SCOPE 49 - Methods to Assess Adverse Effects of Pesticides on Non-target Organisms  

1.1 INTRODUCTION

For purposes of this discussion, a pesticide is any compound or formulation used to control pests which contains active ingredients and other substances (e.g., solvents, emulsifiers, buffers) to aid its delivery to target organisms and hence minimize pests. The major types of pesticides are herbicides, fungicides, rodenticides, molluscicides, soil bacteriostats, disinfectants, and living organisms with pesticidal activity. In practice, mixtures of pesticides rather than single agents are often applied; this practice can lead to synergism or potentiation resulting from interaction between pesticides or among the ingredients of a formulation.

Through the careful use of pesticides, humans have benefited considerably by having an increased abundance of assorted foods. In some places, pesticides have assisted in assuring a continued supply of nutriment to the local population. An estimated 5 million tons of pesticides have been applied to world agriculture. Yet, pests around the globe still destroy about 35 per cent of all potential crops before harvest, indicating that the use of pesticides has been only marginally successful at improving agricultural productivity.

People cannot survive with only their plants and livestock. Natural biota in the ecosystem number 510 million species in the world and 500 000 in the United States alone. Most of these natural species are essential for a quality environment and the survival of humankind. Natural biota perform a diversity of essential tasks including: decomposition of wastes, recycling nutrients, maintenance of biological diversity, stabilization of soil and water resources, continuation of energy flow in natural ecosystems, pollination of crops and natural vegetation, and stabilization of climatic conditions.

*This section was prepared by R. Albert, S. Baker, J. Doull, G. Butler, N. Nelson, D. Peakall, D. Pimentel, and R. G. Tardiff.

Despite their value to agriculture, pesticides have also in some circumstances posed direct and indirect threats to the health of humans and to the environment around the world. Workers, because of ignorance or neglect, have been injuredeven killedby pesticides as a result of improper mixing, loading, and application techniques. At times, those consuming pesticide-tainted foods have been over-exposed, even to the point of illness. In other circumstances, pesticidesagents generated to destroy unwanted organismshave destroyed beneficial organisms in the delicate web of nature, leading in some instances to changes in the human environment that reduce, rather than promote, human well-being. These beneficial species are the non-target organisms (NTO) which are the subject of this report.

The occurrence of such unwanted side-events is of sufficient magnitude to warrant attention from scientists and public officials alike to improve the safety in the manufacture, use, and disposal of pesticidal substances. This volume is dedicated to that objective. In Chapter 2, the ways by which humans come into contact with pesticides are addressed, as are the scientific procedures by which human exposures can be documented to determine later whether injury to people and their environment has been, or is likely to be, manifest. Chapter 3 is devoted to an analysis of the intricacies associated with documenting injuries to humans exposed either only one time or repeatedly for the major part of a lifetime. Chapter 4 pays comparable attention to diverse approaches by which to measure injurious changes at various locations of ecosystems, upon which people depend inextricably for growth and development of a global civilization. Chapter 5 provides an overview of integrated pest management, a complex practice that makes more efficient use of pesticides and reduces the likelihood of over-exposure of humans and other non-target organisms.

Presented below is the consensus view of a global representation as to the major conclusions and recommendations associated with the impacts of pesticides on non-target organisms.

1.2 GENERAL CONCLUSIONS 

1.2.1 PESTICIDE USE

1. Approximately 1000 pesticide formulations are in use throughout the world today for virtually all forms of agricultural commodity. The annual worldwide agricultural use of pesticides has been estimated to be of the order of 5 x 10⁶ tons with a value of about $16.3 billion (US).

2. Despite the use of pesticides, about 35 per cent of crops have been estimated to be lost. Nearly 50 per cent of food in the world may be lost annually despite all pest control procedures. It has been estimated that less than 0.1 per cent of the pesticides applied to crops reach the target pests; thus, more than 99 per cent of applied pesticides have the potential to impact NTOs and to become widely dispersed in the environment.

3. Delineating toxic effects of the use of any pesticide is complicated by the existence of some 510 million species in the environment, most of which are potential unintended targets of the toxicity of pesticides.

4. Approximately 5 million ton of pesticides (perhaps 70 per cent herbicides and only 5 per cent insecticides) are applied annually in the world, of which about 70 per cent is used for agriculture, and the remainder by public health agencies and government agencies for vector control and by home owners. Agriculture and forestry, which occupy approximately 70 per cent of the land area in some countries, are the primary source of pesticides in ecosystems.

1.2.2 INJURIES TO HUMAN AND NON-HUMAN NTOs

1. In developing countries, acute pesticide poisoning is a major public health problem, because it is so frequent (i.e., more than one million cases annually in the 1980s). Classically, acute toxicity has been restricted to morbidity and mortality in those individuals exposed directly; recently, that definition has been enlarged to include injury to developing fetuses.

2. Although not yet well documented, pesticide-induced, chronic toxicity is emerging as a public health concern of major proportions. The toxic manifestations that capture the greatest attention include cancer, reproductive impairment, and irreversible neurotoxicity.

3. Acute and chronic injury to non-target organisms other than humans has been pronounced over the past few decades. The most affected organisms have included fish and birds; and the most prevalent mechanisms of such damage have been depression of reproduction of beneficial organisms and stimulation of reproduction of natural enemies.

4. The extent of ecosystem damage is illustrated by the observations that invertebrate NTOs are often killed by pesticides used against insects and acarine target pests; foliar applications of broad spectrum insecticides produce nearly total depletion of arthropod populations in crops such as cotton; microorganisms are most susceptible to fungicides and bactericides aimed at target plant pathogens in the field.

5. The measurement of adverse consequences in ecosystems is extremely difficult because of the biological complexity of the biosphere. Consequently, considerable resources need to be directed to efficient and reliable methods to identify early effects that may propagate injury throughout the ecological web. 

1.2.3 CONTROLLING EXPOSURES TO PESTICIDES

1. Damage caused to NTOs from the use of virtually all forms of pesticides is large and needs to be reduced appreciably in developing and developed countries. The costs of such unwanted injuries are enormous.

2. Reductions in exposures to pesticides used for agriculture and in the home are possible through education about the proper use of pesticides, the use of application techniques that reduce the environmental dissemination of aerosols, liquids, and powders, and the appropriate use of protective equipment.

3. Limitations on the overall use of pesticides is not only desirable but also achievable through the diverse approaches offered by integrated pest management.

4. The use of techniques developed for recombinant DNA in the biological control of plant pathogens is currently a promising area of research in both academic and industrial institutions. The application of molecular genetics to selected biocontrol systems can potentially provide an understanding of the genes involved in biological control phenomena; an establishment of a genetic basis for biological control is a prerequisite to further molecular studies that centre on the enhancement of biological control phenomena.

1.2.4 ASSESSING EXPOSURES TO PESTICIDES AND ASSOCIATED UNCERTAINTIES

1. Two major approaches exist by which to determine the means through which NTOs come into contact with pesticides and the doses that the NTOs obtain: (a) computerized modelling of the numerous phases of environmental fate and transport, and (b) monitoring specific NTOs for the presence and concentration of pesticides of interest.

2. Models are available at three levels of sophistication, from the more qualitative to the most rigorous quantitative site-specific models. Level three is the most data-intensive, level one the least. While level one models are useful to obtain a sense of trends, site-specific models are needed to provide accurate and precise estimates of exposure that permit an authoritative evaluation of possible damage to NTO species such as humans.

3. The validation of computer models remains a difficult and challenging prospect, because the complexity of environmental processes that govern mobility of chemicals is still poorly understood. Nevertheless, progress is being made in predicting, with substantial quantitative accuracy, exposures in environmental compartments of limited scope.

4. Monitoring represents the most confident means of describing the degree and magnitude of exposures to humans and other species. However, such an empirical approach is quite costly.

5. In humans, exposures are characterized either at the human interface by monitoring the presence of substances in media such as air, food, water, and contact surfaces in the human environment (this is known as `media monitoring') or within the organisms of interest by measuring the presence of pesticides in easily obtainable samples of biological materials such as urine, blood, hair, adipose tissue, and breast milk (`biological monitoring'). Despite the need to assure the application of appropriate ethical constraints to the use of biological monitoring, this approach provides the most precise estimate of dose to the individuals of interest.

6. Of the two approaches, modelling and monitoring, the latter generally contains fewer uncertainties in fully characterizing the patterns of exposure to pesticides.

1.2.5 ASSESSING ACUTE TOXICITY FOR HUMANS

1. The adverse health effects of acute exposure are generally well recognized. Although the incidences of mortality and morbidity are more severe in developing countries, the primary effectsinsecticide-induced neurotoxicity and dermal toxicityare universal.

2. Most known associations of pesticides with neurological effects involve insecticides. Neurotoxicologic methods currently under development provide the opportunity to characterize neurotoxicity for other pesticide classes and to enhance our understanding by examining neurologic endpoints, other than those that are cholinergic, such as behaviour.

3. The clinical features of dermal toxicity are moderately well characterized. Techniques exist to determine skin penetration, correlation of urinary metabolites with dermal exposure, and histological changes after exposure. However, techniques to determine cellular proliferation, the presence of biomarkers, and allergic reactions of skin are presently inadequate.

4. The impact of pesticides on the immune system is less clear than that on other organ systems.

5. Biomarker techniques and toxicokinetics can help to enhance the predictive value of risk assessments for acute exposures and effects.

1.2.6 ASSESSING CHRONIC TOXICITY FOR HUMANS

1. Interference with normal reproduction and development from the manufacture, use, disposal, and misuse of pesticides is a rapidly growing area of concern to public health officials and toxicologists. As the database has grown, the level of concern has increased rather than decreased.

2. A significant shortage exists of epidemiologic studies on exposed humans and of animal toxicologic studies using state-of-the-art methods. Actually, for most pesticides and other chemicals in the environment, epidemiologic data confirm neither the absence nor presence of significant risk, because of (a) the high background and variability and adverse reproductive events in humans, (b) the problems posed by confounders, and (c) the limited power of many epidemiology study designs.

1.2.7 ASSESSING DAMAGE TO ECOSYSTEMS

1. Methods to detect and quantify damage caused by pesticides on terrestrial and aquatic ecosystems are complex and costly depending on the species involved and the pesticides that are targets of investigation.

2. Because less than 0.1 per cent of all applied pesticides are estimated to reach target pests, more than 99 per cent contaminate the environment and are available to disrupt various natural ecosystem processes.

3. Pesticides injure particular ecosystems by upsetting natural stability, destroying natural enemies and key species in the ecosystem, and altering normal trophic structure resulting possibly in the resurgence and outbreak of undesirable species.

4. Furthermore, pesticides may influence the normal decomposition of organic wastes produced by humans, livestock, and other biota. The resulting situation may lead to accumulation of organic wastes and pollutants in the environment. One consequence may be a reduction in the productivity of the ecosystem, because of a critical shortage of elements necessary to support life.

5. Common pesticides may reduce the diversity of food chains, including reductions of parasites and predators at the top of the food chain. In certain cases, this alternative may result in excessive numbers of organisms at the low end of the food chain.

6. Energy is an essential requirement for the normal function of all natural ecosystems. In some situations, pesticides, like herbicides, may reduce plant populations and thus the primary food production. Therefore, the total productivity and survival of a natural ecosystem may be influenced adversely. 

7. Cross-pollination is essential to the reproduction of many plants. For example, 90 US crops, valued at $20 billion (US) (in 1988 dollars), are dependent upon insect pollination (mostly wild bees and honey bees). In addition, a large number of wild plants depend upon insect pollination. Pesticides may upset this delicate balance.

8. The implications of the above observations for those who choose to use predictive models in the assessment of exposure are that it is unlikely today that models of complex environmental systems will have the precision required to predict ecosystem exposure patterns in widely different ecosystems to chemicals with widely differing properties. However, comparative qualitative models for preliminary assessment of trends and optimization of monitoring programs can be useful.

9. There is a need to refine (a) correlative relationships based on calculated properties of a chemical and (b) empirical data on the properties of both chemicals and ecosystems. Carefully constructed and performed studies on models describing kinetics of processes, rather than models of environmental systems, are undoubtedly the most important step in expanding our predictive capabilities.

10. Situation-specific models of troublesome situations for comparative purposes have a role. Such models can provide tests of the usefulness of the data, and form a basis for the prediction of patterns from one chemical to another. 

11. Model validation is dependent on carefully designed field experiments that examine pollutant levels under conditions producing significantly different exposure patterns.

12. Models of environmental systems must depend largely on empirical determinations of the descriptive processes. Hence, the results will be highly system-specific. This outcome makes their use unreliable to predict patterns in highly differing ecosystems. Yet, highly predictive models can be established for a specific ecosystem, if sufficient effort is focused on characterizing the processes.

13.  Some progress has been made to introduce (a) insect development inhibitors, many of which are very selective and nonpersistent, (b) genetically engineered microbes and plants with insecticidal activity, and (c) pesticide resistance in plants, natural enemies, and chemical ecology mediators. Evidently, these approaches are also subject to developed resistance in pests; thus, caution must be exercised in their management. In general, there is a great need to improve understanding of the factors most influential in the perturbation of ecological systems by pesticides and in developing less disruptive pesticides.

1.2.8 INTEGRATED PEST MANAGEMENT

1. Winning increasingly broad support are alternatives to conventional agriculture, often referred to as integrated pest management (IPM) which minimize the use of pesticides.

2. IPM prescribes six forms of controls: cultural, biological, behavioural, biotechnological, environmental, and chemical.

1.3 GENERAL RECOMMENDATIONS

1.3.1 CONTROLLING EXPOSURES TO PESTICIDES

1. As a prerequisite, the development of either new pesticides or new uses of existing pesticides should include means for exposure control proportional to the hazard potential of the chemical. This effort should consider physical form, prepackaged quantities for direct use in the field, closed transfer systems, and application procedures that deposit the pesticide primarily on a specific target. 

2. The success of procedures for pesticide exposure control depends on a proper understanding and motivation of individuals using these substances. Rudimentary education is needed to impart general principles to prevent exposure; these fundamentals can be presented through visual and textual aids and in the language and social style of the populace. The recent initiative under the aegis of the Food and Agriculture Organization (FAO) is an example of this approach.

3. High priority should be given to developing pesticides with increased selectivity toward pest species and greatly reduced damage to non-target species. Furthermore, pesticide management should increasingly prevent the development of resistance in pests, because this phenomenon impairs selectivity.

4. State-of-the-art technologies to apply pesticide are designed to reduce the potential for human exposure. The best available and most cost-effective technologies should be applied to reduce the occurrence of acute poisoning, and new technologies should be encouraged to continue reduction of exposures.

1.3.2 ASSESSING EXPOSURES TO PESTICIDES AND UNCERTAINTIES

1. An international agency, such as the United Nations Environmental Program (UNEP) or the Organization of Economic and Community Development (OECD), should conduct a workshop aimed at developing environmental sampling guidelines for monitoring studies. Participants should include regulatory officials, modellers, epidemiologists, and chemists.

2. Improved methods are necessary on an international scale to provide developing nations with the capability to screen dietary exposures and identify sources of potential hazard in the diet.

3. Serious attention must be given to the effects of pesticide exposures on subgroups, such as infants and children, who are known to be exposed to relatively higher doses of pesticides through dietary and household exposures.

1.3.3 ASSESSING ACUTE TOXICITY FOR HUMANS

1. To characterize the problem of acute pesticide poisoning, conventional public health practices must be monitored. Recognizing that there are geographic, population, climatic, and agricultural differences around the world that influence patterns of pesticide usage, the best approach to study acute pesticide poisoning is from the `bottom up', i.e., beginning at the local level with support from state and national levels.

2. Many immunotoxicity procedures have been developed for classes of chemicals other than pesticides. These techniques need to be adapted to examine the response of the immune system to pesticides. Because of evidence of auto-immune responses in humans after exposure to pesticides, reliable animal models are needed to detect and quantify such effects in a manner predictive of human responses. Newer biochemical techniques need to be incorporated into the investigation of pesticidal effects on the immune response.

3. While technologies for measuring the effect of chemicals on immunosuppression and immunosensitization exist, they have yet to be validated or used to examine the effects on the immune system of acute exposures to pesticides. Measuring functional impairment of the immune system should be part of the evaluation of pesticide toxicity.

4. Tests of acute toxicity in major organs such as the lungs (except for the paraquat effect), blood and blood-forming tissues, the cardiovascular system, kidney, endocrine organs, and musculoskeletal system need to be part of test batteries.

5. Adequate techniques are unavailable to determine in skin cellular proliferation, the presence of biomarkers, and allergic reactions; hence, research is needed into the numerous functions of skin.

1.3.4 ASSESSING CHRONIC TOXICITY FOR HUMANS

1. For the spectrum of pesticides, reproductive and developmental toxicity should be assessed in animals and humans.

2. The current assessment of developmental toxicity focuses primarily on structural rather than functional endpoints. Methods are needed to assess the effect of in utero exposure on the functional development of organ systems in addition to the nervous system.

3. Reproductive toxicity screens should be expanded beyond tests in rodents used to evaluate fertility. Specific methods must be enhanced to detect effects on spermatogenesis and oogenesis to help identify site(s) of action of reproductive toxicants and to distinguish primary (i.e., direct effect) from secondary (i.e., due to other toxicity) reproductive toxicants.

4. Animal models are needed to evaluate the effect of pesticides on lactationboth on its quality and as a source of exposure of neonates to chemicals in the milk. Human milk is an extremely important source of nutrition worldwide, and is probably the most critical source of exposure to neonates, a highly vulnerable age-group.

5. Further development and validation of in vitro tests for developmental toxicity is strongly recommended. Test systems which provide useful mechanistic data would potentially improve our understanding of those mechanisms by which developmental toxicity is caused in animals and humans.

6. Improved reliability is needed for short-term in vitro and in vivo qualitative and quantitative tests for promoters of cancer.

7. Reliable short-term in vivo qualitative and quantitative genotoxicity tests are needed to detect and quantify oncogenes and anti-oncogenes; for in vitro genotoxicity tests, research should focus on quantitation of cancer potency. 

8. The current scientific basis should be greatly enhanced to extrapolate carcinogenic responses from laboratory animals to humans and to extrapolate effects at high doses to those at low doses.

9. Additional epidemiological studies are required of pesticide-exposed populations to establish the presence or absence of cancer induction.

10. Biological markers of carcinogen exposure and effect need to be improved, particularly to detect changes that occur early in the latent period.

11. Public health should be promoted by implementing appropriate monitoring and epidemiologic surveillance, initially to identify improved control measures.

12. In developing countries, local pesticide control boards should be established with representation of all interested parties having authority to implement and supervise the policies and regulations established by national regulatory agencies.

1.3.5 ASSESSING DAMAGE TO ECOSYSTEMS

1. The ecological consequences of pesticide use must be evaluated from the level of a single species to that of multiple species and finally to the level of the ecosystem. Many methods are available to test for susceptibility of NTOs, and some tests are already required for pesticide registration. The effects of pesticides on ecosystem structure and function should be measured in the agroecosystem of interest for a pesticide. Decisions on surveillance of the broadest ecosystem should be based on the hazard of each pesticide.

2. Microcosm studies cannot be relied upon solely to determine complex ecosystem responses to pesticides; however, microcosm methods are appropriate, and are recommended for general information on the relative persistence, bioaccumulation, and ecological kinetics of pesticides in model organisms.

3. Studies of soil subsystems are recommended, because direct and indirect complex processes are caused by pesticide treatments and their residues. Changes in the community structures of soil biota are reflected by altered biological and chemical processes, as well as by their rates of change. These changes could be measured in microcosms (e.g., leaching of nutrients and humic substances) and, albeit less easily, in the field by changed ecosystem parameters such as diversity, CO₂ production, and decomposition rate.

4. The development and application of genetically engineered pesticidal organisms require research to evaluate ecological risks, if any, posed by such organisms. Risks should be evaluated on the bases of (a) ecosystem effects, (b) fate and survival of population, (c) intraspecies and interspecies gene transfer, (d) contaminant and mitigation, (e) transport and dispersal, and (f) detection and enumeration. 

5. Natural ecosystems must be investigated and protected from pesticide damage, because they play an essential role in maintaining a quality environment for humans, agriculture, and forestry.

6. A distinct need exists for a widely accepted procedure to assess ecological effects of pesticides on NTO species in terrestrial and aquatic ecosystems. From the myriad of possibilities that could comprise ecosystem effects, certain factors should receive priority and are amenable to research using biogeochemical cycling, trophic structures, decomposition rates, and transport into non-target environments.

1.3.6 INTEGRATED PEST MANAGEMENT

1. To alleviate public and scientific concern, prior to the approved release of engineered microorganisms into the environment, the efficacy and safety of biological control agents should be fully evaluated, and the risks and benefits carefully assessed.

2. To implement biological control programs based on the biotechnology of IPM, the following must be improved: (a) understanding of total ecosystems, (b) mass production and delivery of control agents, (c) selection and enhancement of control agents, and (d) the specificity of control agents to only one disease on one crop in a small geographic area.