PESTICIDES 967
phorate are acutely toxic to birds but their use patterns are
such that damage to bird populations has not been extensive.
Thin eggshell syndrome Drastic reductions in the pop-
ulations of North American and European raptorial birds
such as the peregrine falcon, ( Falco peregrinus ), sparrow-
hawk ( Accipiter niger ), kestrel ( Falco tinnuncujlus ), osprey
( Pandion haliaetus ), bald eagle ( Haeliaetus leucocephalus ),
and golden eagle ( Aquila chrysactos ) have been observed
during the past 2 decades and these population declines
coincided with the period of large scale use of DDT and
other chlorinated organic insecticides. Although the com-
plex reasons for these population declines are highly con-
troversial, there is ample evidence that reproductive failure
is a major factor (Pimentel, 1971). Egg shell fragility or thin
egg shells is the most common cause and on Anacapa Island
of California, where the complete reproductive failure of
the brown pelican ( Pelecanus occidentalis ) was observed,
egg shells were found to average 0.38 mm in thickness, or a
decrease of 34% over normal (0.57 mm). Residues of DDT
and DDE as high as 1200 ppm (85% DDE) were found and
the fat of the adult birds, contained from 738–2603 ppm
DDT and DDE (Pimentel 1971). A similar effect has been
shown for the Scottish golden eagle where egg shell thick-
ness has declined from an index of 3.146 over the period
of 1848–1946, to 2.839 during 1951–1965, or a decrease
of 9.9% (Ratcliffe, 1970). Bald eagle eggshells in Florida
declined in weight from an average of 12.15 g in the pre-
DDT era to 9.96g in 1947–1962 or an 18% decrease, and this
has been associated with a decline in the eagle population in
Florida (Pimentel, 1971) although other factors must also be
considered.
Laboratory experiments summarized by Pimentel (1971)
show that feeding DDE to mallard ducks at 40 ppm induced
a 14% decrease in eggshell thickness and in cracking of
eggs. Eggshell thinning occurred at DDE levels as low as 10
ppm and duckling production per hen was reduced as much
as 75% when these levels of DDE were fed. DDT was less
effective in producing the thin-eggshell effect than DDE
although this occurred in coturnix fed DDT at 10 ppm and
25 ppm.
After the cancellation of registrations of DDT in 1973,
the average body concentration in the lake trout of Lake
Michigan declined from 19.2 ppm in 1970 to 2.2 ppm in- However, the cancellation of aldrin and dieldrin reg-
istrations in 1974 had little effect on the average body con-
centration of dieldrin in lake trout, which was 0.27 ppm in
1970 and 0.38 in 1984. There has also been a decrease in
the residues of DDT in herring gull eggs from 33.4 ppm
in 1986 to 7.1 ppm in 1986, and in dieldrin residues from
0.82 ppm in 1976 to 0.28 in 1986 (Council Environ. Qual.
1987).
Methylmercury Fungicides These compounds, especially
Panogen (® or methylmercury dicyandiamide, have been very
widely used as fungicidal treatments for small grains. In
Sweden, as much as 80% of the spring wheat sown from
1940–1965 was treated with such alkylmercury fungicides.
As a result, mercury became very widely distributed in wild
birds. Borg et al. (1966) studied the mercury content of the
livers of seed eating birds, pheasants, partridges, pigeons,
finches, and so on, which were found dead. Of 253 birds
investigated, 48% had Hg levels above 2 ppm and 20% above
10 ppm. There was a remarkable increase in the incidence of
high levels of Hg in these bird livers during May–June and
October–November, which related to the planting of seed
dressed with alkylmercury fungicides during these months
(Borg et al., 1968). When pheasants were fed wheat treated
with 20 ppm methylmercury dicyandiamide, a normal rate of
agricultural use, the eggs had reduced hatchability with Hg
residues of 1.3−2.0 ppm and the birds died in 29−61 days
with liver residues of Hg ranging from 30 to 130 ppm. Wild
pheasants and partridge eggs in Sweden contained about 30
ppm Hg (Borg et al., 1966).
Predatory birds, hawks, falcons, eagles, and owls were
also examined for Hg content of the liver. Of a total of 412
predators found dead, shot, or trapped for examination, 62%
had Hg levels above 2 ppm and 19% above 10 ppm (Borg
et al., 1966).
The methylmercury readily entered food chains and it
was found that hens in Sweden fed grain grown from wheat
whose seed was treated with alkylmercury fungicides pro-
duced eggs abnormally contaminated with Hg. Swedish
eggs on the open market, 1964–1966, averaged 0.029 ppm
Hg as compared with 0.007 ppm Hg in eggs on the market
in Continental Europe (Westöö, 1969). Thus a daily con-
sumption of two Swedish eggs could exceed the FAOWHO
recommended safe level for Hg intake of 0.00005 mg per
kg body weight. As a result of the wildlife contamination
and the dietary egg problem, alkylmercury fungicides were
banned in Sweden on February 1, 1966. Subsequently, the
Hg contents of Swedish hens’ eggs decreased to an average
of 0.009 ppm by September 1967 (Westöö, 1969).Pesticides and BeesThe honeybee Apis mellifera is not only an important domes-
ticated animal producing honey and bees wax valued at $50
million annually in the U.S., but also is the primary agent
responsible for the pollination of fruit, vegetable, and field
crops valued in excess of $12 billion annually. As represen-
tative insects, bees are highly susceptible to insecticides and
are a prime non-target victim of pesticides applied during
blossom time when the bees’ foraging patterns take them
to sprayed orchards and field; or from pesticides carefully
applied near apiaries. As an example of the damage that
insect control programs can do to bee colonies, the repeated
application of carbaryl to cotton in the Imperial Valley of
California as part of an eradication program for the pink
boolworm Pectinophora gossypiella, is estimated to have
killed 30,000 colonies of bees in 1967.
Anderson and Atkins (1968) have classified the toxic-
ity of pesticides to the honeybee Apis mellifera in groups as
follows:
Group I highly toxic LD 50 0.001–1.99 m g per bee: includes
the organophosphorus esters parathion, methyl parathion,C016_004_r03.indd 967C016_004_r03.indd 967 11/18/2005 11:00:08 AM11/18/2005 11:00:08 AM