Plant and Pest Science, Waite Campus, The University of Adelaide SA 5005, Australia. email@example.com
In order to improve the level of adoption of integrated pest management (IPM), it is important to understand the benefits of integrating IPM practices. Integrated systems are less prone to failure and, when they incorporate natural enemies, they are also more resilient than systems that rely on a single method of pest suppression. The impact of changing IPM practices on the pest population dynamics was evaluated in a qualitative manner by varying the parameters of the Lotka-Volterra Model. Factors that reduced the mean population density, reduced the amplitude of pest population fluctuations or increased the interval between pest population peaks were considered to improve IPM systems. Practices that reduce the net reproduction of pests, like resistant plant varieties and promotion of generalist natural enemies, are one way to improve IPM systems. Providing food resources for specialist natural enemies can also improve the level of control. Both broad-spectrum and selective insecticides can disrupt biological control systems that involve specialist natural enemies, so it is important to use pesticides only as a last resort. Even when IPM practices deliver only a fraction of the overall level of control, they can contribute to an effective IPM system. There are many practices that can be incorporated into integrated systems directed at management of the diamondback moth (DBM). Further theoretical and empirical research is needed to assist farmers with the implementation of integrated systems for management of DBM and other pests.
Lotka-Volterra Model, conservation biological control, integrated pest management
There is a growing awareness that the potential of integrated pest management (IPM) is not being realised in many crops (Ehler & Bottrell 2000, Stephenson et al. 2001). Elements of IPM practice, such as the use of economic thresholds in making decisions, are widely recognised as important tools for the management of pests. However, biologically-based IPM systems have not been developed in many instances, in part because of poor understanding of the ecological complexity of farming systems (Ehler & Bottrell 2000).
The integration of pest management systems can occur at several levels (Kogan 1988). At the lowest level, the methods used against a single pest can be carefully combined to deliver more effective pest suppression. At higher levels, integration can include the methods used against several to many pests in different classes of organism (insects, weeds, plant pathogens) and also can involve the concerted efforts of farmers, advisers, researchers and others involved in IPM.
The integration of pest management methods can enhance the level and reliability of pest suppression. Such integration has strong theoretical foundations. With a clearer understanding of these principles, better integrated management systems can be developed for use against the diamondback moth and other crucifer pests. These are the subjects of this paper.
Why integrate pest management methods?
Integrated systems of pest management are potentially more reliable and robust than those based on a single method of pest suppression. This can be understood by considering three hypothetical pest management systems used against a lepidopteran pest. In the first, a single method is used to control the target pest, for example, an insecticide spray that delivers 95% control. In the second, partial host plant resistance and augmentation with egg parasitoids each deliver 78% control. In the third, generalist egg predators and parasitic wasps that attack small larvae and sprays of Bacillus thuringiensis directed against large larvae, each deliver 63% control. If it is assumed that there are no interactions that affect the efficacy of the methods, then it is easy to see that all three systems deliver the same overall level of mortality (Figure 1). These examples illustrate the value of using methods that do not completely control pests when they are combined in integrated pest management systems.
Figure 1. A comparison of the effectiveness of three different pest management systems. To achieve 95% pest suppression, it is possible to use one highly effective method that delivers the full 95% reduction in numbers (right), two methods that reduce numbers by 78% each (middle) or three methods that reduce numbers by 63% each (left; the fraction surviving each practice is shown in successive open bars). However, if the first method employed in each system is 20% less effective, then the overall level of control is poorest if only one method is used (19% greater pest survival) compared with systems that employ two (+3.5%) or three (+1.7%) control methods (grey bars).
The efficacy of pest management methods can vary. For example, rainfall after an insecticide spray can wash some of the active ingredients off treated plants. To see how such variation can influence the overall degree of control in integrated pest management systems, consider the previously-discussed hypothetical systems of pest management. In particular, assume that the first method in each alternative system was 20% less effective, i.e. 20% fewer pests died. In this case, the single insecticide spray would allow 19% more pests to survive while only 1.7% more pests would survive if the combination of three integrated methods was used (Figure 1). This example shows that integrated pest management systems are more robust, i.e. they are less prone to failure.
Biologically-based IPM systems are also resilient. Following natural or human disturbances, natural enemies and other biotic factors that limit pest damage can recover through the combined effects of reproduction and immigration. The development of resilient and robust pest management systems should be a primary goal of pest management practitioners.
The theoretical foundation of integration
There are three ways to reduce pest numbers within an agricultural production system: reduce the net reproduction of the pest, increase the pest’s mortality or inhibit immigration. The latter is not considered theoretically here, but where knowledge of the factors that influence pest movement is available, inhibition of immigration into crops should be pursued as a management method, e.g. by planting trap crops (Hokkanen 1991, Mitchell 2000).
The predictions of the Lotka-Volterra model illustrate in a qualitative way how pest management methods can influence the degree of pest suppression and the frequency at which pest populations reach damaging densities. This is a relatively simple mathematical model (Wilson & Bossert 1971), but the predictions of the model reflect how changing biological characteristics and circumstances affect pest population dynamics when a specific natural enemy contributes to pest suppression in an IPM system. The Lotka-Volterra model is given by two equations:
N is the population size of the prey,
P is the population size of the predator,
a1 is the instantaneous per capita reproduction rate of the prey in the absence of the predator,
b1 describes the instantaneous attack rate of the predator on the prey,
a2 describes the efficiency of conversion of prey resources into predator reproduction,
b2 is the instantaneous per capita death rate of the predator.
The model can be modified by incorporating density-dependent prey population growth in the absence of predation in order to aid in the interpretation of the model’s predictions. A term for logistic population growth can be added to equation (1):
where k is the carrying capacity of the prey population.
This model predicts delayed density-dependent fluctuations of the prey (= pest in this context) and predator populations that asymptotically approach a stable equilibrium (Figure 2a).
The effects of different management methods can be predicted by changing the model parameters. For example, if the net reproduction of the prey decreases (decrease the value of a1), the intervals between population peaks of the prey are longer and the amplitude of fluctuations in the prey population is smaller (Figure 2b). The net reproduction parameter in this model represents the net difference between the production of offspring and density independent mortality factors. Thus damaging pest densities should occur less frequently if either individual reproduction is reduced by factors like host plant resistance or non-specific mortality factors like generalist predators are enhanced. Another way to improve the degree of control is to enhance the activities of the specific natural enemy. While it may not be practical to increase the attack rate of the predator, it should be possible to increase predator longevity (decrease the value of b2 in the model). For example, the longevity of parasitic wasps can be increased by providing floral nectar in agricultural systems (Idris & Grafius 1995, Landis et al. 2000). This leads to a lower mean prey density and longer intervals between peak densities (Figure 2c).
The Lotka-Volterra model can also be used to show how insecticides can affect biological control systems. Consider a situation where an insecticide spray kills 80% of both the pest and its specific predator (Figure 3a). Following the spray, the prey population recovers more quickly than the predator population. This illustrates the resurgence of pests that often follows insecticide applications (DeBach & Rosen 1991). Pest resurgence arises as a result of “Volterra’s Principle” (Wilson & Bossert 1971). Following simultaneous harvest or removal of both prey and predator, the prey population will always recover its original numbers more quickly than the prey. Inspection of the model equations shows why. The net reproduction of the prey depends only on its own numbers (model term a1N in equation 1), while the reproduction of the predator depends on the numbers of both the prey and the predator (model term a2NP in equation 2). The effects of the insecticide are multiplied for the predator population. In many situations, pesticides are more deadly to natural enemies than to pests, which accentuates the effects of Volterra’s Principle.
Figure 2. Predictions of the modified Lotka-Volterra Model, which incorporates density dependent population growth of the prey in the absence of the predator. (a) Predictions of the basic model. (b) Effects of a reduction of the net reproduction of the prey on numbers of prey. (c) Effects of a decrease in the mortality rate of the predator on numbers of prey (predator numbers not shown). E0 is the equilibrium density of the prey in the basic model. T0, T1 and T2 are arbitrarily selected times. Initial conditions are the same in each model.
Some selective “soft” insecticides are relatively benign to predators and parasitoids, which limits the level of predator mortality (Singh & Varma 1986, Udayagiri et al. 2000). However, the Lotka-Volterra model predicts that soft insecticides can still disrupt biological control (Figure 3b). When prey numbers decline, predator reproduction is still reduced. The result is a decline in populations of specific predators. Thus, pest resurgence can still occur following the application of a “soft” insecticide. Pesticides often have a disruptive effect on biological control systems. The primary benefit of selective pesticides is that interactions among non-target species are not affected by them.
Figure 3. Effects of pesticide sprays on the dynamics of predator and prey populations as predicted by the modified Lotka-Volterra Model. (a) Pesticide kills 80% of both predator and prey populations at time T1. (b) Pesticide kills 80% of prey population only at time T1. E0 is the equilibrium density of the prey.
General population models like the Lotka-Volterra model can offer insight into how various pest management practices can influence the population dynamics of pests. However, these predictions are only qualitative since they depend on simplifying assumptions. The impact of pesticides on parasitoid-host interactions can also be influenced by other biological factors and more specific predictions about the impact of pesticides on parasitoid-host population dynamics have been made (Hassell 1984). In the future, more detailed studies of how management activities affect the dynamics of real pest and natural-enemy populations are needed in order to gain a more quantitative understanding of the interactions that influence the outcome of pest management programs. Inevitably such studies will be more complex, so it is imperative that scientists distil the key outcomes of such studies into simpler recommendations in order to persuade farmers to change their farming methods.
Practical approaches to the integration of pest management methods
(a) Reducing the net reproduction of pests
The net reproduction of pest populations can be reduced by directly inhibiting growth, development and individual reproduction and indirectly by increasing density-independent mortality levels. In addition to the use of resistant plant varieties to reduce the net reproduction of pests, plant health can be managed to reduce their fitness. For example, when high rates of nitrogen fertiliser are used to produce host plants, the diamondback moth develops more quickly and reaches a larger adult size (Fox et al. 1990). Since body size is correlated with fecundity in insects (Honek 1993, Nylin & Gotthard 1998), this suggests that the rate of population increase in diamondback moth is probably greater when high levels of nitrogen are used to produce host plants. Oviposition by a range of pests can be inhibited by under-sowing crops with plants like clover (Finch & Kienegger 1997). This should also reduce the net reproduction of the pest.
(b) Conserving and enhancing natural enemies
Both generalist and specific natural enemies can contribute to the effectiveness of an IPM system. Although the population dynamics of generalist predators are not tightly linked to the pest, they can act as a buffer against pest incursions and can reduce the population growth by reducing the net reproduction of pest populations. Generalist predators can be conserved by providing alternative prey, non-prey foods like pollen and nectar (syrphids and coccinellids) and seasonal refuges (Wratten 1996, Gurr & Wratten 1999). The longevity of parasitic wasps can be prolonged if they feed on sugar sources (Idris & Grafius 1995). Floral and extrafloral nectar and homopteran honeydew can all contribute sugar food for parasitoids. Floral diversity in and around crops can be enhanced by planting selected species around crop borders, along irrigation and tractor alleys within crops and by under-sowing with a cover crop. Care must be taken when selecting flowering plants because the structure of some flowers prevents parasitoids and predators from gaining access to nectar and pollen (Jervis et al. 1993), while some species provide food that can enhance pest reproduction (Baggen & Gurr 1998).
Avoiding and minimising negative interactions
While there are many methods that could be combined in an IPM system, it is important to avoid the negative interactions that may occur. The potentially negative impacts of insecticides on the subsequent reproduction of predators and parasitoids has already been described. The sudden mortality caused by insecticidal pathogens could cause the same negative effects. This could be minimised by using lower “IPM rates” of insecticides. For example, pirimicarb (Pirimor®) is applied at 10% of the recommended rate in Australian citrus to control aphids (Smith et al. 1997). This tends to reduce aphid numbers to tolerable levels while conserving natural enemies of aphids and other insect pests. Although pesticide sprays directly kill pests, sprays may have unintended effects on their behaviour. The surfactants used to increase the coverage of insecticide sprays are known to stimulate oviposition by diamondback moth (Rigginbucci et al. 1998). It seems that this is due to a change in the wax structure on the leaf surface and several different types of surfactants have the same stimulatory effect on oviposition. Negative interaction can also occur when certain resistant plant varieties interfere with the behaviour and survival of predators and parasitoids (van Lenteren et al. 1995). Negative interactions can be unpredictable, so it is important to monitor populations of pests and natural enemies when new methods are introduced into pest management systems.
There is a need to better understand how mortality caused by predators and parasitoids influences the population dynamics of pests and the damage they cause. Such information could be used to develop more comprehensive action thresholds for the use of selected insecticidal agents. For example, Loke et al. (1992) developed action thresholds for control of the diamondback moth that incorporated information about larval densities, plant growth stages and levels of parasitism. Their work was the result of empirical research on management of DBM. Unfortunately there is no body of theoretical work that can guide the development of action thresholds that incorporate the activities of natural enemies. This is a fertile area for future theoretical and empirical research.
If the mortality caused by natural enemies is to be reliably incorporated into IPM decision-making advice, then it is important to have available methods to assess their activities. Dissection of larval DBM is easy and can indicate the presence of parasitoid eggs and larvae. All that is needed is a low magnification dissecting microscope, two fine forceps and a dish of water with a dark background. After grasping the head and tail of a larva with the forceps, it can be pulled apart to reveal eggs and larvae floating freely in the haemocele. Where dissection is not practical, yellow sticky traps (Idris & Grafius 1998) and traps baited with virgin female parasitoids (Decker et al. 1993) can be used to indicate parasitoid activity. The numbers of insects collected in traps would only give an index of activity rather than a measure of the mortality they cause, but trap catches may be sufficient to convince farmers that natural enemies are active in their crops.
Practical integration of pest management methods
The integration of pest management methods should commence when planting a crop is first planned and should continue after harvest. For transplanted vegetable Brassica crops, this spans the production of seedlings, transplanting and crop establishment, vegetative crop growth, the final period when the harvested plant parts are produced and beyond harvest. There are many methods that could be integrated into a pest management program (Talekar & Shelton 1993).
When planning a crop, the choice of plant variety can influence the likelihood of pest damage. Consumer preferences for certain vegetable characteristics tend to be more important in the selection of varieties than resistance to insect attack, so resistance has not been a primary objective of plant breeders. This might change with the introduction of transgenic crops, but consumers must be convinced of the safety of transgenic crops before they will buy them. Seedlings could be produced under screens to physically prevent infestation by pests like diamondback moth, thereby limiting selection for resistance. In addition, natural enemies could be seeded on plants in the nursery before they are transplanted (Hofsvang & Hagvar 1979), thereby ensuring that biological control is more reliable. Both of these methods highlight the advantage of farmers and nurseries forming a partnership in the development of an IPM system, which would raise the level of human integration.
Once seedlings reach the farm, there are many possible methods that can be incorporated into a pest management system. For example, crops could be under-sown with clover or another plant to inhibit colonisation by pests (Finch & Kienegger 1997), flowers could be planted to conserve and enhance the activities of predators and parasitoids (Landis et al. 2000) and soil fertility could be managed to avoid high levels of nitrogen in plants. Colonisation of the crop by DBM could be inhibited by planting a trap crop (Mitchell et al. 2000), or a “dead-end trap crop” could be grown that attracts oviposition by DBM, but does not support larval development (A. Shelton, personal communication). In the longer term, farmers may begin to manage the landscape surrounding their fields to achieve an ecological integration that more comprehensively reduces pest activities (Landis et al. 2000). To succeed, the farmer must anticipate pest activity and respond by adopting methods that reduce the likelihood of crop damage.
Once the crop is transplanted, monitoring and the use of selective control methods are important components of an integrated pest management system (Talekar & Shelton 1993). Monitoring can indicate the densities of pests, the incidence of parasitism and the efficacy of the pest management program. Monitoring of pest activity and damage using pheromone traps and direct plant inspection should be done at intervals related to prevailing weather. When warm and dry conditions prevail, DBM develops more quickly and typically has greater survival (Harcourt 1986), hence monitoring should be more frequent at these times. If the potential for damage is indicated by monitoring, then farmers should preferentially use a soft insecticide like Bacillus thuringiensis or one of the newer selective insecticides. There should be no need to use older products like organophosphates or synthetic pyrethroids that have a broader spectrum of activity and are known to disrupt biological controls.
Farmers are concerned with how effectively a pest management system suppresses pest populations and thereby reduces damage caused by pests. There are clear benefits from integrating pest management practices to achieve this aim. Pest management systems can be more robust and resilient when the means of pest suppression are carefully selected and integrated. An understanding of how various practices interact can guide the development of pest management systems. However, farmers must also weigh up the practicality and cost-effectiveness of their pest management practices. The challenge for those who develop pest management systems is to develop better theoretical understanding of the benefits of integrating pest management practices and to translate this into practical systems that will be adopted by farmers.
Financial support for this work was provided by a grant from Horticulture Australia Limited.
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