Ecotoxicology, 4, 281-298 (1995)

Effects of insecticide use on breeding birds in Christmas tree plantations in Quebec GUY RONDEAU

1'2 and J E A N - L U C

DESGRANGES

1.

1Environment Canada, Canadian Wildlife Service, PO Box 10100, Sainte-Foy, Quebec, G1V 4H5, Canada 2World Wildlife Fund, CH-196, Gland, Suisse Received 12 September 1994; accepted 10 January 1995

This research, which was carried out in the spring of 1989 and 1990 in seven balsam fir (Abies balsamea) plantations in southeastern Quebec, examines potential deleterious effects of three insecticides (i.e. dimethoate, diazinon and insecticidal soap) on breeding American Robins (Turdus migratorius) (n = 87 nests) and Song Sparrows (Melospizsa melodia) (n = 41 nests). Through analyses of blood serum cholinesterases (ACHE and BChE) activity both prior to and the second day following applications of the two organophosphorus insecticides, we showed that adult American Robins, Song Sparrows and Chipping Sparrows (Spizella passerina) breeding in the treated plantations were exposed to diazinon and dimethoate (p < 0.05). Signs of exposure to diazinon (p < 0.05) were also found in young American Robins. However, despite sharp reductions in blood ChE (and, in some cases, marked inhibition confirmed by 2-PAM reactivation), no cases of adult mortality were recorded following the treatments. Cases of complete or partial mortality were recorded in American Robin and Song Sparrow nests, even among control birds (non-exposed birds). No mortality was recorded for broods exposed to the insecticidal soap. Abandonment of nests and egg infertility were ruled out as possible causes of mortality. The cases of total mortality observed in American Robin and Song Sparrow broods exposed to dimethoate were similar to those recorded for control nests (18 and 25% compared to 14 and 21%, respectively). However, among American Robin and Song Sparrow nestlings exposed to diazinon, essentially twice as many cases of total mortality (31 and 38%, respectively) were recorded as for the control nests. It appears that American Robin eggs are sensitive to diazinon and dimethoate, particularly when spraying is carried out early in the incubation stage. In the case of the Song Sparrow, it is mainly the nestlings that succumb after diazinon is sprayed on them or when dimethoate applications are made during the egg stage.

Keywords: songbirds-reproductive success; Christmas tree plantations; cholinesterase-inhibiting pesticides

Introduction

In wooded areas, dimethoate and diazinon, two organophosphorus insecticides, are currently used in Christmas tree plantations. The application of these insecticides coincides with the nesting period of most of the bird species found in this specific type of plantation. Unlike the practice in public and private forests, where forest stands may *To whom correspondence should be addressed. 0963-9292 © 1995 Chapman & Hall

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be sprayed with pesticides only one to three times in their lifetime, Christmas tree cultivation calls for systematic yearly use of insecticides. Organophosphorus compounds are particularly toxic for birds (Stone 1979; Grue et al. 1983; Smith 1987) although they generally remain in the environment for shorter periods than organochlorines. Organophosphorus pesticides act on living organisms by reducing the activity of cholinesterase (ChE) in the blood and acetylcholinesterase (ACHE) in the brain. Accumulation of acetylcholine in nerve tissues causes a change in the transmission of nerve impulses in the synapses (Stone 1979). This leads to paralysis of the respiratory muscle and depression and paralysis of the respiratory centre (Murphy 1986). Living organisms can come into contact with organophosphorus insecticides through inhalation, ingestion or skin contact. Following acute oral exposure to an organophosphorus pesticide, an inhibition in the order of 80% of brain AChE activity causes death. In the case of continued exposure, an inhibition in the order of 40-50% in brain AChE activity is enough to cause death (Eisler 1986; Grue et al. 1991). In the case of diazinon, brain AChE measurements on 27 Canada Geese (Branta canadensis) found dead on turf sites gave values ranging from 49 to 89% inhibition (Frank et al. 1991). Organisms that survive inhibition of cholinesterase activity can recover fairly rapidly (Niethamer and Baskett 1983; Eisler 1986; Stromborg et al. 1988). Dimethoate is a systemic contact and residual insecticide and acaricide. The lethal dose is normally set at 280 mg kg -1 for the Ring-necked Pheasant (Phasianus colchicus) and 14mgkg -1 for the Mallard (Anas platyrhynchos) (Smith 1987). Although this pesticide is widely used and highly toxic to certain wildlife species, particularly birds (Schafer 1972), there seem to be no published reports indicating dimethroate as the causative agent in any wildlife die-offs (Smith 1987). Yet, Graham et al. (1990) report that a Quebec apple farmer found several American Goldfinch (Carduelis tristis) dead following dimethoate spraying in his orchard. Diazinon is an insecticide and acaricide with stomach-poison and contact activity. The lethal doses are normally set at 2.0 mg kg -1 for the Ring-necked Pheasant and 3.5 mg kg -1 for the Mallard (Smith 1987). The literature reports several cases of diazinon poisoning, particularly in waterfowls and passerines on turf (Stone 1979, 1980; Smith 1987; Frank et al. 1991; Drcarie et al. 1993). A Quebec Christmas tree producer has already reported mortality in the American Robin (Turdus migratorius) and Eastern Bluebird (Sialia sialis) following the application of diazinon (Rondeau and DesGranges 1991). Insecticidal soap is a contact insecticide occasionally used in Christmas tree plantations. Some of the fatty acids in this soap penetrate the bodies of insects causing the loss of cell contents. The result is that the insects quickly die on contact with this product. However, the insecticidal action of the soap disappears once the solution dries. This is a relatively new product and we know of no studies assessing its effects on birds. Based on the need to assess the effects of both diazinon and dimethoate on nesting birds, this study is basically a comparison aimed at (1) determining the level of exposure of birds to the products under study, (2) observing the extent of adult bird mortality and (3) assessing the consequences of these insecticides on the breeding success of broods following spraying with dimethoate and diazinon in Christmas tree plantations. To achieve this, various spraying scenarios were monitored to determine the effects of these organophosphorus insecticides at the concentrations and dates normally used in the cultivation of Christmas trees.

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Methodology Spraying scenarios and surveillance A number of harmful insect species are targeted by insecticide treatments in Christmas tree plantations. At the time of our study, the main targets were balsam twig aphids (Mindarus abietinus). The dimethoate formula used for spraying Christmas tree plantations is an emulsifiable concentrate sold under the trade name CYGON (480-ETM). The concentration of dimethoate in this formula is 480 g of active ingredient per litre. The diazinon formula used in Christmas tree plantations is sold under the trademark BASUDIN 500 E.C. This formula contains 500 g of active ingredient per litre of product. The concentration normally used for diazinon and dimethoate is 1.25 1 ha -1. Insecticidal soap (SAFER) was used by only one grower in the region. This product was in fact the only insecticide applied in his plantations in 1990, the year of our studies in his location. Insecticidal soap was applied in a 1% water solution (Safer Ltd, information folder). For this product to be effective, trees must be completely wet with the soap preparation. According to Mineau and Collins (1988), the observation of bird mortality due to the use of pesticides is the best indicator of the direct impact of spraying. Yet, as they recognized, a surveillance exercise is unlikely to be useful except under conditions of catastrophic impact on a large segment of the population. We therefore put in a significant effort in the field at looking for possible effects of these insecticides on the mortality of adults, eggs and nestlings. Breeding success (the hatching rate of the eggs and the survival rate of the young) is a good indicator of the effects of these pesticides since insecticide spraying coincides with the nesting period of the majority of bird species in this type of environment. In addition to the potential exposure to products through the food of adults and nestlings, eggs and nestlings may come into direct contact with insecticides at the time of spraying. Both Hoffman and Eastin (1981) and Grue et al. (1986) consider that embryos and young birds may be particularly sensitive to pesticides. The sublethal effects of exposure of birds to organophosphorus compounds can be assessed by analysis of cholinesterase inhibition. According to Hill and Fleming (1982), the measurement of inhibition of this enzyme is one of the best available methods to show the exposure of a subject to one of these insecticides. For each bird species under study and for each organophosphorus insecticide, we have matched up cholinesterase results for the period prior to spraying in a plantation and compared them to the results obtained in that plantation the second day (for security reasons) after the pesticide applications. In cases where plantations were sprayed twice, the effects were considered separately since spraying took place at 2-week intervals. Only two Robin nests were actually exposed to two treatments.

Sites and species studied The study was carried out in the springs of 1989 and 1990. The 17 study sites were all located in the Eastern townships, close to Sherbrooke, Quebec (45°25'N; 71°54'W) (Table 1). The minimum and maximum distances between any two plantations was 10 and 60 km, respectively. These were Christmas tree plantations several hectares in size. Most of the trees in the selected plantations had reached market size (from 1.50 to 2.10m high), giving a very homogeneous aspect to the whole set of study sites. No Christmas tree plantation in the townships could be used as a control site, since all growers contacted through the Quebec Christmas Tree Growers' Association used

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284 Table 1. Number of Christmas tree plantations involved in each treatment each year Treatments

1989

1990

Diazinon Dimethoate Safer

4 3 0

4 5 1

insecticides to combat destructive insects. To compensate for the lack of control plantations, we used broods that were fledged before spraying with insecticide. Since all spraying was not carried out at the same time, we were able to locate several early and late nests to use as adequate controls. Therefore, control and treated broods were equally represented throughout the sampling design (i.e. the 17 plantations and the two study periods), so that several control and treated broods coincided in time at different sites. This level of interspersion of the sampling design constitutes an acceptable safeguard against pseudoreplication (Fite et al. 1988). Furthermore, birds nesting in plantations exposed to insecticidal soap could be used as controls for the comparison of levels of cholinesterase activity inhibition, since this biological pesticide has no effect on the enzyme system. Further details regarding the study design are presented in Rondeau and DesGranges (1991). We chose the most common bird species nesting in the low shrub stratum and the herbaceous stratum to determine the effects of insecticides on nesting birds in Christmas tree plantations. Based on a search for old nests built in previous years and on information obtained from growers familiar with birds, we selected American Robin and Song Sparrow (Melospiza melodia). We also collected partial data on another abundant species, Chipping Sparrow (Spizella passerina), in order to compare exposure of this species, which builds its nest in trees, to that of Song Sparrow which nests mainly in the herbaceous stratum. Through systematic searches both on starting the project and throughout our subsequent movements about plantations, we found nests of American Robin and Song Sparrow.

Data collection The second day following application of the insecticides, we searched meticulously through plantations to find dead birds. This was done by tracing three 100 m 2 quadrants distributed systematically in each plantation and looking carefully for dead birds in and under each tree (i.e. 20-25) in every plot. In addition whenever we had to move about in the plantations, particular attention was paid to looking for dead birds. Every three days, we visited all of the nests under study to note the number of eggs or nestlings, their age, the presence of parents on the nest and the parents' behaviour. Cases of predation were also noted. These visits served to calculate the hatching and survival rates of chicks. The hatching rate is the ratio of the number of eggs hatched to the number of eggs laid while the survival rate is the number of nestlings fledged compared to the number of eggs hatched. The survival rate of chicks was assessed using nests that were monitored from the beginning of incubation until the nestlings could leave the nest. In this study, we found that, if disturbed, nestlings may leave the nest as early as 9 days old for the American Robin and 8 days old for the Song Sparrow. We

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minimized the time of visiting each nest as much as possible and spread the visits evenly across treatments to avoid disturbing the brood and risk having the parents abandon the nest. This also meant less risk that the location of the nest would be revealed to predators such as the American Crow (Corvus brachyrhynchos) which tended to watch our movements in the plantations from their perches. Predation usually occurred shortly after nest discovery, most often before the nest was even exposed to pesticide application. If a nest was predated, it was excluded from the calculations of brood productivity. However, in several cases, we were able to use it in calculating the hatching rate (if predation occurred after hatching). Individuals of the three species under study were captured in order to take the blood samples needed to determine inhibition of cholinesterase activity. The samples were taken the day before spraying and during the second day following applications. Birds were captured using Japanese nets set around the plantations, insofar as possible in parts of the plantations near those where the nests under study were located. In addition, several adult and young American Robins were captured right on the nest to take blood samples. In the case of captures of adults on the nest, these were made towards the end of brood development to avoid causing parents to leave the nest. The blood was taken from the jugular vein using a 50/A insulin syringe. Approximately 10 and 15/A of blood was taken from each Sparrow and American Robin individual, respectively. The blood was then transferred to three or four heparinated microcapillaries (2 USP), centrifuged and placed in a freezer at -80°C. In the case of young American Robins, whom we tried to sample when they were 8 days old (8.1 + 1.9), it proved easier to take the blood from the alar vein. The brains of captured birds were immediately removed by decapitating the bird and placing the whole head on dry ice while awaiting transfer to a freezer at -80°C. Analyses of ChE activity were made with the methodology used by Ellman et al. (1961) and modified by Hill and Fleming (1982) at the laboratory of the National Wildlife Research Centre (NWRC). For samples that showed a reduction in ChE activity, two cholinesterase reactivation tests (spontaneous reactivation and 2-PAM, cf. Martin et al. 1981) were performed to confirm whether there was actual inhibition, although a negative reactivity does not necessarily mean there is no inhibition (S. Kennedy, personal communication).

Statistical analyses We used descriptive statistics (frequency, mean, standard deviation, and coefficient of variation) to combine and classify information from brood monitoring and analyses of cholinesterase activity in the blood and brains. A series of non-parametric variance analyses (Mann-Whitney) comparing control data with treated data was used to compare both the results of analyses of cholinesterase activity obtained before and after applications of insecticides and the hatching and chick survival rates for different brood development periods. For each species and each insecticide, comparisons of cholinesterase activity were made between all control tissues and all treated tissues. Results

Exposure to insecticides A total of 219 blood and 69 brain samples were collected during two field seasons. Tables 2 and 3 give the mean values of ChE activity, the measurement of inhibition (expressed

Table 2. Comparison of blood serum cholinesterase (ACHE and BChE) activity in birds between

control samples and those sprayed with organophosphorus insecticide Species

Controls

Dimethoate

Diazinon

Adult Robin Mean ChE (,u 1-1) (+SD) Mean reduction (+SD) [n(treated-controls), p]

2708 -+ 1311 -

2009 + 762 26% -+ 28% (24-16, p = 0.05)

48% -+ 61%

Young Robin Mean ChE ~ 1-1) (__+SD) Mean reduction (+SD) [n(treated-controls), p]

1712 -+ 848 -

1116 _+ 542 35% _+ 32% (5-9, p = 0.18)

582 + 310 66% -+ 18% (13-9, p = 0.005)

4626 -+ 1652

3067 _+ 1226 34% -+ 27% (15-20, p = 0.003)

3363 _+ 1967 27% _+ 43% (29-20, p = 0.03)

Song Sparrow Mean ChE ~ 1-1) (+SD) Mean reduction (-+SD) [n(treated-controls), p] Chipping Sparrow Mean ChE ~ 1-1) (-SD) Mean reduction (-+so) [n(treated-controls), p]

3777 + 1131

1403 _+ 1660 (21-16, p = 0.0002)

2232 + 1041

2402 -+ 1747

41% _+ 28%

36% + 46%

(27-23, p = 0.0001)

(19-23, p = 0.003)

Significant decreases (p ~< 0.05) are shown in bold-face type. Table 3. Comparison of brain acetyl cholinesterase (ACHE) activity in birds between samples

sprayed with an organophosphorus insecticide and controls Species

Controls

Dimethoate

Diazinon

Adult Robin Mean AChE (u g-l) (_SD) Mean reduction (+SD) [n(treated-controls), p]

28.9 -+ 1.1 -

32.3 _+ 2.6 0% _+ 9% (3-3, p = 0.19)

26.3 _+ 6.4 9% -+ 22% (6-3, p = 0.25)

Young Robin Mean AChE (u g-l) (+SD) Mean reduction (+SD) [n(treated-controls), p]

-

9.5 (1-0)

7.5 -+ 1.2 (2-0)

Song Sparrow Mean AChE (p g-l) (_+SD) Mean reduction (-+SD) [n(treated-controls), p]

25.8 -+ 2.8 -

23.2 -+ 3.1 10% --+ 12% (4-5, p = 0.18)

23.2 + 3.1 10% + 12% (11-5, p = 0.07)

26.6 --+ 1.7

23.1 + 5.2 13% + 20% (14-6, p = 0.06)

23.2 + 4.1 13% + 16% (14-6, p = 0.05)

Chipping Sparrow Mean AChE (~ g-i) (-+SD) Mean reduction (-+so) [n(treated-controls), p]

Significant reductions (p ~< 0.05) are shown in bold.

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287

as %) of ChE activity after spraying and the results of analysis of variances between control samples (the day before spraying) and treated samples (the second day after spraying) for samples of blood and brain, respectively. Pooling of ChE data was done after an inspection of the data which revealed no statistical differences (ANOVA) either due to the sexes of the adult birds or the age of the young at the time of blood sampling (normally conducted around noon on clement weather days).

American Robin.

We noted a significant reduction in blood serum cholinesterase (ACHE and BChE) activity for adult American Robins exposed to dimethoate (Table 2). In this case, the mean reduction ws 26%. This decreased activity was not observed in the case of brains, where fewer samples were available, both for adults and for young birds (Table 3). Despite a 35% lower mean ChE activity in young robins exposed to dimethoate, no significant difference was measured between mean blood ChE activity of treated nestlings and those serving as controls (Table 2). The mean 35% reduction in ChE activity exceeds the level we had set for heavy spraying. Although a reactivation test was attempted on a treated blood sample with a particularly low level of ChE activity, the test was negative and we could thus not conclude with certainty that there had been exposure to an organophosphorus compound. Despite the high valuation in blood ChE activity observed in adult American Robins, we nevertheless observed a significant mean reduction, in the order of 48% for samples from individuals exposed to diazinon (Table 2). Reactivation of two samples of blood with very low levels of ChE activity compared to other treated samples was attempted. One of the samples confirmed an inhibition in the order of 50% while the other could not be reactivated. As in the case of dimethoate, we found no significant difference (p = 0.20) in brain AChE activity of adult robins that had been exposed to diazinon (Table 3). It should be noted, however, that only one sample could be reactivated, confirming a reduction of 45%. The variations in ChE activity observed in young American Robins were much lower than those observed in adults. We observed in these birds a significant mean reduction (66%) in ChE activity for blood samples from young robins exposed to diazinon (Table 2). Two brains from young American Robins exposed to diazinon were subjected to reactivation tests. Only one brain confirmed an AChE reduction in the order of 32%.

Song Sparrow. Variations in the blood ChE activity between Song Sparrows exposed to dimethoate are relatively slight compared to those measured in control birds or those exposed to diazinon (Table 2). Despite this, the reduction was quite pronounced in the case of samples of blood from individuals exposed to dimethoate at a mean of 34%. We attempted unsuccessfully to reactivate ChE in two samples exposed to this insecticide. As opposed to blood, we observed no significant difference in the brain AChE activity of this species (Table 3). No reactivation was attempted in this case. The variation in the measurement of the blood ChE activity of Song Sparrows exposed to diazinon was very high, although this did not prevent detection of a significant difference (p = 0.02) between control samples and those exposed to this insecticide. In this case, the mean reduction was in the order of 27% (Table 2). Three samples of treated blood were put to a reactivation test. Two of these showed considerable inhibition, one of 121%. It is interesting to note that in this particular case, despite such

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a great inhibition of ChE activity, the bird was still alive and showed no abnormal signs some 24 h after spraying. No significant difference in the levels of AChE activity between control brains and those treated with diazinon, was seen in exposed birds (Table 3). No reactivation tests were performed on brains from exposed Song Sparrows.

Chipping Sparrow. Although variations in blood ChE activity in Chipping Sparrows exposed to dimethoate were relatively small, they differed significantly between birds exposed to dimethoate and control Chipping Sparrows (Table 2). In this case, the mean reduction in ChE activity was 41%. Four samples of blood showing low ChE activity were put through reactivation tests without positive results. The mean levels of brain AChE activity showed an almost significant downward trend ( - 1 3 % on average) in exposed birds (Table 3). Reactivation tests were performed on two brains from birds found in plantations sprayed with dimethoate but it was not possible to demonstrate inhibition. Although variations in the blood ChE activity of birds exposed to diazinon were quite high, there was nevertheless a significant difference between the mean ChE activity in treated blood and control blood (Table 2). This difference was shown in a mean reduction in the order of 36% in the case of birds exposed to diazinon. No sample of blood from a Chipping Sparrow exposed to diazinon was subjected to reactivation tests. In this species, we did however find a significant difference ( - 1 3 % on average) between levels of brain AChE activity in Chipping Sparrows treated with diazinon and control brains (Table 3). Two brains were subjected to reactivation tests, but it proved impossible to reactivate them. Mortality of adult birds, eggs and nestlings. No trace of adult bird mortality was observed in systematic searches carried out in each plantation 24-48 h after spraying. Filming with video cameras confirmed that, for all nests observed (n = 83), the parents of both species were still alive and looking after their broods several days after spraying (Rondeau and DesGranges 1991). Although we cannot be certain that these were actually the same parents, since it is possible that a dead parent might be replaced, we doubt that this could happen in such a short period, at a time when nesting was already well advanced. A total of 131 American Robin nests and 70 Song Sparrow nests were monitored during this study. However, predation by American Crow, Racoon (Procyon lotor) and Red Fox (Vulpes vulpes) occurred throughout the nesting season and resulted in the complete loss of 41% of American Robin nests (controls 57%, dimethoate 5%, diazinon 8% and insecticidal soap 57%) and 53% of Song Sparrow nests (controls 52%. dimethoate 56%, diazinon 14% and insecticidal soap 0%). Broods predated at the feeding stage could still be considered in calculating the hatching rate. Table 4 summarizes brood mortality (i.e. that of eggs and nestlings combined) that could not be attributed to predation since dead eggs or young were still present in the nest. It is interesting to note that control broods of American Robin and Song Sparrow showed considerable 'natural' mortality which was often partial in the nest. It can be seen that the mortality observed for American Robin and Song Sparrow broods sprayed with dimethoate was similar to the 'natural' mortality calculated for control broods. However, in the case of American Robin and Song Sparrow broods exposed to diazinon, it can be seen that mortality in the nest was approximately twice that found in control broods.

289

Avian impact of tree plantation sprays Table 4. Mortality of eggs and nestlings observed in broods of American Robin and Song Sparrow by insecticide used Insecticide

American Robin

Song Sparrow

Natural mortality

14% (15 nests)

21% (9 nests)

Mortality with dimethoate

18% (41 nests)

20% (9 nests)

Mortality with diazinon

31% (24 nests)

38% (19 nests)

Mortality with insecticidal soap

O% (3 nests)

O% (1 nest)

Predated nests (i.e. showingpremature loss of entire clutch or brood) are excludedfrom calculations

Tables 5 and 6 show the mean hatching and survival rates of American Robin and Song Sparrow chicks, based on the stage of development of the brood at the time of spraying with insecticides. They describe all the broods monitored, whether these were the first broods started in early May or second broods hatched in mid-June. Given that the clutch size of the American Robin varies from the first to the second brood (Howard 1967, Morneau et al. 1990, 1995), we did not attempt to compare the mean numbers of eggs laid and hatched and the mean number of nestlings fledged. We instead assessed the extent of mortality in the nest and the time at which it occurred, comparing the mean hatching and survival rates of chicks between exposed and control broods. As both types of broods were equally represented throughout the study period (i.e. May and June), early (initiated before June 5) and late nests do not need to be analysed separately. Incidentally, there were no statistical differences in reproductive success between the 2 years of the study (Izl ~< 1.12, p > 0.27) as well as between early and late nests (Izl 0.88, p / > 0.38) for both the American Robin and Song Sparrow.

American Robin. The mean hatching rate and the mean survival rate of chicks calculated for all broods completed before spraying were used as control measurements to compare to those obtained for broods exposed to insecticides. These control broods had a mean hatching rate of 89% and a mean chick survival rate of 94% (Table 5). Mortality was generally seen to be low (14%) and occurred mainly in the egg stage (62%). When mortality (other than predation) occurred, it was always partial within a given brood. The mean hatching rate (]Z I = 0.46, p = 0.64) and the mean survival rate of broods (IZ] = 0.24, p = 0.81) of the American Robin exposed to dimethoate are similar to those of control broods (Table 5). However, when spraying with dimethoate took place at the beginning of incubation (up to the third day), the mean hatching rate was significantly lower than that of broods sprayed towards the end of incubation (Izl = 2.81, p = 0.05). The mortality observed in broods sprayed with dimethoate early in

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Table 5. Relations between treatments and nesting parameters in American Robins Treatment

Perioda

Mean number of eggs laid ± SD(n)

Mean number of eggs hatched

Mean number of nestlings fledged

Hatching rate

g ± SD (n)

~ ± SD (n)

%(n)

Control

5

3.6 + 0.4 (37)

3.3 ___0.8 (18)

3.2 + 0.9 (15)

Dimethoate

0 1 2 3 4 0-4

3.5 3.8 3.7 3.6 3.0 3.7

3.5 2.0 3.5 3.3 3.0 3.1

3.5 1.7 3.4 3.1 2.5 3.0

Diazinon

0

3.2 + 1.2 (5)

1.3 + 1.2 (3)

1.3 + 1.2 (3)

1

3.0 + 1.2 (4)

1.8 + 1.8 (4)

1.8 + 1.8 (4)

58 (4)

2 3 4 0-4

3.8 3.8 4.0 3.6

_+ 0.4 ± 0.4 ± 0.0 + 0.8

2.7 3.1 2.5 2.5

2.7 2.7 2.5 2.3

70 82 63 74

0 2 3 4 0-4

4.0 3.3 4.0 3.5 3.6

(1) + 0.5 (3) (1) + 0.5 (2) + 0.5 (7)

Safer

+ + + + + +

0.5 0.4 0.4 0.5 0.0 0.5

(4) (8) (19) (11) (2) (44)

(6) (9) (2) (26)

+ + + + + +

± + + +

0.5 1.5 0.7 0.8 0.0 1.0

1.4 1.1 0.5 1.4

(2) (8) (19) (11) (2) (42)

(6) (9) (2) (24)

4.0 (1) 3.5 + 0.5 (2) 3.7 + 0.5 (3)

+ + + + + +

0.5 1.4 0.7 1.0 0.5 1.1

+ 1.4 + 1.1 ± 0.5 _+ 1.4

(2) (7) (19) (11) (2) (41)

(6) (9) (2) (24)

4.0 (1) 3.5 + 0.5 (2) 3.7 + 0.5 (3)

89 (18) 100 (2) 46 (7) 93 (19) 90 (11) 100 (2) 85 (42) 50 (3) (6) (9) (2) (24)

100 (1) 100 (2) 100 (3)

aPeriod 0 from start to end of laying; period 1, from start up to 3 days of incubation; period 2, from 4 to 12 days of incubation; period 3, from hatching up to 7 days of growth; period 4, from 8 days of growth to fledging; period 5, breeding success of nests used as controls since they were sprayed after tiedging of the young.

incubation was partial (in a given brood) in a proportion of 57% while it was total in 29% of all broods. None of the nestlings hatched from eggs sprayed with dimethoate died before 'fledging age', determined at 9 days. Overall, the mean hatching rate was significantly lower for broods exposed to diazinon than for control broods (IZ[ = 2.13, p = 0.03) (Table 5). This was mainly due to the low mean hatching rates observed when spraying was done during egg laying or early in the incubation of eggs (50 and 58%, respectively). The mean hatching rate for eggs exposed during laying was significantly lower than that calculated for control broods ([Z I = 2.53, p = 0.01). In this case, the mortality of the eggs was mainly partial (67% of broods). No mortality was observed in nestlings when spraying was done at the egg stage. Only three broods of the Amerian Robin were found in plantations sprayed with insecticidal soap. These three broods showed no losses following spraying with insecticidal soap (Table 5).

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Table 5 (continued) Chick survival rate

Mortality since egg laying

% (n)

% (n)

Stage at which mortality occurs % Eggs

Nestlings

94 (15)

14 (15)

62

100 (2) 100 (7) 99 (19) 94 (11) 83 (2) 97 (41)

0 (2) 54 (7) 8 (19) 15 (11) 17 (2) 18 (41)

100 83 67 0 85

-

100 (3) 100 (4) 100 (6) 86 (9) 100 (2) 94 (24)

50 42 30 29 0 31

100 (1) 100 (2) 100 (3)

(3) (4) (6) (9) (24)

0 (1) 0 (2) 0 (3)

Type of mortality % None

Partial

Total

38

60

40

0

0 17 33 100 15

100 14 68 64 50 58

0 57 32 36 50 37

0 29 0 0 0 5

100 100 100 60 85

0 0 0 40 15

0 50 50 33 100 41

67 0 33 67 0 42

33 50 17 0 0 17

-

-

100 100 100

0 0 0

0 0 0

Song Sparrow. The mean hatching rate of control broods of Song Sparrow was 82% while the mean survival rate of chicks was 97% (Table 6). Mortality (21%) was seen only in a few broods, in which case it was normally total in any given nest. Overall, there was no noteworthy difference between the mean hatching rates ([Z[ = 0.21, p = 0.83) and the mean chick survival rates ([ZI = 0.84, p = 0.40) in control broods and those sprayed with dimethoate (Table 6). We did, however, note lower mean hatching (Izl = 1.62, p = 0.10) and chick survival rates (Izl -- 2.04, p = 0.04) when spraying took place during egg laying or towards the end of incubation. No mortality was observed for any of the four broods sprayed early in incubation. Although it was the eggs that were sprayed, it was mainly nestlings which died (in proportions of 40 and 67%, respectively). This mortality was only partial in the majority of cases where it occurred. This situation differs from that observed for the American Robin. There was no significant difference between the mean rates of hatching ([Z[ = 0.71, p = 0.48) and survival of chicks ([Z[ = 0.76, p = 0.45) in control Song Sparrow broods and those sprayed with diazinon (Table 6). A high degree of nestling mortality (47%) was, however, observed following spraying at the feeding stage. This mortality was total for two of the four broods where this occurred. We also observed high mortality when

Rondeau and Desgranges

292

Table 6. Relations between treatments and nesting parameters in Song Sparrow Treatment

Period a

Mean number of eggs laid

Mean number of eggs hatched

Mean number of nestlings fledged

Hatching rate

.f _ SD(n)

.~ --+ SD (n)

.f + SD (n)

%(n)

Control

5

4.6 + 0.7 (21)

3.6 + 1.8 (12)

3.4 + 1.9 (9)

Dimethoate

0 1 2 3 0-3

4.9 5.0 4.3 4.0 4.7

(16)

3.7 5.0 3.7 4.0 4.2

+ 1.2 + 0.0 + 0.5 (1) + 0.9

2.0 5.0 2.5 4.0 3.7

0

4.0 (1)

1

4.0 (1)

2 3 0-3

4.8 + 0.5 (16) 4.7 + 0.4 (4) 4.7 + 0.5 (22)

4.0 4.0 4.7 4.1

(1) + 1.7 (14) + 0.4 (4) + 1.5 (19)

3

4.0 (1)

4.0 (1)

Diazinon

Safer

+ 0.3 + 0.0 + 0.5 (1) + 0.4

(8) (4) (3)

(3) (4) (3) (11)

+ 0.0 + 0.0 + 1.5 (1) + 1.5

(2) (4) (2) (9)

4.0 (1)

82 (12) 66 100 88 100 90

(2) (4) (2) (1) (9)

3.0 + 1.8 (14) 2.5 + 2.5 (4) 2.9 + 2.0 (19)

100 (1) 84 (14) 100 (4) 88 (19)

4.0 (1)

100 (1)

aPeriod O from start to end of laying; period 1, from start up to 3 days of incubation; period 2, from 4 to 11 days of incubation; period 3, from hatching up to fledging;period 4, breeding success of nests used as controls since they were sprayed after fledging of the young. spraying was done towards the end of incubation (37%). In this case, it was mainly nestlings that died when they had been exposed to the insecticide in the egg stage. Only one sprayed Song Sparrow nest was found. No mortality was reported for this brood, which had been sprayed during the feeding stage (Table 6). It should be emphasized that, for broods exposed to spraying of all three insecticides during the feeding stage, the mean hatching rates were 100%.

Discussion Nesting birds in Christmas tree plantations are exposed to the organophosphorus insecticides used in these plantations. Despite significant reductions in blood ChE activity (and in some cases marked inhibition of the enzyme confirmed by P2AM reactivation), we observed no mortality in adult birds. However, our observations tended to show that broods of these birds were particularly sensitive to these products. Analysis of the level of ChE activity in the blood of birds proved to be very reliable in determining exposure to an organophosphorus compound and assessing its intensity. As observed in another study on organophosphorus insecticides (D6carie et al. 1993), the same cannot be said for analyses of brain A C h E activity. Major inhibitions of blood ChE found in certain American Robin and Chipping Sparrow individuals are not reflected in the brain A C h E of these individuals. According to Niethamer and Baskett

Avian impact of tree plantation sprays

293

Table 6 (continued) Chick survival rate

Mortality since egg laying

% (n)

% (n)

Eggs

97 (9)

21 (9)

88

66 (2) 100 (4) 71 (2) 100 (1) 89 (9)

56 (2) 0 (4) 38 (2) 0 (1) 20 (9)

60 33 50

100 (1) 75 (14) 53 (4) 71 (19)

0 (1) 37 (14) 47 (4) 38 (19)

44 0 32

-

-

l o o (1)

o (1)

Stage at which mortality occurs % Nestlings

Type of mortality % None

Partial

Total

12

67

11

22

40

50

100 100 50 100 67

0 0 50 0 33

0 0 0 0 0

56 100 68

100 43 50 48

0 36 0 26

0 21 50 26

-

lOO

o

o

67 -

(1983) and Custer and Mitchell (1987), it takes longer for the effect of organophosphorus insecticides to be observed in the brain than in the blood. This is why, in the second field season, we waited to the second day after spraying instead of the following day, without, however, noting any significant effect in brains. A wait of 2 days after spraying may be too short to allow the product to have an effect on the brains of species monitored. Nevertheless and to make things more complicated, it should be borne in mind that the level of ChE activity in birds recovers fairly rapidly once exposure has ceased (Niethamer and Baskett 1983; Eisler 1986; Stromborg et al. 1988). We are of the opinion that monitoring blood ChE activity is a good way of determining exposure to inhibitors of that enzyme. In addition, use of this tissue does not require the subject to be killed. Despite the high daily and age variation in ChE activity in nestlings (Thompson 1991), our observations nevertheless showed significant reductions in ChE activity in the blood of American Robin chicks exposed to diazinon. It is likely that the main means of exposure to the pesticides responsible for reductions in ChE activity observed in adult birds and nestlings are associated with the inhalation, ingestion and dermal contact with these products. We found traces of organophosphorus compound in the digestive tubes of adult Chipping Sparrows and Song Sparrow nestlings (Rondeau and DesGranges 1991). However, no traces of these organophosphorus insecticides were detected in the digestive tubes of American Robins (adults and nestlings) sacrificed the day following applications. The fact that we found no traces in the digestive tubes of robins might mean that this species normally does not eat prey exposed to pesticides. LaboratOry studies by Bennett (1989) showed that birds may

294

Rondeau and Desgranges

develop an aversion for food contaminated by pesticides. It is possible that reductions in ChE activity may also upset birds enough to prevent them from seeking food or affect their appetite until their ChE activity recovers, at a time when contaminated prey may no longer be available. D6carie et al. (1993) observed that nesting American Robins exposed to diazinon in urban areas made less feeding flights and that production was decreased. Coderre, in Morneau et al. (1990), demonstrated that the number and the total biomass of earthworms decreased following repeated applications of chlorpyrifos and lawn herbicides. Using remote sensing and video observations, we observed that parents left the nest temporarily during spraying (Rondeau and DesGranges 1991). It is thus possible that both eggs and nestlings came into direct contact with the insecticide at the time of spraying. Analysis of the blood ChE of young robins supported this hypothesis. In the case of eggs, another possible means of contamination would be internally, by the mother who may have been exposed to these products just before laying. In addition to direct contact during spraying, nestlings may be exposed to pesticides by ingesting contaminated food brought by their parents and as was shown in the analysis of residues in a pool of stomach contents of Song Sparrow nestlings (Rondeau and DesGranges 1991). There is a level of mortality in control broods which we have termed 'natural'. This mortality is often seen to be partial in a given nest as opposed to reports by Kemper and Taylor (1981) that, when mortality occurs in a brood of American Robin, it is normally complete. As we have just seen, this may not exclude the fact that control birds may have been exposed to other products either before nesting or during their search for food outside the plantations. In the tree-farming sites where the study took place, this background phenomenon is part of a situation beyond our control and it must necessarily be taken into consideration. The mortality observed in broods of American Robin and Song Sparrow cannot be explained just by abandonment of nests. Contrary to observations by Busby et al. (1990) with nesting populations of White-throated Sparrow (Zonotrichia albicollis) sprayed with fenitrothion, we observed no cases of nest abandonment except in one case where spraying machinery practically ran over a Song Sparrow nest built on the ground. Given the large number of cases where mortality was only partial, we are convinced that abandoning the nest contributes very little to the high rate of mortality observed in a number of broods exposed to insecticides. In addition, our data shows that almost all unhatched eggs (treated and controls) were fertilized, suggesting that the partial mortality normally seen in nests cannot be due to greater sterility of eggs. The mortality observed following spraying with diazinon was approximately double the so-called 'natural' mortality observed in control broods. For the two species under study, high mortality rates were recorded following applications of dimethoate, with the extent of losses depending on the stage of development of eggs (both in the oviduct and in the nest) or young birds. Patnode and White (1991) and Kilbride et al. (1992) also reported significant differences in egg and nesting success among various pesticides applications. American Robin embryos seem vulnerable to the two organophosphorus insecticides studied and losses were much heavier when spraying took place during egg laying or early incubation in the case of diazinon or at the beginning of incubation in the case of dimethoate. In many cases (sometimes partially in a given brood), exposed eggs failed

Avian impact of tree plantation sprays

295

to hatch. However, the eggs of American Robin, which were exposed and yet survived, normally showed no problems at the chick stage. This suggests that the affected eggs must have been directly exposed to the spraying itself or been in contact with the soiled plumage of females. Although nestlings may be exposed indirectly to these products by ingesting contaminated prey, this must not be a common occurrence since American Robins appear to seek food for their young mainly outside plantations (Rondeau and DesGranges 1991). Johnson et al. (1976) reported that American Robins nesting in orchards sought food mainly outside the orchard. With respect to the Song Sparrow, the nestlings were the main victims of the applications of the organophosphorus insecticides studied. In the case of diazinon, it was exposed chicks which died (totally in a given nest) while for dimethoate, it was both eggs (partially in a given nest) and chicks exposed at the egg stage which failed to mature. As opposed to American Robins, nesting Song Sparrows mainly seek prey for their chicks right in the Christmas tree plantation (Rondeau and DesGranges 1991). Mortality in Song Sparrow broods thus seems to be due both to direct contact of the eggs with dimethoate and to indirect poisoning by eating food contaminated with diazinon. This study did not look at the survival rate of juveniles that had left the nest. However, Stromborg et al. (1988) conclude that the effects of organophosphorus treatment in the nest on European Starling (Sturnus vulgaris) nestlings do not extend to those that survived and left the nest. A number of effects on bird behaviour were linked to exposure to organophosphorus compounds. The main effects were a reduction in singing (Grue and Shipley 1981), decreased vigilance (Levin and Rodnitzky 1976) and disturbance of nesting behaviour (Grue et al. 1982) and feeding behaviour (Adams 1977). Behavioural changes seen following spraying, although noteworthy, do not appear to have been directly responsible for the mortality observed in certain broods (Rondeau and DesGranges 1991). These behavioural changes, which resulted in less prey being brought to nestlings in some broods of American Robin and by the increased presence on the nest for some Song Sparrows nesting in plantations sprayed with dimethoate, suggest that nesting birds are exposed for a much longer period than the actual time of spraying. According to Smith (1987), diazinon is moderately persistant (i.e. half-lives in soil are approximately 4-6 weeks) while dimethoate has a relatively short (half-lives in soil less than 5 days) environmental persistence. The systematic action of dimethoate (and to a lesser extent diazinon) means that the product remains for some time in the ecosystem and thus causes continued exposure through ingestion of contaminated prey or by skin contact. The fact that we observed mortality in Song Sparrow nestlings exposed to dimethoate in the egg stage supports our hypothesis that adult Song Sparrows sought food in the sprayed plantation and that dimethoate is active in the ecosystem for several days after application. Despite the fact that some American Robins might bring less food to their nestlings after heavy organophosphorus spraying, this has no major impact on broods since the mortality observed was mainly on eggs. The same was true for Song Sparrows which, after heavy spraying with dimethoate, spent more time on the nest, while still bringing more food to their nestlings. We are of the opinion that, as currently applied (dates and doses), diazinon is particularly toxic for birds in Christmas tree plantations. We effectively observed mortality up to twice as high in broods of the American Robin and Song Sparrow exposed to this insecticide. The insecticide itself, whether by direct contact or by

296

Rondeau and Desgranges

indirect contact through eating contaminated food, seems to be directly responsible, since changes in nesting behaviour, although observed, do not appear to contribute significantly to this abnormally high mortality.

Acknowledgements We wish to thank the Quebec Christmas Tree Growers Association Inc. for having agreed to participate in this study. We would also like to express our appreciation to the growers who allowed us to use their plantations: Rral Beloin, Daniel Cr~te, Larry Downey, Sam Harbinson, BenoR Labbr, Jocelyn Lavertu and Serge Vaillancourt. We thank Environment Canada's Sean Kennedy and Suzanne Trudeau for having carried out the cholinesterase analysis and Bernard Tardif for his help with the statistical analysis. Thanks go also to Pierre Leclerc and Sylvain Loranger (l~co-gestion en Ressources Renouvelables Inc.) and Pierre Mineau (CWS-NWRC) for their helpful suggestions and comments on this report. We should also mention the fact that this study could not have been carried out without financial assistance from the Canadian Wildlife Service and the 'PestFund' (Environment Canada and WWF-Canada).

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Service, Quebec Region, Sainte Foy. Grue, C.E. and Shipley, B.K. (1981) Interpreting population estimates of birds following pesticide application-behavior of male starlings to an organophosphate pesticide. Stud. Avian. Biol. 6, 292-6. Grue, C.E., Powell, G.V.N. and McChesney, M.J. (1982) Care of nestlings by wild female starlings exposed to an organophosphate pesticide. J. Appl. Ecol. 19, 327-35.

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Grue, C.E., Fleming, W.J., Busby, D.G. and Hill, E.F. (1983) Assessing hazards of organophosphate pesticides to wildlife. Trans. North Am. Wildlife Nat. Res. Conf. 48, 200-20. Grue, C.E., De Weese, L.R., Mineau, P., Swanson, G.A., Foster, J.R., Arnold, P.M., Huckins, J.N., Sheenan, P.J., Marshall, W.K., Ludden, A.P. (1986) Potential impacts of agricultural chemicals on waterfowl and other wildlife inhabiting prairie wetlands: an evaluation of research needs and approaches. Trans. North Am. Wildlife Nat. Res. Conf. 51,357-83. Grue, C.E., Hart, A.D.M. and Mineau, P. (1991) Biological consequences of depressed brain cholinesterase activity in vertebrates. In Mineau, P. ed. Cholinesterase inhibiting insecticides - their impact on wildlife and the environment, pp. 151-209. Amsterdam: Elsevier. Hill, E.F. and Fleming, W.J. (1982) Acetylcholinesterase poisoning of birds: field monitoring and diagnosis of acute poisoning. Environ. Toxicol. Chem. 1, 27-38. Hoffman, D.J. and Eastin, W.C. (1981) Effects of malathion, diazinon and parathion on mallard embryo development and cholinesterase activity. Environ. Res. 26, 472-85. Howard, D. (1967) Variation in the breeding season and clutch-size of the Robin in the Northeastern United States and the Maritime Provinces of Canada. Wilson Bull. 79, 432-40. Johnson, E.V., Mark, G.L. and Thompson, D.Q. (1976) The effects of orchard pesticide applications on breeding robins. Wilson Bull. 88, 16-35. Kemper, L. and Taylor, M. (1981) Seasonal reproductive changes in the American Robin (Turdus migratorius L.) of the Pacific Northwest. Can. J. Zool. 59, 212-17. Kilbride, K.M., Crawford, J.A. and Williams, B.A. (1992) Response of female California Quail (Callipepla californica) to methyl parathion treatment of their home ranges during the nesting period. Environ. Toxicol. Chem. 11, 1337-43. Levin, H.S. and Rodnitzky, R.L. (1976) Behavioral effects of organophosphate pesticides in man. Clin. Toxicol. 9, 391-405. Martin, A.D., Norman, G., Stanley, P.I. and Westlake, G.E. (1981) Use of reactivation techniques for the differential diagnosis of organophosphorus and carbamate pesticide poisoning of birds. Bull. Environ. Contam. Toxicol. 26, 775-80. Mineau, P. and Collins, B.T. (1988) Avian mortality in agroecosystems. II. Methods of detection. In Greaves, M.P., Greig-Smith, P.W. and Smith, B.D. eds. Field methods for the study of environmental impacts of pesticides, pp. 13-28. Thornton Heath, UK: British Crop Protection Council, Monograph No. 40. Morneau, F., D6carie, R. and DesGranges, J.L. (1990) Effets du Traitement des Arbres Ornementaux au Diazinon (BASUD1N) et ~ l'Acdphate (ORTHENE) sur le Merle d'Amdrique (Turdus migratorius) en Milieu Urbain. GRI~BE Inc. for Environment Canada, Terchnical Report Series no. 104, Canadian Wildlife Service, Quebec Region, Sainte Foy. Morneau, F., LEpine, C., D6carie, R., Villard, M.A. and DesGranges, J.L. (1995) Reproduction of American Robin (Turdus migratorius) in a suburban environment. Landscape Urban Plan. in press. Murphy, S.D. (1986) Toxic effects of pesticides. In Klaassen, C.D., Amdur, M.O. and Doull, J. eds. Casarett and Doull's toxicology: the basic science of poisons, pp. 519-81. New York: Macmillan. Niethamer, K.R. and Baskett, T.S. (1983) Cholinesterase inhibition of birds inhabiting wheat fields treated with methyl parathion and toxaphene. Arch. Environ. Toxicol. Chem. 12, 471-5. Patnode, K.A. and White, D.H. (1991) Effects of pesticides on songbird productivity in conjunction with peacan cultivation in southern Georgia: a multiple exposure experimental design. Environ. Toxicol. Chem. 10, 1479-87. Rondeau, G. and DesGranges, J.L. (1991) Effets des arrosages du Diazinon (BASUDIN), du Dimethoate (CYGON) et du Savon Insecticide (SAFER TM) sur la Faune Avienne dans les Plantations de Sapins de Noel. l~co-gestion en Ressources Renouvelables Inc. for Environment Canada, Technical Report Series No. 141, Canadian Wildlife Service, Quebec Region Sainte For.

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Schafer, E.W. (1972) The acute oral toxicity of 369 pesticidal, pharmaceutical, and other chemicals to wild birds. Toxicol Appl. Pharmacol. 21,315-30. Smith, G.J. (1987) Pesticide use and toxicology in relation to wildlife: organophosphorus and carbonate compounds. US Fish Wildlife Serv. Resour. Publ. 170. 171. Stone, W.B. (1979) Poisoning of wild birds by organophosphate and carbamate pesticides. N Y Fish and Game J. 26, 37-47. Stone, W.B. (1980) Bird deaths caused by pesticides used on turfgrass. N Y State Turfgrass Conf. Proc. 4, 58-64. Stromborg, K.L., Grue, C.E., Nichols, J.D., Hepp, G.R., Hines, J.E. and Bourne, H.C. (1988) Postfledging survival of European starlings exposed as nestlings to an organophosphorus insecticide. Ecology 69, 590-601. Thompson, H.E. (1991) Serum "B" esterases as indicators of exposure to pesticides. In Mineau, P. ed. Cholinesterase inhibiting insecticides - their impact on wildlife and the environment, pp. 109-25. Amsterdam: Elsevier.

Effects of insecticide use on breeding birds in Christmas tree plantations in Quebec.

: This research, which was carried out in the spring of 1989 and 1990 in seven balsam fir (Abies balsamea) plantations in southeastern Quebec, examine...
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