Introduction

Chapter 1

Why use natural enemies?

Humans share the planet earth with some 10 million species of organisms. Each species eats, grows and reproduces in different ways in different locations around the world but virtually no species does this in isolation. All species are interconnected to some extent, with some organisms more dependent on others, especially those higher in the food chain. Tigers would not live long without their prey being available, just as rabbits would not survive for long without plants to eat. Humans have quite a dominant position in many ecosystems and they depend on many other species for food and shelter. Especially because the influence of humans is so pervasive throughout the world, humans also compete with many organisms and we generally think of many of these competitors as “pests.”

   Man has been plagued by “pests” since time began. A pest can be formally defined as any organism that reduces the availability, quality, or value of some human resource (Flint & van den Bosch, 1981). The definition of pest needs to be broad due to the great diversity in the ways that pests affect humans. The resources in question can be a plant or animal grown for food, fiber or pleasure (e.g., pets, plants in recreation areas). Another resource is human health and well-being, making organisms directly affecting human health, such as mosquitoes, pests too. Pests are as diverse taxonomically, ranging from microorganisms to mammals, as they are in the ways that they compete with humans. With such variability comes a variety of adaptations, and some organisms competing with humans are tough adversaries.

   There are many different means for controlling pests but this book is concerned only with methods using living organisms to control pests, a strategy called biological control. We will therefore not be covering all pests but only those specifically targeted by biological control. The major types of pests that are addressed by biological control include weedy plants, microorganisms attacking plants (often crop plants or forest trees), invertebrates (especially arthropods that often attack plants or animals), and vertebrates.

1.1 Historical perspective on chemical pest control

Humans have always needed to control pests affecting them directly, such as mosquitoes or bed bugs, or competing with them for a great diversity of resources. Through the ages pest control practices have changed dramatically. The earliest known record for the use of naturally occurring compounds for pest control was in ≈1000 BC, when the Greek Homer mentioned using sulfur as a fumigant. In the 1800s, tobacco extracts and nicotine smoke were applied for insect control. In 1867, we see the first mention of a mixture concocted for pest control that became widely used; Paris green, an arsenic-based compound, was developed and applied against Colorado potato beetle in the USA. Bordeaux mix, a combination of copper sulphate and hydrated lime, was developed in 1882 in Bordeaux, France, for control of plant pathogenic fungi on grapes and other fruits.

   Throughout these times, the overriding methods for pest control were cultural controls, such as leaving fields to lie fallow and rotating crops. For example, when soybean crops are rotated with corn, the soil-dwelling nematodes that attack soybean roots are nearly eliminated so that soybeans can again be planted. Other cultural controls included practices such as altering dates for planting and harvesting, using trap crops, planting mixtures of crops, managing drainage and removing crop residues that harbor pests. Growers were basically manipulating and augmenting the naturally occurring processes of pest suppression.

   Between World Wars Ⅰ and Ⅱ, several developments took place, setting the stage for major changes in pest control. Industries developed methods for large-scale production and chemists vastly improved their abilities to synthesize chemicals. In 1939, both DDT for control of insects and 2,4-D for control of weeds came on the scene. These extremely effective compounds revolutionized pest control. Since that time, a cascade of different compounds, belonging to an increasing number of chemical classes, have been synthesized for pest control. Most of the early compounds were effective against a broad spectrum of pests, killed pests very quickly, and were relatively easy to apply using spray equipment. Availability of these synthetic chemical pesticides changed the potential for successful harvests and, consequently, use of these compounds skyrocketed.

   Use of pesticides over time increased but these changes are not easy to quantify. Figure 1.1 illustrates the increase in value of different types of pesticides on the worldwide market from 1980 to 1999. While the majority of this pesticide use occurs in North America and Europe (56%), use in Asia and South America is also significant (Bateman, 2000). Between 1980 and 2000, the total value of pesticide sales increased approximately 2.5 times. Looking at the weight of pesticides applied can be a misleading statistic because over time, the potency of pesticides has increased, confounding comparisons through

Fig 1.1 Worldwide pesticide markets in the final two decades of the twentieth century. Data compiled from the annual reviews of the British Agrochemicals Association. (Bateman, 2000.) GM crops, genetically modified crops.

time. Data for the amount of land on which pesticides are applied are rarely available. A major fact to be gleaned from Fig. 1.1 is that among the numerous types of pesticides, the use of herbicides increased substantially from 1980 to 1999. Surprisingly, although genetically modified crops began to be used, they are not used very extensively in contrast to the publicity they have received. The bottom line is that as of 1990, an estimated 2.5 million tons of pesticides were applied each year worldwide at a cost of $20 billion. In the USA alone, 500,000 tons were used yearly at a cost of $4.1 billion. Today, synthetic chemical pesticides are clearly the most commonly used method for pest control (OTA, US Congress, 1995).

1.2 Why consider biological alternatives?

Synthetic chemical pesticides are used so widely because they often work very well for controlling pests. However, pesticides are not always the correct answer; sometimes they cannot control pests effectively for a variety of reasons. The major reasons that alternatives to synthetic chemical pesticides have been developed are presented below. In describing these scenarios, control of arthropods (i.e., insects and mites) will be used as examples, although similar issues occur relative to control of weeds and plant pathogens.

1.2.1 The pesticide treadmill

Although synthetic chemical pesticides are still the pest control method most widely used by many people, we are finding that there are growing reasons to consider alternatives. When pesticides are applied to control arthropods, naturally occurring controls are frequently severely disrupted and natural enemies normally living by consuming a pest are no longer abundant, or even present. Therefore, when the target pest reinvades the area, there are no natural enemies present and the target pest population increases again, frequently to higher densities than were present initially (= target pest resurgence) (Fig. 1.2). Figure 1.3 shows the growth of an outbreak in

Fig 1.2 Target pest resurgence can occur when natural enemies are destroyed. Pesticides often kill a higher proportion of natural enemies than pests so that after application, the pest can increase again rapidly. (From Flint & Dreistadt, 1998.)

Fig 1.3 Increases in California red scale, Aonidiella aurantii, on citrus tree associated with light monthly sprays of DDT, compared with nearby untreated trees under biological control. (From DeBach et al., 1971.)

a target pest, the California red scale, due to light, regular spraying of DDT.

   Since all of the natural enemies are often killed when pesticides are applied, other insects that had not previously been pests can increase to densities that cause damage, because the natural controls previously maintaining their populations at low densities are no longer present or abundant enough for control (Fig. 1.4). This scenario of a secondary pest outbreak can be demonstrated with the increase in the European spruce sawfly, which was under biological control until DDT was applied to control spruce budworm, Choristoneura fumiferana, in the same forest (Fig. 1.5). New York State apples provide an example of the diversity of secondary pests that can become

Fig 1.4 Secondary pest outbreaks occur when pesticide applications kill the natural enemies that have been controlling a species that has not been a pest. Without natural control, this species increases and can become a “secondary pest.” For example, a pesticide applied to kill Pest A (aphids) killed aphids and their predators, the green lacewings, but also killed predatory mites, resulting in a secondary pest outbreak of Pest B (spider mites), previously at lower densities due to predatory mites. (From Flint & Dreistadt, 1998.)

Fig 1.5 Increases in populations of a secondary pest in New Brunswick, Canada. European spruce sawfly (Gilpinia hercyniae) had been under biological control since 1940 but from 1960 to 1962 DDT was sprayed to control a different pest, spruce budworm. Spruce sawfly populations plummeted and their parasitoids could no longer be found, subsequently leading to an outbreak of spruce sawfly in 1964. On Grand Manan Island, no DDT was applied and an outbreak did not occur (Neilson & Elgee, 1965.)

problematic due to the application of broad-spectrum insecticides for control of different primary pests (Table 1.1). In this case, several different insect and mite species, previously not pests, can increase to pest levels due to severe reductions in the populations of their natural enemies, thus demonstrating that a diversity of problems can arise due to outbreaks of secondary pests.

   A third effect of extensive use of pesticides can be development of pesticide resistance (Fig. 1.6). Resistance can develop when a pesticide is extremely effective and the majority of the pest population dies after an application. However, sometimes a few individuals remain

Table 1.1 Key and secondary arthropod pests in apples in New York State

Fig 1.6 Pest populations can develop resistance to pesticides through natural selection. 1. When pesticides are applied, most individuals are killed but a few are less susceptible and these remain. 2. The less susceptible individuals or their progeny are less likely to die with subsequent applications. 3. After repeated applications, the resistant or less susceptible individuals predominate and applying the same pesticide is no longer effective. (Flint & Dreistadt, 1998.)

that are physiologically different and can tolerate the pesticide. The “new” strain of the pest that has been created is resistant to the pesticide and the population can then increase even when the pesticide is reapplied. Overusing the pesticide in response to lack of control only hastens the occurrence of resistance throughout the pest population. Eventually, the pesticide applied has no effect on the pest and a different control strategy must be used. It is often assumed that when a new material is developed, it will only be a matter of a few years

Fig 1.7 Numbers of arthropod species resistant to pesticides and the total of resistant species × compound combinations (= cases) in the United States from 1914 to 2000. (Redrawn from Mota-Sanchez et al., 2002.)

before resistance to the new compound begins to develop in some pest population.

   In fact, resistance to DDT was first seen in 1946 in houseflies, only 7 years after DDT began being used. By 1948, pesticide resistance was seen in 14 species and by 1990 over 500 species of arthropods displayed resistance to insecticides (Fig. 1.7). First, when resistance to insecticides begins to develop, growers characteristically apply more insecticide, often not realizing that the lack of control is due to resistance. Next, growers might switch to a closely related pesticide, but once pests develop resistance to one pesticide in a pesticide class, they are often at least partially resistant to other similar pesticides. The grower also might choose another class of pesticides, for example switching from organophosphate insecticides to pyrethroids, under the assumption that the pest had acquired at least partial resistance to all organophosphates. However, pests can be resistant to several classes of pesticides at the same time and resistance can eventually develop to this second choice of control agent. As a double whammy, frequently the alternative pesticide can be more costly. For example, with development of resistance to DDT, malathion was substituted at five times the cost but when resistance developed to malathion, fenitrothion, propoxur, or deltamethrin were often substituted by growers at 15–20 times the cost.

   These three phenomena together (target pest resurgence, secondary pest outbreaks, and development of resistance in pest populations) have been termed the pesticide treadmill. They lead to increasing dependence on pesticides, seemingly an addiction for use of this type of control.

1.2.2 Fewer pesticides are available

Due to the development of resistance to classes of pesticides, there is a constant demand for new types of pesticides. However, the costs of developing and registering new pesticides have increased over time.

Fig 1.8 Numbers of registered pesticides for arthropod control in the USA from 1914 to 1999. (Redrawn from Mota-Sanchez et al., 2002.)

Since 1970, there has been a significant slow down in the rate of new pesticides being introduced to the market. In addition, due to increased regulation, some of the pesticides that have been available for many years are no longer legally available for application. For both of these reasons, in many countries there are fewer pesticides registered and thus available for use (Fig. 1.8). As one example, a mainstay for control of soil-borne pathogens and pests as well as storage diseases of fruits and vegetables has been fumigation with methyl bromide. In the year 2010, this chemical will be banned worldwide due to its role in ozone depletion (Ristaino & Thomas, 1997) so alternative controls must be used. In summary, there is a trend toward fewer synthetic chemical pesticide options due to increased resistance to existing insecticides, banning some compounds, and decreased development and registration of new compounds.

1.2.3 Synthetic chemical pesticides aren’t always the answer

There are some situations in which chemical pesticides are not the most appropriate choice for controlling pests. One example would be introduced exotic organisms that become pests; it has been estimated that 30,000 exotic organisms have been introduced to the USA. In fact, invasive species are now considered a major problem worldwide due to the increasing human population frequently moving organisms around the globe and thereby altering ecosystems at an increasing rate. Many invaders become pestiferous largely due to the fact that they are no longer associated with the natural enemies with which they coevolved. Among pests in agriculture, approximately 20–40% have been introduced from elsewhere. Most are accidental introductions, although a small percentage of these were purposeful introductions such as crop plants and honeybees. Some were purposeful introductions with unexpected side effects. For example, the weed kudzu was introduced to the southeastern USA to control erosion and has since spread rampantly through most of the southeast, becoming a problematic weed. Introduced organisms are not always identified quickly, so they establish and become ubiquitous before it is possible to eradicate them. It is difficult to imagine how a synthetic chemical pesticide can easily solve such a problem as a fast-growing weed, without continual human intervention and its associated costs. Problems due to such pests are therefore often not readily addressed using synthetic chemical pesticides because more permanent control is what is needed. Classical biological control has frequently been successfully used against such pests (permanently introducing natural enemies from the land of origin of the pest). Unfortunately, by all predictions, accidental introductions of invasive species will only continue with the increased global movement of humans and materials (see below).