Disease, Pests and Impact Assessment

Paul R. Epstein, M.D., M.P.H.
Associate Director

Center for Health and the Global Environment Harvard Medical
School Oliver Wendell Holmes Society
260 Longwood Avenue Boston, MA 02115
Phone: 617-432-0493 Fax: 617-432-2595 E-mail:pepstein@igc.org

As currently performed, risk analyses of chemicals in the environment account only for direct effects: cancers, birth defects, premature births, etc. But chemicals like dioxin, PCBs and pesticides may have even greater indirect affects on emerging infectious diseases. Through immune suppression and by mimicking hormones, these chemicals may affect bird and fish populations -- not merely as sentinels of future human impacts. Weakened bird populations may harbor an elevated burden of viruses (e.g., Eastern Equine, Western Equine and St. Louis Encephalitides); and, with reduced numbers of inland fish (consumers of insect larvae), mosquito carriers may flourish. Morbilliform viruses (measles) have been fatal to aquatic and terrestrial mammals (Australian horses, Serengeti lions), and an iridovirus may be involved in the disappearance of frogs from six continents. How do these evolving pandemics across a wide taxonomic range reflect altered agents, weakened hosts and environmental change?

True impact assessment must include ecological impacts, not merely for aesthetic reasons, but for the biological control of opportunistic pests and pathogens. Owls refuged in Northwest forests, for example, control rodent populations involved in Lyme disease and Hantavirus events that occur elsewhere. To fully assess impacts, obvious first order results must be integrated with background changes, such as habitat loss that crowds bird populations thus amplifying contagion, and wide temperature fluctuations and altered timing of the seasons (climate instability) that disturb species' synchronies.

Thus assessing the impacts of change on pests and infectious disease patterns is important for assessing the full impacts of our actions on the set of interacting complex systems that make up our world.

Ecology, pests and disease

Rejecting the "central dogma" that all information flows from genes to proteins, Barbara McClintock helped us understand that genes are expressed and repressed, regulated and controlled by other genes; that they "jump" (transposition) and, perhaps, even mutate more rapidly than random in response to environmental pressures, perturbations and nutrient availabilities.

The same is true on a macro, phenotypic level as the pattern of a stand of trees or a colony of fire ants forms in relation to the environment, competitors and nutrients. We now know that "survival of the fittest" includes how organisms and species fit and co-evolve in complex ecological systems, not just that they fight themselves with the strongest surviving. Competition and cooperation, symbiosis and mutualisms are necessary within nuclei, within cells, within the body, within ecological systems (in networks involving several species) and indeed to create a functioning, self-regulating and sustainable biosphere. Biological control of opportunistic species requires an intact "immune" system in nature, just as a healthy body needs a diversity of vigorous responses to microbiological intruders.

Weeds, rodents, insects, fungi, algae, protozoa, bacteria and viruses are opportunistic species. According to ecologists, these organisms exhibit r-selection; i.e., they grow rapidly, are small in body size, have huge broods and good dispersal mechanisms (thus high r, the intrinsic rate of increase). Rs are good colonizers of disturbed environments and of weakened hosts. Species exhibiting K- selection are larger, reproduce later in life and are slower to develop, but are good competitors in a stable environment. Rs would proliferate exponentially if not kept in check by the Ks through predator/prey relationships and competition, the systems of biological control or the "immune" system of the environment. As "specialists" dependant on localized niches, predator Ks are ultimately more fragile than their opportunistic prey. The rs are "generalists" with wide ranging diets (some decomposers), and dominate over Ks in disturbed, fragmented or polluted environments; and those undergoing climatic change.

The Volterra predator-prey relationship is an ecological principle fundamental for understanding disease emergence and resurgence. When predator and prey are both reduced from habitat fragmentation, pesticides, or climate extremes, the prey -- more rapidly reproducing and evolving (resistance) -- can rebound with punishing ferocity. Additionally, population dynamics of predators, prey and competitors cannot be modeled without inclusion of refuges, (and camouflages) and migration. Habitat reserves are necessary, for example, to preserve large raptors (e..g., owls) that control rodent populations elsewhere.

Many diseases of plants, birds, fish and mammals are indicators of environmental ill-health as a result of direct effects on toxins or indirect effects on species composition and selection. The factors regulating the abundance of species, including parasites and pests, are: 1) nutrients (chemical), 2) competition, predation and disease (biological), and 3) meteorological conditions and habitat (physical). A disturbance in one factor is destabilizing; multiple perturbations affect the resilience and resistance of a system.

Stressors and responses occur in biogeochemical and social/economic/political realms. Inputs (e.g., chemicals) or resource depletion have direct and indirect local impacts. Widespread perturbations (e.g., fossil fuel pollutants, deforestation) affect ecosystems. When changes involve biotic feedbacks and occur on a global scale, they can affect the climate system. Periods of ecological change may be associated with extinctions of some species and the emergence of new ones; in particular, pests and pathogens. An altered balance of species combined with a stressful environment may increase the selection of opportunistic and toxin-producing organisms, and contribute to the redistribution of vectors and animal reservoirs of disease.

Biological indicators

Insects are especially sensitive biological indicators in terrestrial ecosystems, given their short generation time and environmental-hardiness. With thresholds and optimum ranges in bioclimatic conditions (temperature, humidity and wind) determining their maturation, intrinsic parasite incubation and biting behavior, and control of their abundance being a function of predator/prey relationships, insect populations rapidly reflect ecosystem health. Paleological records support a strong link between past climatic transitions and increases in insect fauna. Rodent populations in arid rural - and urban - settings are another group of rapid responders to environmental change (e.g., food supplies and wastes) and altered biodiversity (loss of predators). In coastal marine systems algae are key indicators of ecosystem integrity, and the incidence and abundance of toxic algal species may reflect adaptive responses to enhanced environmental stress and altered biodiversity.

Moreover, insects and rodents are carriers of many plant and animal (including human) viral, bacterial, rickettsial and parasitic diseases, and some are avid consumers of vegetation. Algae transport Vibrio cholerae and other human enteric pathogens, and harmful species emit biotoxins that affect finfish, shellfish, marine mammals, sea birds and humans.

Combining the surveillance of biological indicators and relevant health outcomes (to include food security and nutrition) with ecological and meteorological data sets can strengthen an integrated assessment of climate and ecosystem change, provide a basis for calculating the costs of climate change, contribute to the detection of climate change ("fingerprints"), and support a systems-based approach to the design of adaptive and preventive responses to ecosystem management and environmental change.

Biological indicators and environmental monitoring

Bioindicators have primarily been used to monitor environmental accumulations of chemicals. But biotic responses are also integrators of ecosystem vulnerability and stresses endured. Monitoring key species that respond rapidly to environmental change (e.g., insects, rodents - urban and rural - and algae) can facilitate impact monitoring, climate change detection and the design of adaptations, mitigations and preventive interventions that improve generalized resistance (e.g., to invasion of exotic species).

Some such efforts are currently in the planning or early implementation stage. A network of regional centers with support from the World Climate Program (Global Climate Observing System or GCOS) is being planned to monitor meteorological data. Other programs are planned to monitor ecosystem integrity and biodiversity (Global Terrestrial and Ocean Observing Systems or GTOS and GOOS), augmented by remote sensing assimilated into geographic information systems. The Global Change System for Analysis, Research and Training (START) program of the International Geosphere-Biosphere Program (IGBP) will involve 13 Regional Research Networks, numerous Regional Research Centers and affiliated Sites. At the same time the Centers for Disease Control and Prevention (CDC) and the World Health Organization are planning an international Consortium of regional centers to monitor health from a clinical, laboratory and epidemiological perspective.

The principles of examining marine, terrestrial and ice-covered systems may be extended to monitoring on regional scales. In 1994, for example, Large Marine Ecosystem (LME) monitoring, funded by the Global Environment Facility, is scheduled for the Gulf of Guinea. Proposals are being submitted for the Chinese Yellow Sea and the Black Sea, with the intention of extension to the world's 49 LMEs under the GOOS. The relative value of the driving forces in each system (e.g., overfishing, pollution, habitat loss and climate) will be evaluated in order to inform policies for mitigation and prevention. Monitoring plankton, bivalves and finfish for biotoxins and vibrios, and surveillance of coastal nations for relevant health outcomes, will form an integral part of these projects.

Monitoring by ecosystem involves a number of strategies, including ecosystem status monitoring (extent, distribution and rates of loss [or gain]), fragmentation and edge effects by remote sensing and fractal dimensions analysis of landscapes, carrying capacity (storage), intensity (processes and functions), and population-community (biodiversity) indices. Stresses and perturbations may be site-specific and generalized and time series are needed to detect shifts and early warning signs. Analytical methods utilized are canonical, cluster, discriminant and principal component.

For each region, primary, secondary and tertiary driving forces of environmental change will differ. Among the principal forces are extraction of non-renewable resources, exploitation of renewable resources, and the generation of waste beyond the environment's capacity to assimilate it. These forces are sometimes "exported" to other regions, through the import of goods or exports of aerosolized, liquids and solid wastes. These driving forces are all influenced by population growth, affluence and development practices, poverty, culture and beliefs, behavioral and technological changes, economic policies, and political will.

CONCLUSIONS

To provide an integrated assessment of the human impacts of our interventions in the environment, information on health outcomes and biological indicators must be "fused" with data sets on ecology and meteorology. Following human population abundance, density, composition and movements are essential for projecting inputs and demands.

There are practical applications for future scientific inquiry and for ecosystem management. Integration can be applied on national levels through coordination of programs, including weather stations, environmental resource managers and agricultural and health authorities. In the U.S., for example, the Climate Analysis Center (NOAA) defines four regions for weather surveillance: Coordinating ecological (EPA), agricultural (USDA) and health data (CDC) through these centers could provide the basis for integrated assessment and monitoring.

Internationally, regional application centers can be established for advising the agricultural and health sectors. Specifically, advances in climate forecasting can be useful in the development of Famine and Health Early Warning Systems. These can provide advanced warning of conducive bioclimatic conditions for disease outbreaks, allowing time for the implementation of environmentally-sound interventions (e.g., community education, water boiling, vaccination campaigns). These Application Centers (conceived by the NOAA) can form a network under the rubric of the World Climate Program and its major components: the Global Climate, Terrestrial and Ocean Observing Systems (GCOS, GTOS and GOOS), and be integrated into the planned 13 regional START centers under the direction of the IGBP and the International Council of Scientific Unions.

This fusion of systems and scientific work, drawing on remote sensing, field and laboratory observations that include biotic feedbacks and key indicator species abundance, composition and distribution and outcomes, can comprise an efficient methodology for achieving a dynamic, integrated ecological assessment of anthropogenic activities impacting our ecosystems, our climate and our health.
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