INTEGRATION OF BIOLOGICAL CONTROL INTO IPM SYSTEMS FOR AQUATIC WEEDS

James J. Marois, Department of Plant Pathology, University of California, Davis, CA 95616 USA

ABSTRACT

The development of effective long-term control programs for aquatic weeds is dependent upon the ability to integrate biological, chemical, and cultural control strategies. Successful IPM programs are dependent upon a sound knowledge of the cropping system (especially the inputs and outputs of the system), the biology of the aquatic weed pest, and the biology of the control agent(s). There are several ways to analyze these complex systems, from the molecular to the community level. This presentation will emphasize the ecological interactions that should be con- sidered.

INTRODUCTION approach may be to augment or inundate the system with the control organisms at specific times in the Integration of biological control of paddy and cropping history. This is especially true when the aquatic weeds into integrated pest management control agent is a fungus or bacterium, since these programs is a necessary goal for the implementation are relatively easy to produce in large quantities and of sustainable rice production systems. To reach are dependent upon specific environmental this goal, however, a number of obstacles must be conditions for greatest efficacy. When a fungus is overcome. Most important is the current status of used to control a weed in this manner, it is referred biological control of aquatic weeds which, in this to as a bioherbicide (Emge and Templeton 1981). discussion, will be defined narrowly as the use of Successful integration of control agents, either beneficial or their gene products pathogens or insects, is dependent upon the for . Although considerable research compatibility of the biological control system with has been done and several successful systems have the entire crop production system. been implemented for the control of weeds, these Most of the difficulties in developing are usually restricted to low-input systems such as functional biological controls are related to the public lands and range lands. This is because most complexities of the biological systems being of the work has been based on the classical approach managed. In spite of this difficulty, there are to biological control, in which the strategy is to increasing economic and social pressures to develop establish pathogens or herbivores in an area where practical biological control strategies. This paper the weed is a problem. Classical biological control addresses the potential for integration of biological is dependent upon long-term population dynamics; control with other strategies. Also however, in intesively managed systems such as discussed are perspectives of research at population Asian rice production, where three crops are grown and community levels which should be considered each year, it is not possible for the long-term if viable biological control strategies are to be interactions necessary for suppression of the weed developed. population to take place. Thus, a more appropriate

Keywords: Ecology, biological control, IPM

210 BIOLOGICAL CONTROL IN INTEGRATED PEST weed) (Supkoff et al. 1988). Because this weed is MANAGEMENT important in low input systems, such as range land, it is not economically feasible to control it with Biological control for aquatic weeds will be chemical . implemented most readily when no other means of Biological methods can also be used to increase control are available, when public awareness of the level of disease control attainable with chemicals. use is high, and when pesticide applications It is possible for resident microorganisms to increase are particularly hazardous or disruptive to the directly the efficacy of a chemical treatment. For environment. Such opportunities for implementation example, herbicides may stress a plant so that it is are becoming more common. In the past, more susceptible to infection by plant pathogens, appeared to control aquatic weeds relatively cheaply competition from other plants (including the crop because the negative impacts of pesticides on the plant), or to being eaten by insects. A combination environment were costs which were not transferred of herbicides with biological control agents may to the users or manufacturers of pesticides. Recently, result in the control of weeds which cannot be a volatile political climate has developed concerning controlled by chemicals alone, or a reduction in the exposure of workers and consumers to pesticides, amount of chemical applied, by reducing either the and there is an increasing body of information number of necessary applications or the rate needed describing the negative effects that pesticides can for each application. have on cropping systems and surrounding In each of these instances, the beneficial ecosystems. Cosequently, many older pesticides organisms must have a tolerance to the are no longer available for use, and registration of applied to control the weed. This is often the case new materials is becoming more difficult and with herbicides, since they usually affect only plants. expensive. It appears that despite the complexity of In some production systems, however, the beneficial biological control programs for aquatic weeds, such organisms may be affected adversely by an herbicide. methods will have to be utilized in future In such cases, it would be necessary to apply the management strategies. Fortunately, there are many organisms at suitable intervals after pesticide possibilities for this type of approach. application, or develop resistant strains of the Integrated pest management has been defined beneficial organisms. many different ways for different purposes. I will Biological control measures can also be used use the definition as proposed in a USDA report to minimize the potential of some herbicides to (1982) “... (the combining) of two or more pest increase other, nontarget, weeds. In plant pathology, suppression methods into practical systems of IPM this concept is termed “disease trading” (Kreutzer to reduce pest problems.” Although other definitions 1960). For example, applications of herbicides that may be more appropriate in other situations, the are specific for broadleaf weeds can lead to rapid goal here is to identify opportunities for effectively infestations of weedy grasses. Herbicide treatment combining biological control methods with other can reduce population densities of these broadleaf disease control strategies which are based on weeds which may be important competitors, not chemical, cultural, and genetic methods. only with the crop plants, but also other weed species. A similar situation occurs whenever land is Integration of Biological Control with severely disturbed. Many organisms, including Chemical Control weedy plant species, have developed specific life histories to exploit severely disturbed areas. Often There are many weeds which cannot be these species are considered r-selected species controlled effectively with present chemical (MacArthur and Wilson 1967), which have methods, often because of the toxicity of the characteristic traits such as rapid reproduction, chemicals to nontarget species or high costs. effective dissemination, and tolerance to conditions Biological control measures might be adopted most associated with disturbed systems. These species rapidly by growers in these instances because no often do not do well in undisturbed systems, usually chemical alternative would be available. An example because they are poor competitors in communities is the use of the rust fungus Puccinia chondrilina for of high diversity. the control of Chondrilla juncea (rush skeleton

211 Integration of Biological Control with should be much less specific, and selection for Cultural Control resistance should be less likely to occur.

Cultural controls are commonly used to create CONSTRAINTS TO DEVELOPMENT OF an environment which is not conducive to the BIOLOGICAL CONTROL development of weeds. Establishment of beneficial organisms within this environment might increase In most of the scenarios described, biological levels of weed control which cannot be attained by control can best be used to augment other weed the cultural practices alone. For example, water- control strategies rather than to replace them. hyacinth (Eichhornia crassipes) can be controlled However, the development of such augmentative by draining waterways for a period of time. However, biological control methods is difficult because of this method is very labor-intensive and is often not the complexity of biological systems and the impact practical, especially when considering the negative of economic and sociological factors. impact that such a practice has on the rest of the aquatic environment. However, if the repopulation Biological Limitations of the waterway by water-hyacinth could be reduced by beneficial organisms, from fish to fungi, it may Biological limitations on the biological control be possible to delay the need to repeat such a drastic of weeds are directly associated with the very practice cultural practice. of agriculture. As recognized by Feeny (1976), fast- Although many situations can be envisioned growing plants often rely on their “unapparency” as in which biological control could be integrated with a defense against natural predators. Unapparency is cultural control, the potential for integration may be defined as the period of growth during which the limited in some instances. In particular, it may be plant is not obvious to potential predators. For difficult to integrate biological control with cultural example, a plant that is susceptible to attack may practices designed to create environmental minimize the chance of encounter with its pests conditions unfavorable for a targeted weed, for it because it is small or present for a short period of may also inhibit the beneficial organisms. For time. In agriculture, this is achieved by planting example, irrigation during the fallow portions of the short-season crops, in which the pests do not have year is an effective way to induce rapid parasitism of enough time to reach economic levels of infestation. weed seeds. However, that very same moisture may Many of our crop and weed species depend upon a also serve as the necessary source of water needed low level of apparency in their natural ecosystems. for germination. A similar situation may occur However, agricultural practices such as monoculture when water is kept from a field to inhibit weed seed limit this protective factor, since plants become germination and growth. Such arid conditions would more apparent to pests when they are grown in also inhibit the naturally occurring or introduced monoculture systems. At the same time, cultural pathogens that may otherwise exact a toll on the practices may decrease the apparency of weeds as a weed population. result of the lush, high density growth of the crop. By the time the weed biomass is large enough to Integration of Biological Control with became “apparent,” economic damage to the crop is Genetic Control significant. One would not expect biological control strategies to be effective under such conditions. There are instances when it may be useful to Another important aspect of how the biology integrate biological control measures with plant of agricultural production systems limits the breeding programs. For example, in some breeding implementation of biological control is the concept programs it may be possible to select for plants of enemy-free space (Price et al. 1980). Organisms, which have allelopathic properties that reduce weed including weedy plants and their associated pests, populations. often disperse or evolve in various ways in order to Within each of these integrated strategies, escape their enemies. In the biological control of biological control should assist in management of weeds, it is imperative that the control agent be within weed populations. Many introduced and maintained in its own enemy-free chemicals have specific modes of action and can space, so that its unrestricted growth will have a rapidly select for portions of the plant population better chance of responding to any rapid increase in resistant to them. Interactions between a weed and the biomass of the weed. Goeden and Louda (1976) populations of one or more biological control agents felt when biological control of a weed fails after

212 introduction of an herbivore, which occurs about through new government policies and programs 50% of the time, it is due in part to the interference will these barriers be eliminated. by enemies of the herbivore control agent. Price (1981) applied the interactions between Economic Limitations natality, predation, and intraspecific competition to a three dimensional model. He concluded that for The economics of the development of strongly r-selected species (such as weeds) in biological controls for aquatic weeds are complex. unstable habitats, natural enemies have little or no The classic approach to biological control of weeds effect on the population dynamics of the weed. It is is based upon single releases of selected predators not until more stable, K-selected, communities or parasites which maintain themselves at population develop that natural enemies limit a population, densities high enough to effect economic control. which of course does not occur in the intensive Thus, the major expenses are incurred in the management of many crops, including rice. identification and release of the control agent; little Much of the research done in the last few or no costs are incurred after release. In contrast, decades has not addressed these complexities to the augmentative or inundative releases require that degree required to develop workable biological control agents be applied over large areas each time control strategies. Many organisms have been control is required. In this approach costs are selected as potential control agents on the basis of incurred throughout the period of control, not just limited greenhouse tests. When these organisms are during the research phase as in classical biological introduced into natural systems with variable control. This type of scenario is often more environmental conditions, it is very difficult to appropriate for private industry involvement and reproduce the level of pest pressure observed in the will require increased cooperation between the public intensively managed experiments. and private sectors. Under these constraints, biological factors determining the classic predator-prey/herbivore- Research Perspectives at the Population host relationships of population biology which have Level been applied successfully to the control of insects and weeds in low-input systems are not as helpful Solutions to sociological and economic when we are investigating the control of aquatic constraints lie largely outside the realm of biology, weeds in high-input, rapid turnover systems. and will not be discussed further here. However, Unfortunately, few models exist which describe the constraints which are imposed by biological complex biological interactions in relation to complexity might be better understood if we adopt biological control of aquatic weeds. new approaches to their study. Much has been accomplished at the organism level in developing Sociological Limitations an understanding of types of interactions which can take place between a plant and its enemies. However, The implementation of workable biological more work needs to be done to develop insight into control strategies has also been constrained by the types and numbers of interactions which take sociological factors, although more so for the use of place at the population and community levels of beneficial plant pathogens than for beneficial insects. biological organization. Much more attention should Generally, the complexity of the microbial world be focused at these levels of examination – and the insidious nature of diseases produced by particularly within spatial and temporal frameworks. microorganisms are misunderstood by the public. Because of the limited opportunities to manage This is not a trivial situation. It has resulted in weed populatins over extensive areas, many control extremely broad government regulations that are strategies have focused on the protection of specific stricter with regard to the registration and importation fields. This reduces greatly the spatial dimensions of , fungi, viruses, and nematodes than of a pathosystem, and is an approach commonly those for plants and animals. These constraints used with chemical control. However, biological make research difficult, decrease the alternatives control methods may best be developed at the available for selection of possible control agents, regional or ecosystem level. The use of refuges and and in general, increase the costs of bringing a staggered crop periods can maintain a high level of product to market. A similar situation exists when beneficial control agents from year to year, thus we try to develop effective biological control agents minimizing the temporal enemy-free space available utilizing the tools of genetic engineering. Only to the weed.

213 Development of successful protective successful biological control strategies depends on strategies will depend on knowledge of the evaluating systems at many levels, ranging from the population behaviors of beneficial organisms and overall crop system to the microsite where the the weeds. The in vitro methods of screening for interaction occurs. Consideration of behavior at antagonists which have been used historically may these levels within the framework of population and not be the best approach. Much more attention must community concepts should assist in developing be given to the behavior of potential beneficial principles of biological control which are applicable organisms in situ. Studies are needed to determine across a range of agricultural systems. Within this how beneficial organisms survive under adverse framework it should be possible to move beyond the environmental conditions, how rapidly they increase empirical approaches used so often in the past. their populations, how the maintain these populations under favorable conditions, and how they interact FUTURE RESEARCH DIRECTIONS with weed populations under variable conditions. For biological control of aquatic weeds to be RESEARCH PERSPECTIVES AT THE a valuable tool in integrated pest management, the COMMUNITY LIVEL approach to the study of integrated pest management itself may need to be redirected. Levins (1986) Interactions between populations of beneficial makes the case for an ecological approach to organisms and weeds do not occur in isolation from agriculture. Until now, integrated pest management populations of other organisms. It is likely that has been applied to production practices which interactions between these groups of organisms in a were developed during a period when pest community will determine the success of a biological management in agricultural systems focused on control strategy. Therefore, the complexity of an elimination or control of single pests independently. agroecosystem must be considered in biological It may be more productive to approach agriculture control research. itself as an ecological system in which diversity, An ecological continuum exists in crop long term dynamics, and social goals are considered production systems ranging from the very simple to within the framework of community concepts. the very complex. In a simple agricultural system, Not only is the ecological approach desirable, such as hydroponic culture, biological diversity is but now for the first time it may be possible. The very low and environmental conditions may be rapid development of advanced instrumentation, relatively homogeneous and strictly controlled. such as field computers which can monitor a myriad Conversely, in a perennial forest system, there is of environmental conditions at short time intervals, great diversity in the abiotic and biotic conditions. has had a tremendous effect on how we produce Regardless of the complexity of a production crops and control their pests. The areas of applied system, strategies for optimizing interactions and mathematical ecology, combined with the between populations of beneficial organisms and tremendous computing power now available, put targeted weeds will have to survive severe time series analysis, geostatistics, simulation models, perturbations of the system. Most agricultural and complex sampling strategies within the grasp of practices severely disturb an agroecosystem, thus every grower. These new methods of understanding interrupting the natural species interactions that agricultural communities will enhance the potential would have otherwise taken place. Since classical to apply biotechnology to crop production. biological control is more susceptible to Ultimately, the integration of biological control perturbations, it is usually assumed that the with other aspects of crop production may enable us inundative or augmentative approach would be more to develop production systems which approach the appropriate for a cropping system that experiences lofty goal of sustainable agriculture. severe perturbations. However, this may be in part because most biological control agents have extremely specific host ranges. Endemic, broad REFERENCES host range organisms may actually increase their negative impacts on the pest if a perturbation, such Emge, R.G. and G.E. Templeton. 1981. as irrigation, were applied at the appropriate time Biological control of weeds with plant and under the right conditions for the control agent pathogens. In: Beltsville Symposia in to attack the plant. Agricultural Research 5, Biological It should be evident that the development of Control in Crop Production, G.C.

214 Papavizas (ed.). Allanheld Osmun, Princeton University Press, Princeton, New Granada, USA, pp. 219-226. Jersey, USA. Feeny, P. 1976. Plant apparency and Price, P.W. 1981. Relevance of ecological chemical defense. In: Biochemical concepts to practical biological control. Interaction Between Plants and Insects. In: Beltsville Symposia in Agricultural Recent Advances in Phytochemistry 10, Research 5, Biological Control in Crop Plenum Press, New York, USA, pp. 1-40. Production. G.C. Papavizas (ed.). Goeden, R.D. and S.M. Louda. 1976. Biotic Allanheld Osmun, Granada, USA, pp. 3- interference with insects imported for 19. weed control. Annual Review of Price, P.W., C.E. Bouton, P. Gross, B.A. Entomology 21: 325-342. McPheron, J.N. Thompson, and A.E. Kreutzer, W.A. 1960. W.A. 1960. Soil Weis. 1980. Interactions among three treatment. In: Plant Pathology, An trophic levels: Influence of plants on Advanced Treatise. Vol. 3. J.G. Horsfall interactions between insect herbivores and and A.E. Dimond (eds.).Academic Press, natural enemies. Annual Review of New York, USA, pp. 431-476. Ecology and Systematics 11: 41-65. Levins, R. 1986. Perspectives in integrated Supkoff, D.M., D.B. Joley and J.J. Marois. pest management: From an industrial to 1988. Effect of introduced biological an ecological model of pest management. control organisms on the density of In: Ecological Theory and Integrated Pest Chondrilla juncea in California. Journal Management Practice. M. Kogan (ed.). of Applied Ecology 25: 1089-1095. John Wiley & Sons, New York, New USDA. 1982. Crop Protection-Annual York, USA, pp. 1-18. Report. United States Department of MacAurther, R.H. and E.O. Wilson. 1967. Agriculture, Agricultural Research Service, The Theory of Island Biogeography. Washington, D.C.

215 DISCUSSION

Dr. Baki asked about the probable reaction of politicians to biological control. Dr. Marois informed the meeting about the influential lobbies in Washington working to promote acceptance of biological methods in USA. He pointed out that government policy in most countries is concerned to minimize the risk of overproduction, as well as the risk of underproduction. Dr. Baki agreed, but felt there is a serious dichotomy between the developed world, where there are powerful pressure groups working to promote research and development in biological control, and less developed countries where there seems to be little or no pressure on governments to promote biological control. With regard to the protocols for integrated weed management, Dr. Moody pointed out that any system has to be simple. Farmers are unlikely to reject a laborious procedure such as counting weeds in the field. Dr. Marois agreed, and suggested that the most difficult part of research is often simplifying it and explaining it clearly to those who will use the technology. He suggested that advances in computer technology have meant that it is now easy to use computers in highly complex systems. More information specialists are needed, to simplify information into a “sound bite”.

216