995-96 when large numbers were killed in Argentina. The three longest series of Swainson’s Hawk population data include the Butte Valley, California study area of Woodbridge et al. (1995a) and the Saskatchewan and Alberta study areas of Houston and Schmutz (1995b) and Schmutz et al. (unpublished ms.). The Butte Valley population (after 1990) provided no evidence of a population decline, and new nesting territories seemed to appear in response to improved habitat conditions for Swainson’s Hawks, i.e., native fields converted to alfalfa (Woodbridge et al. 1995b). A detailed analysis of this long-term study may be particularly useful because most of the population is colour-marked and information about changes in annual survival of adults may become available.

Population densities were apparently healthy with reproduction consistently high in Saskatchewan and in southern Alberta through 1987 (Houston and Schmutz 1995a). Near Kindersley, Saskatchewan six consecutive years of declining populations began in 1988, while declines in production by 1991 were evident at Hanna, Alberta. However, Houston and Schmutz (1995a) noted that the decline in productivity was accompanied by a drastic decline in Richardson’s Ground Squirrels Spermophilus richardsonii which were the Swainson’s Hawks main prey. Schmutz et al. (unpublished ms.) concluded it was difficult to evaluate the potential impact of the poisoning on their study populations. They noted the declines in nesting success can be logically linked to changes on the study areas, but they were unable to discern whether the declines in numbers of breeders may be due to a combination of local prey declines and winter (pesticide) mortality. Prior to finding dead hawks in Argentina, population declines were reported in California, Nevada, and Oregon (see references in Woodbridge et al. 1995b) with various causal factors suggested.

Bald Eagles in British Columbia

Since 1991, the Canadian Wildlife Service has monitored causes of illness and death of Bald Eagles and selected other raptor species in the lower Fraser valley and south-east Vancouver Island. The project involves an organised call-in for sick, injured and dead birds, from which plasma and/or brain ChE activity is measured and those with inhibited levels have ingesta (where available) analysed for pesticide residues. Necropsys were completed on all carcasses to determine the most probable cause of death.

Many of the bald eagles collected came from the Fraser River delta, an area of intensive agricultural and high biological productivity which is used in winter by large numbers of waterfowl, raptors and other birds. Whereas the most common causes of death of Bald Eagles from other parts of B.C. were electrocution and trauma, pesticide poisoning was the most important cause in the delta. Here we examine the available data to determine if poisoning by anti-ChEs influenced the number of resident Bald Eagles nesting on the delta and/or migrant Bald Eagles wintering on the delta.

The process or mechanism by which eagles and other raptors were poisoned by anti-ChEs on the Fraser delta is somewhat unusual. The primary route of uptake is passive exposure of waterfowl to anti-ChE granules acquired while sifting sediments and crop residues in puddles or waterlogged soils in agricultural fields. This feeding and subsequent poisoning tends to occur in late fall and winter, several months after harvest and at least 6 months after pesticide application. In the soil and climatic conditions in the delta, the insecticides have unusual persistence (Wilson et al., 1996). Thus, both resident breeding and migrant wintering eagles were exposed while feeding on dead or debilitated waterfowl.

Christmas bird counts show that the number of Bald Eagles wintering in the Fraser delta increased dramatically since the 1970s, when less than 10 birds were observed to an average of about 300 counted since 1990. That increase probably reflects a general post-DDT recovery of Bald Eagle populations, possibly coupled with decreased options elsewhere for winter feeding (M. Porter et al. unpublished ms, Canadian Wildlife Service, Delta, B.C.). The numbers of Bald Eagles roosting at several sites in the delta were counted weekly during winters of 1994 to 1998. Numbers rose steeply through December and January at all roost sites, to peak in February. Most birds had left the area by early April. Increased densities in February coincided with timing of peak poisoning incidents; this suggests that the number of eagles present likely increases the chances of finding eagle carcasses. Prior to the winter of 1989-90 in the delta, despite many documented incidents of waterfowl poisonings, a few of which were accompanied by other raptors, there were no documented pesticide poisonings of Bald Eagles (Wilson et al., 1995). In the winter of 1989-90, the number of wintering eagles about doubled over the previous year and has remained at that level. That year, the first incidents of Bald Eagle poisoning by anti-ChEs were reported from the delta. (Elliott et al., 1996) Thus, the incidence of poisonings may reflect a larger number of wintering birds and increased scavenging pressure, although increased surveillance since that time also may have been a factor (Elliott et al., 1997).

From 1991 to 1997, an average of 5 to 10 Bald Eagles per year were diagnosed as anti-ChE-poisoned in the delta. This constitutes at most 5% (probably 2-3%) of the estimated wintering population. It was difficult to estimate what percentage of dead eagles were retrieved. Bald Eagles are large visible birds for which there is a high degree of public interest. The terrain in the delta comprises large areas of flat open fields in winter with considerable commercial and recreational activity on surrounding roads and dykes, so the percentage of carcasses recovered is undoubtedly higher than in most other parts of British Columbia. Regardless of the efficiency of the program at detecting dead eagles, i.e., the rate of poisoning, and number of eagles wintering on the delta remained stable.

The breeding population in the Fraser delta numbers about 30 to 36 eagles, or 15 to 18 breeding pairs. Mean productivity over the period 1993-97 averaged about 1.1 young/occupied territory, which indicates a healthy population (Elliott et al., 1998). Despite evidence of pesticide poisoning of local breeding birds (Elliott et al., 1997), the number of successful breeding territories increased over that period by about 30 %.

Changes in pesticide availability to local farmers have occurred because of the raptor poisonings. Two of the most toxic compounds, carbofuran and phorate, were voluntarily withdrawn from the local market by the manufacturers, while a third, fensulfothion, is no longer available in North America. Also, lead shot, shown to be a major cause of Bald Eagle deaths in British Columbia, was banned in 1990 for waterfowl hunting in the Fraser delta and surrounding areas (Elliott et al., 1992). Other improvements include changes of electrical transmission facilities to reduce electrocutions of bald eagles, another major cause of death. In addition, many birds poisoned by pesticides or lead have been brought to wildlife rehabilitation centres where they were treated, recovered and eventually released. Without removal of those major causes of death and the intervention of rehabilitators, it is possible that the wintering population could have sustained sufficient losses to reduce the number of birds.

The USEPA (1989) modelled a breeding Bald Eagle population that was exposed to carbofuran along the lower James River in Virginia. The Virginia situation was similar to British Columbia. Both study areas contained a wintering and a spring breeding population. The observed rate of secondary poisonings on the James River in 1985 may have been as high as 8.3% for birds of the year and 6.5% for older birds. EPA focused on the breeding population using the stochastic model of Grier (1980). Grier found that survival rate may be the more important factor affecting eagle populations. EPA concluded that at the rate of pesticide-related mortality observed in Virginia and under favourable survival and breeding conditions, the small breeding population of Bald Eagles on the lower James River could sustain itself, but may not increase. And, if less than the maximum breeding potential is achieved, or if other factors result in decreased survival below 90% annually for birds >1 year, the population of breeding birds will probably decrease, even if pesticide-induced mortality remains at or below 7%.

We found no evidence that poisoning by anti-ChEs significantly affected the long-term numbers of either wintering or breeding Bald Eagles in the Fraser River delta. This is likely in part because of the continent-wide increase in Bald Eagles and therefore recruits to the wintering population, and a high level of local production. However, we should stress that in the past eight years significant changes have occurred in pesticide usage, lead shot regulations and other factors which have significantly reduced Bald Eagle mortality from human activities.

In summary, we evaluated available data in an attempt to determine if anti-ChEs had an adverse effect on the long-term size of Swainson’s Hawk and Bald Eagle populations. No obvious population declines (at species level or regional level) were apparent that could be positively related to the pesticide mortality incidents. It is worth noting that the documented dead birds accounted for about 2-5% of the birds in the populations of concern in both examples. No procedure currently in operation, and probably no procedure that can be developed for raptors, can measure a 2-5% pesticide-related change in a normally fluctuating raptor population. Furthermore, other mortality factors may compensate for the pesticide-related loss. If the dead Swainson’s Hawks (estimated 20,000) were from a regional population of 40,000, instead of a species population of 540,000-845,000, the problem would have been extremely serious -- perhaps we were lucky this time. We have shown that under certain circumstances, large numbers of raptors can be killed by pesticides approved for use.

RECOMMENDATIONS FOR FUTURE RESEARCH AND MONITORING

The value of collecting and making data available on incidents is critical for the credibility of any pesticide regulatory system. Unfortunately, few jurisdictions are currently assembling this information, let alone providing the resources needed for adequate investigations. The biggest problem encountered by Mineau et al. (in press) in preparing their assessment was the lack of detail or completeness supplied with many incidents. An example of a valuable step forward is the training program on pesticide poisoning incidents now given to enforcement agents and other investigators of the U.S. Fish and Wildlife Service. Making investigators aware of the relevant questions has resulted in a net improvement in the data collected and the quality of the investigations.

Potentially the most valuable piece of information, but the one most often neglected, is a thorough analysis of the carcass gut contents. This is often a valuable indicator of what the bird ate immediately before it died. The other major improvement needed is to increase the number of birds routinely screened for ChE inhibitors. The number of birds found exposed (either lethally or sublethally) is dramatically higher in those situations where large numbers of birds coming into rehabilitation centres are assayed regardless of the initial diagnosis. The link between sublethal impairment and other ‘causes’ of mortality such as electrocution or impact strikes has been made often enough that this should be considered a possibility in any case investigation. Cholinesterase determinations are inexpensive and easy to perform. Automated analysis systems, field kits or improvements that allow the collection of blood on filter paper without need for refrigeration (Trudeau et al. 1995) puts the technique within easy reach for rehabilitation centres.

Basic issues seldom addressed with most raptor kills include: (1) what is the size of the population exposed, and does it represent a local or regional population, or the total species, and (2) how many individuals in the population were killed by insecticides? Attempts were made in this review with the Swainson’s Hawk and Bald Eagle to address the above basic issues which permits a preliminary evaluation in terms of populations and potential population effects. We believe large long-term research projects are necessary to fully address the ‘population effect’ issue.

Two points remain: (1) raptor mortality is preventable when less toxic alternative products are available, and only a few products and/or formulations were responsible for most of the problems, and (2) to ignore the continuing problem with currently-registered pesticides contradicts the effort and expense that groups of individuals in our society are willing to expend in order to rescue an rehabilitate individuals of those species.

ACKNOWLEDGMENTS

We wish to thank L. Goodrich, Hawk Mountain Sanctuary, for providing unpublished hawk migration data from Veracruz, Mexico. J. K. Schmutz, C. S. Houston, and S. J. Berry provided access to their unpublished manuscript and M. I. Goldstein provided a copy of his unpublished M.S. Thesis from Clemson University.

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Table 1. Summary of organophosphorus and carbamate pesticides implicated in U.S. raptor kills (1985-94) and subdivided into labelled use, abuse, spill or unknown use (adapted from Mineau et al. in press).

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Table 2. Species summary of organophosphorus and carbamate raptor kills in the United States, 1985-94 (adapted from Mineau et al. in press).

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