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Pesticides such as DDT and dieldrin have a bad reputation. They acquired
it in the 1960s and 1970s, when people began to realise that these chemicals
were accumulating in birds and animals, with disastrous results. The poisonous
effects of this accumulation were particularly apparent among raptors –
birds of prey – in Europe and North America, where in several areas some
species became extinct. For example, the peregrine falcon disappeared from
most of England and the northeastern US. When, by the early 1970s, these
pesticides were banned or restricted in most developed countries, many raptor
populations recovered. The past 15 years have seen the gradual reappearance
of peregrines in Britain, ospreys and bald eagles in the northeast US, and
white-tailed eagles in Finland.

But not all populations recovered equally well. In the late 1970s, ornithologists
in several countries tried to find out why. Charles Henny and his colleagues
from the Patuxent Wildlife Research Centre in Oregon discovered that seven
per cent of adult female peregrines caught in the eastern US while migrating
back from their wintering grounds in central and southern America had accumulated
enough DDT to affect their reproductive ability. Swedish researchers led
by Peter Lindberg from the University of Gothenburg showed that breeding
peregrines feeding on trans-Saharan migratory waders, such as the greenshank,
absorb more DDT than those feeding on resident birds such as wild pigeons.

These findings came as a great surprise to the ornithologists. Until
then, they believed that organochlorines did not persist long enough in
hot climates to cause such problems. There are sound chemical reasons for
their assumption. Organochlorine pesticides can be broken down by strong
light, lost by evaporation and dispersed by wind and water. These processes
tend to be faster in the tropics than elsewhere because of the higher temperatures.
For example, in temperate zones, the half-life of DDT (the time taken for
half any quantity of DDT to disappear) in soil is 2-8 years; in tropical
soils it is between one and four months. The half-lives of dieldrin are
about the same.

These assumptions are also borne out by experiments done in the field.
During the 1970s, Dick Yeadon and John Perfect of the British Overseas Development
Administration (ODA) studied pesticide persistence in the tropical humidity
of Ibadan, Nigeria. They applied 70 kilograms of DDT per hectare of land,
over four years, to fields used for growing cowpea. At the end of the fourth
year, they could detect only 2-8 per cent of the original amount of pesticide
in the soil. In another study, Robert MacCuaig of the United Nations Food
and Agriculture Organisation (FAO) applied radioactively labelled dieldrin
to soil in Ethiopia used for growing cotton. After one month, only 10 per
cent remained in the soil.

But despite these shorter persistence rates, there is evidence that
these pesticides accumulate in food chains in Africa. The chemicals are
both stable and lipophilic (fat-loving) so they build up, apparently harmlessly,
in the fat of animals. Carnivores accumulate the pesticide residues quicker
than herbivores. It is this ‘biomagnification’ of pesticide residues within
food-chains that has such lethal consequences for the animals and birds
at the top when they mobilise their fat reserves into the bloodstream at
times of stress. In 1974, Yvonne and Algirdas Greichus from South Dakota
State University and their colleagues from the Department of Nature Conservation
in South Africa and Harare University in Zimbabwe provided the best example
of this process in the heart of Africa, when they found that cormorants
from three lakes in South Africa and Zimbabwe had between 30 and 37 times
the levels of DDT and dieldrin found in fish from the same lakes.

But the suspicions of ornithologists – that these processes were threatening
African raptors – were difficult to prove. Population changes in African
raptors are hard to assess accurately, because of the lack of fieldworkers
and the fact that the birds often nest in well hidden or inaccessible places.
So ornithologists must turn to other, indirect evidence that organochlorines
are killing birds of prey. They could infer the level of damage by measuring
levels of pesticide residues in adult raptors and their eggs. But in Africa,
even this evidence is scarce. There have been just 20 published studies
between 1979 and 1988 from 12 African countries, covering 40 species of
raptor. Fortunately, raptors from falcons to eagles have remarkably similar
physiological responses to organochlorine pesticides, so ornithologists
can extrapolate the effects on European and North American raptors to those
in Africa.

The most accurate way of predicting these effects on raptor populations
is to measure the levels of pesticide residues in the brains of a sample
of dead birds from the population. Samples taken from the blood are much
more variable. Residue levels are expressed in parts per million (grams
of pesticide per million grams of brain tissue), and the figure varies depending
on whether the tissue is wet or dry. In adult raptors, between 4 and 10
ppm wet weight of dieldrin is lethal, while 1 ppm of dieldrin is lethal
to raptor eggs. Between 100 and 200 ppm wet weight of DDT is lethal to adult
raptors, while 10 ppm wet weight makes egg shells 16 per cent thinner, so
that they break when the female adult sits on them to incubate them. This
level of thinning threatens the raptor population with decline.

The African data from the 20 known studies show that in the eggs of
six species – especially peregrine, black sparrowhawk and African fish eagle
– the average levels of DDT and its derivatives were high enough to cause
a decline in local populations through the thinning of eggshells. Other
organochlorines, such as toxaphene and dieldrin, have been found at levels
which could threaten the hatchability of eggs in certain populations of
white-headed, white-backed and cape vultures, and of three raptor species
already suffering from high levels of DDE formed from DDT .

Of the four organochlorine pesticides found in adult African raptors,
DDT and dieldrin occur at potentially lethal levels in five per cent and
at sublethal but still potentially harmful levels in 12 per cent of the
birds tested in seven studies, mainly from Kenya and South Africa. As in
Europe and North America, the species most at risk are those that eat carrion,
birds or fish rather than mammals, reptiles, insects or fruit, because they
are higher up their respective food chains.

At first sight, such levels of pesticide residues may appear to be a
minor problem. But many of the birds studied so far came from remote and
wild areas. Those that came from intensively farmed areas, such as near
Harare in Zimbabwe, or Nairobi in Kenya, had higher levels of pesticides.
The eggs of cape vultures, for example, are more heavily polluted in the
Cape Province of South Africa than in the less densely populated areas of
Transvaal or Botswana.

Statistics of land use can also be misleading. According to the FAO’s
latest Production Yearbook (1988), only six per cent of land in Africa is
under permanent crops, compared with 21 per cent in the US and 30 per cent
in Europe. But six per cent of Africa is a much larger area than 30 per
cent of Europe and it is nearly as large as 21 per cent of the US. And as
the human population grows in Africa, the area affected by intensive agriculture
will grow, as will environmental contamination from pesticides.

Banning or restricting the use of pesticides, as many developed countries
have done, is not the simple answer it may seem. Africa has more than its
fair share of devastating pests. Organochlorine compounds have played a
crucial role in controlling carriers of disease, such as the malaria-transmitting
anophelene mosquitoes, and the destruction of crops by pests. These chemicals
have been and still are effective, cheap and relatively safe to use, even
though the long-term effects of DDT and dieldrin in people are unknown.

In Africa, spraying DDT has been of immense benefit in controlling the
tsetse fly, which carries sleeping sickness in both man and cattle. In practice
this means ground teams walk through hundreds of miles of bush spraying
DDT onto the sheltered resting sites of the tsetse fly. In the early 1980s,
Peter Mattheissen of the ODA showed that this method was the main source
of DDT contamination in freshwater mussels, fish, birds and bats in western
Zimbabwe. Ron Thompson, then working at the Zimbabwe Department of Natural
Resources, also gathered evidence between 1974 and 1980 on the effects of
DDT from tsetse control. In one unpublished study he collected and analysed
eggs of eight different raptor species, including the African fish eagle
and black sparrowhawks. The levels of DDE in these eggs would threaten local
populations. For example, the residues of DDE in dehydrated tissue of 33
clutches of African fish eagle eggs varied from 10.8 ppm to 291 ppm, averaging
53.3 ppm. This was 15 per cent higher than the level at which shell thinning
is likely to cause a population decline.

Between the 1940s and 1970s governments in northern and central Africa
also encouraged the use of another organochlorine, dieldrin, to control
locusts. A common method involves spraying the dieldrin to form barriers
several kilometres long between strips of untreated desert, to poison roving
bands of young, non-flying insects. When the drought ended in North Africa
in 1985, desert locusts began swarming again and during the next two years
farmers had no option but to treat 3.6 million hectares with pesticides
to control these and other grasshoppers. People as influential as Rafik
Skaf, then director of locust control at the FAO, called for the reintroduction
of dieldrin. In 1988, the FAO reported that this chemical had been used
for 13 per cent of the spraying, in addition to 24 other pesticides, including
about a million kilograms of bait dosed with lindane, another organochlorine.
There was no systematic assessment of the environmental effects of these
control methods, but ornithologists have reported birds dying; there was
widespread concern about the threat to the last few breeding colonies of
the Bald Ibis in Morocco.

The best available solution

Farmers have also used DDT heavily to protect cotton from pests, such
as the pink bollworm. Recent work by Ronald Davies and Ron Randall in South
Africa shows that eggshell thinning in African fish eagles is higher where
cotton production has been intense. In Egypt in 1977, two Dutch ornithologists,
Wim Mullie and Peter Meininger, initiated a project to map all the birds
in the country. Although the project is still in progress, a preliminary
analysis reported in 1982 suggested that two resident species of raptor,
the blackshouldered kite and the black kite have disappeared from the main
areas of cotton production along the River Nile. Fortunately, modern methods
for the control of cotton pests, including the use of pheromones – chemicals
similar to hormones, produced by the insects themselves – are being introduced
as these pests become increasingly resistant to DDT. But DDT often remains
the only practical solution for many of Africa’s small farmers, because
it is cheap.

Two other pesticides, aldrin and dieldrin, have for many years been
the only effective method of protecting crops, trees and buildings from
termites. Alternatives are now available for buildings; and where these
chemicals are used in planting-hole treatments or by incorporation into
potting soil, the quantities used are small and the areas affected highly
localised. However, there are no alternatives to aldrin and dieldrin for
protecting seeds. The recommended doses for dressing seeds are 10 to 100
times as high as those used in Britain during the 1960s when so many pigeons
and raptors were killed. If the seed is scattered on the ground, rather
than drilled directly, this method of controlling termites could be extremely
hazardous to grain-eating birds, and the birds that prey on them.

Nevertheless, such chemicals may be preferable to using large quantities
of less persistent pesticides. In 1984 and 1985, I studied the side-effects
on songbirds of fenitrothion, a pesticide sprayed by helicopter in pine
plantations to control the Pine Beauty Moth. The dosage rates used against
locusts during the campaigns in Africa in 1986 and 1987 would kill most
birds caught in the spray. Used intensively, organochlorine pesticides can
have the same effects on raptor populations in Africa as in temperate North
America and Europe. But in Africa they ensure the survival of man, his livestock
or his crops. It would be irresponsible and indefensible to advocate their
immediate ban. But equally, there seems little excuse for the continued
use of environmentally damaging chemicals, when less damaging alternatives,
such as pyrethroid pesticides and pheromones, may be available.

* * *

Early warnings of a silent spring

During the late 1950s and early 1960s, thousands of pigeons died in
British fields. They had eaten seed which had been coated with dieldrin
or some other cyclodiene pesticide. Soon, birds of prey, such as sparrowhawks
and peregrines, began to die because they fed on heavily contaminated pigeons.
In 1962, similar events in the US prompted Rachel Carson to write her powerful
book Silent Spring, which predicted a bleak future for our environment.
The title encapsulates the idea of a world in which the songbirds have been
killed off by pesticides.

The discovery of these deadly effects was followed in the 1960s by the
discovery of eggshell thinning in birds of prey. This was uncovered in a
curiously roundabout manner. By the late 1950s, pigeon fanciers and racers
in Britain had been complaining for some time that peregrine falcons were
eating too many of their birds.

In 1960, the British Trust for Ornithology employed Derek Ratcliffe
to investigate the problem. He soon realised that rather than there being
too many peregrines, the species were suffering a drastic population crash.
The falcons were already extinct in southeast England, were declining in
other parts but apparently still thriving in northwest Scotland. As well
as being killed by pesticides, the surviving peregrines were failing to
reproduce successfully because their eggs had thin shells that broke easily.
Ratcliffe found that the degree of thinning was proprotional to the concentration
in the egg of DDE, the stable breakdown product of DDT. In the 1970s work
by various researchers in Britain and the US rapidly confirmed this relationship.
In 1975 Jeffery Lincer of Cornell University also found that raptors responded
to very low dietary doses of DDE (3 parts per million in their food) and
very rapidly (within a few days of being given the chemical).

These alarming results could not have been predicted by standard testing
procedures in use at the time. They alerted pesticide manufacturers and
governments to the scope that pesticides have, as widely dispersed poisons,
to produce unforeseen side effects.

* * *

Swiss chemists working for J R Geigy discovered the insecticidal properties
of DDT (dichlorodiphenyltrichloroethane) in 1940. It belongs to the organochlorine
group of pesticides, organic molecules in which one or more chlorine atoms
replace hydrogen. Because they are chemically stable these molecules persist
for a long time in the environment. Other examples are lindane and the cyclodiene
pesticides, dieldrin and aldrin.

DDT is both a stomach insecticide and a contact insecticide. It works
by interfering with the insects’ nervous system, but it has no effect on
that of warm-blooded animals. But both DDT and its breakdown product DDE
tend to accumulate in the fat of carnivorous animals and birds at the top
of food chains, a process called biomagnification.

At sufficiently high levels – 10 ppm wet weight in birds of prey – DDE
causes thinning of eggshells. One theory is that DDE inhibits a receptor
of the hormone progesterone in the shell gland of these birds, and that
this reduces the rate at which the bird deposits calcium carbonate, the
main component of eggshells. Songbirds and ducks are more resistant. Some
insects have developed resistance to DDT, in the shape of enzymes that will
break it down to DDE, which has no insecticidal properties.

Modern alternatives to organochlorines include pyrethroid pesticides
such as permethrin and deltamethrin. These are synthetic analogues of pyrethrum,
an extract from the flowers of the chrysanthemum. They have short environmental
persistence and low toxicity to mammals.

Humphrey Crick was a research fellow in the department of Zoology at
Aberdeen University before joining the British Trust for Ornithology as
head of the Nest Records Unit.