2. Niche invasion and cross-species transfer of pathogens
3. Why can high biodiversity prevent disease emergence?
4. Harming habitats can harm human health: Tropical rainforest destruction and the rise of malaria
5. Agricultural development, crop irrigation, and breeding sites
Changes in biodiversity and habitat change affect the transmission or emergence of a range of infectious diseases. These environmental factors include agricultural encroachment, deforestation, road construction, dam building, irrigation, wetland modification, mining, the concentration or expansion of urban environments, coastal zone degradation, and other activities. As a result, a cascade of factors can exacerbate infectious disease resurgence, such as forest fragmentation, disease introduction, pollution, poverty, and human migration. Subsequent biological mechanisms of disease emergence that are affected include altered vector breeding sites or reservoir host distribution, niche invasions or interspecies host transfers, changes in biodiversity (including loss of predator species and changes in host population density), human-induced genetic changes of disease vectors or pathogens (such as mosquito resistance to pesticides orthe emergence of antibiotic-resistant bacteria), and environmental contamination of infectious disease agents.
emerging disease. As defined by the Centers for Disease Control and Prevention, emerging infectious diseases are diseases of infectious origin whose incidence in humans has increased within the past two decades or threatens to increase in the near future. In general, an emerging disease can be a completely new disease or an old disease occurring in new places or new populations or that is newly resistant to available treatments.
gonotrophic cycle. The complete cycle of time between a mosquito’s blood feeding and subsequent laying of eggs.
reservoir host. A reservoir host can harbor human pathogenic organisms without acquiring the disease, and so serves as a source from which the infectious disease may spread.
vector-borne disease. Infectious diseases spread indirectly via an insect or rodent. Often, part of the pathogen’s life cycle occurs within the insect vector. Examples include malaria, dengue fever, West Nile virus, Lyme disease, plague, and Hantavirus.
zoonotic disease. Any disease that is spread from animals to people. These are also called “zoonoses” (as opposed to “anthroponoses,” which are diseases transmitted directly from person to person). Examples of zoonotic diseases include rabies, Lyme disease, and bat-borne Nipah and Hendra viruses.
Widespread deforestation and habitat destruction not only threaten biodiversity worldwide, but land use change influences a range of infectious diseases. Anthropogenic (human-created) drivers that especially affect infectious disease risk include destruction or encroachment into wildlife habitat, particularly through logging and road building; changes in the distribution and availability of surface waters, such as through dam construction, irrigation, or stream diversion; agricultural land use changes, including proliferation of both livestock and crops; deposition of chemical pollutants, including nutrients, fertilizers, and pesticides; uncontrolled urbanization or urban sprawl; climate variability and change; migration and international travel and trade; and either accidental or intentional human introduction of pathogens (table 1 and figure 1).
Table 1. Mechanisms and processes of land use change that affect health
| Agricultural development |
| Urbanization |
| Deforestation |
| Population movement |
| Increasing population |
| Introduction of novel species/pathogens |
| Water and air pollution |
| Biodiversity loss |
| Habit fragmentation |
| Road building |
| Macro- and microclimate changes |
| Hydrological alteration |
| Decline in public health infrastructure |
| Animal-intensive systems |
| Eutrophication |
| Military conflict |
| Monocropping |
| Erosion |
Source: Patz et al., 2004.
Note: Ranked from highest to lowest public health impact by meeting participants. Criteria for ranking were based on estimated impacts on both the number of infectious diseases and the prevalence of those diseases.
Ecological changes can affect specific biological mechanisms of disease transmission. Several biological mechanisms have been identified and are reported in the Millennium Ecosystem Assessment. These include niche invasions or interspecies host transfers; changes in biodiversity (including loss of predator species and changes in host population density); altered vector breeding sites or reservoir host distribution; humaninduced genetic changes of disease vectors or pathogens (such as mosquito resistance to pesticides or the emergence of antibiotic-resistant bacteria); and environmental contamination of infectious disease agents.
Figure 1. Examples of habitat change and vector-borne disease. Rising water table, irrigation, mining, and deforestation can increase the risk of mosquito-borne diseases. (From Patz et al., 2005)
Many widespread diseases of today originally stemmed from domestication of livestock. For example, measles, smallpox, and tuberculosis resulted from the domestication of wild cattle. Pathogens that are currently passed from person to person (anthroponotic), including some influenza viruses and human immunodeficiency virus (HIV), were formerly zoonotic but have diverged genetically from their ancestors that occurred in animal hosts.
Rapid population growth and population movements have quickened the pace and extensiveness of ecological change over the past two centuries. New diseases have emerged even as some pathogens that have been around for a long time have been eradicated or rendered insignificant, such as smallpox. Ecological change, pollutants, the widespread loss of top predators, persistent economic and social crises, and international travel, which drive a great movement of potential hosts, have progressively altered disease ecology, affecting pathogens across a wide taxonomic range of animals and plants.
According to estimates, nearly 75% of human diseases are zoonotic and stem from wildlife or domestic animals. The emergence of many diseases has been linked to the interface between tropical forest communities, with their high levels of biodiversity, and agricultural communities, with their relatively homogeneous genetic makeup but high population densities of humans, domestic animals, and crops. For instance, expanding ecotourism and forest encroachment have increased opportunities for interactions between wild nonhuman primates and humans in tropical forest habitats, leading to pathogen exchange through various routes of transmission.
When severe acute respiratory syndrome (SARS) virus erupted and almost became pandemic, the cause was linked to an animal human interaction occurring in customary wet markets in China—a known source of influenza viruses since the 1970s. (Live-animal markets, termed “wet markets,” are common in most Asian societies and specialize in many varieties of live small mammals, poultry, fish, and reptiles.) The majority of the earliest reported cases of SARS were of people who worked with the sale and handling of wild animals. The species originally at the center of the SARS epidemic was the palm civet cat, but further research implicated the Chinese horseshoe bat as the definitive reservoir host.
Bush-meat hunting in the deep jungle has afforded easier exchange of pathogens between humans and nonhuman primates. In Central Africa, 1 3.4 milliontons of bush meat is harvested annually. In West Africa, a large share of protein in the diet comes from bush meat. The bush-meat harvest in West Africa includes a large numbers of primates, so the opportunity for interspecies disease transfer between humans and nonhuman primates is significant, providing ample opportunity for cross-species transmission and the emergence of novel microbes into the human population.
The “Taxonomic Transmission Rule” states that the probability of successful cross-species infection increases the closer hosts are genetically related (chimpanzees are closer genetically to humans, for example, than birds or fish are) because related hosts are more likely to share susceptibility to the same range of potential pathogens. Bush-meat consumption has been implicated in the early emergence of HIV (and workers collecting and preparing chimpanzee meat have become infected with Ebola).
Unfortunately for wildlife, transmission across species can also go from humans to wildlife. For example, the parasitic disease Giardia was introduced to the Ugandan mountain gorilla by humans through ecotourism activities. Gorillas in Uganda also have been found with human strains of Cryptosporidium parasites, presumably from ecotourists. Human tuberculosis has also jumped species, infecting the banded mongoose. Such transfer and emergence events not only affect ecosystem function but could possibly result in a more virulent form of a human pathogen circling back into the human population from a wildlife host.
Habitat fragmentation generally reduces species biodiversity. Infectious diseases, especially those involving intermediate reservoir host species in their life cycle, can thereby be affected. Organisms at higher trophic levels usually exist at a lower population density (per classic food webs) and are often quite sensitive to changes in food availability. Smaller forest patches left after fragmentation, for example, may not have sufficient prey for top predators, resulting in local extinction of predator species and a subsequent increase in the density of their prey species.
Lyme disease in particular is influenced by the level of species diversity in the biome. In eastern U.S. oak forests, studies on the interactions among acorns, white-footed mice (Peromyscus leucopus), moths, deer, and ticks have linked defoliation by gypsy moths with the risk of Lyme disease. Most tick vectors feed on a variety of host species that differ dramatically in their function as a reservoir for the bacterium that causes Lyme disease—that is, the probability of a tick picking up the bacterium from different reservoir hosts varies substantially. Increasing species richness has been found to reduce disease risk, and the involvement of a diverse collection of vertebrates in this case may dilute the impact of the main reservoir, the white-footed mouse.
Also, small woodlots tend not to have the range required of predator mammalian species, and probable competitors occur at lower densities in these areas than in more continuous habitats. Therefore, habitat fragmentation causes a reduction in biodiversity within the host communities, increasing disease risk though the increase in both the absolute and relative density of a primary reservoir, the white-footed mouse. Other diseases are known to have resurged following land use change, including cutaneous leishmaniasis, Chagas disease, human granulocytic ehrlichiosis, babesiosis, plague, louping ill, tularemia, relapsing fever, Crimean Congo hemorrhagic fever, and LaCrosse virus.
The global rate of tropical deforestation continues at staggering levels with nearly 2–3% of global forests lost each year. Recent evidence from Africa, the Amazon, and parts of Asia now identify deforestation as one of the causes for the increase in malaria across the tropics and for habitat fragmentation (e.g., “fishbone” pattern in the Amazon from road building, creating breeding sites and “edge effects”).
The World Health Organization (WHO) estimates that malaria is responsible for 13% of global disability and mortality from infectious and parasitic diseases. It is the world’s most widespread fatal or debilitating vector-borne disease, killing nearly 2 million (mostly children) annually. Southeast Asia, Africa, and the Amazon have experienced increased malaria risk accompanying both human population growth and environmental change.
Habitat disturbance has been changing mosquito distributions for centuries. For example, the draining of swamps surrounding Rome reduced mosquito populations and malaria in the city. When agricultural practices spread across Europe, the resultant social and land transformations contributed to the eradication of malaria. However, adverse effects resulted from the removal of forests from within the ancient Indus valley and are proposed to have shifted the habitat preferences of the dangerous A. stephansi mosquito from the forest to urban areas and waterways and thereby to have contributed to the civilization’s collapse circa 2000 BC. To this day, A. stephansi remains the most prolific vector for urban malaria transmission across the Middle East.
Figure 2. Biting rates of An. darlingi mosquitoes (y-axis) versus percentage forest contained in a 2 km x 2 km grid (x-axis). The black line is the high-probability curve and shows that mosquito biting rates lor abundance because each mosquito is captured when it comes to bite) decline rapidly as the amount of mature forest increases within the grid area. These curves account for potential confounding by human population density. (From Vittor et al., 2006)
Soon after the discovery that malaria was transmitted by mosquitoes, attention shifted away from the influence of Land Use and Cover Change (LUCC) on malaria risk. Priority of malaria programs became vector eradication, via insecticides and clinical health interventions. If LUCC was recognized as a risk factor, it was used to focus the application of DDT to mosquito breeding sites.
Malaria entomology studies have examined sites for adult or larval abundance in different habitats and or gradients of one LUCC type. For example, a project in western Venezuela found greater mosquito species richness in tall forests in comparison to short forests and open areas. Larval species richness in open areas was higher for swamps and flooded pastures than ground pools, lagoons, or rivers. In Africa, breeding pools for Anopheles larvae had significantly less canopy cover than breeding pools for other mosquito species, and the larval habitat size was significantly different across several different LUCC categories. These and other observations continue to show that LUCC can alter the distribution of a disease-causing vector.
Throughout Amazonia, Anopheles darlingi is the most efficient and principal interior vector of falciparum malaria. In a recent field study from the Peruvian Amazon, sites surrounded by deforestation had An. darlingi biting rates nearly 300 times larger than forested sites, even after controlling for human population density. Sites with greater than 80% deforestation had a mean biting rate of 8.33, whereas sites with less than 30% deforestation had a mean biting rate of 0.03 (figure 2). These findings suggest that environmental risk factors for malaria are related to the LUCC changes associated with human expansion into forested areas. Additionally, larvae of An. darlingi were more often found in breeding sites with more sunlight (less forest canopy), with emergence grasses, and with algae. figure 3 illustrates likely steps between deforestation and malaria risk. Current indicators of LUCC related to malaria risk from localized studies remain to be tested across a broader region, and investigations of ecology have not been performed.
Figure 3. Schematic summary of likely steps explaining how deforestation may increase malaria risk in the Amazon region. Note that habitat change can affect mosquito biodiversity lby altering niches and, subsequently, relative mosquito species abundance.
Changing landscapes can significantly affect local weather more acutely than long-term climate change. Land cover change can influence microclimatic conditions including temperature, evapotranspiration, and surface runoff, all key to determining mosquito abundance and survivorship. In Kenya, open treeless habitats average warmer midday temperatures than forested habitats and also affect indoor hut temperatures. As a result, the gonotrophic cycle of female An. gambiae was found to be shortened by 2.6 days (52%) and 2.9 days (21%) during the dry and rainy seasons, respectively, compared to forested sites. Similar findings have been documented in Uganda, where higher temperatures have been measured in communities bordering cultivated fields compared to those adjacent to natural wetlands, and the number of An. gambiae s.l. per house increased along with minimum temperatures after adjustment for potential confounding variables. Also, survivorship of An. gambiae larvae in sunlit open areas is much greater than that in forested areas. In short, deforestation and cultivation of natural swamps in the African highlands create conditions favorable for the survival of An. gambiae larvae, making analysis of land use change on local climate, habitat, and biodiversity key to malaria risk assessments.
Land converted for agriculture represents the Earth’s largest land surface change since human existence began. Migrant farmers appear to be the primary direct agents of tropical deforestation around the world, although the initial causes are often roads built by logging, mining, or petroleum interests. Agricultural development in many parts of the world has resulted in an increased requirement for crop irrigation, which reduces water availability for other uses and increases breeding sites for disease vectors. An increase in soil moisture associated with irrigation development in the southern Nile Delta following the construction of the Aswan High Dam has caused a rapid rise in the mosquito Culex pipiens and a consequent increase in the arthropod-borne disease Bancroftian filariasis (or elephantiasis). Onchocerciasis (river blindness) and trypanosomiasis (sleeping sickness) are further examples of vector-borne parasitic diseases that may be triggered by changing land-use and water management patterns.
One example of a very specific agricultural development that created a new ecological niche that caused a malaria epidemic occurred during the 1930s in Trinidad with the production of cacao. Cacao trees establish a lighter and drier environment than the surrounding natural forests. Thus, large shade trees (called immortelles) were planted to provide shade to the cacao trees. But immortelles support epiphytes, mostly bromeliads. In Trinidad, these immortelles supported a bromeliad tank species that naturally collects a small amount of water that is an ideal breeding site for A. bellator. A. bellator is a malaria vector that also prefers drier areas and the subcanopy elevation of the forests. Public health officials noted that splenomegaly among schoolchildren correlated with the areas cultivating cacao and that the vector A. bellator was not found outside of the cacao farm area. Removal of the bromeliads, by hand or with herbicides, reduced A. bellator populations and returned malaria rates to prior endemic levels.
Another example of agricultural land use practices and disease emergence arises from Malaysia, where Nipah virus first occurred in pig farmers in the late 1990s. Throughout the peninsula, pig farms were expanding and were often colocated with fruit orchards. The leading theory is that contaminated bat saliva on fruit dropped into pig pens and infected the pigs when they ingested the fruit. Porcine Nipah virus causes severe coughing in pigs, and it is believed that farmers contracted the disease by inhaling the aerosolized form of the virus.
The notion of sustainable health—mirroring the concept of sustainable development—means to provide health for today’s generation without compromising that same opportunity for future generations. This chapter has illustrated how managing our natural resources is tightly linked to sustaining human population health. Along the path toward global economic development, health risks must be considered at various levels. These levels include (1) specific health risk factors, (2) landscape or habitat change, and (3) institutional (economic and behavioral) levels. It is essential that societies shift away from dealing primarily with specific risk factors and look “upstream” at land-use and biodiversity changes for causative factors of effects on infectious disease. As such understanding increases, it will become more feasible to plan approaches to prevent new infectious disease emergence.
Inherent trade-offs become evident when land-use change and health are correlated. These involve ethical values, environmental versus health choices, and disparities in knowledge and economic class. Trade-offs are between short-term benefit and long-term damage. For example, draining swamps may reduce vectorborne disease hazards but also destroy the wetland ecosystem and its inherent services (such as water storage, water filtration, biological productivity, and habitats for fish and wildlife). Research can help decisionmaking by identifying and assessing trade-offs in different land-use-change scenarios. Balancing the diverse needs of people, livestock, wildlife, and the ecosystem will always be a prominent feature.
As illustrated, biodiversity loss, habitat destruction, and agricultural practices can lead to infectious disease emergence or resurgence; the public, therefore, needs to be attentive to entire ecosystems rather than simply their local environs. Although we may not live within a certain environment, its health may indirectly affect our own. For example, intact forests support complex ecosystems and provide essential habitats for species that are specialized to that flora and, in turn, may end up as relevant to our health. The challenge then is to identify and promote optimal situations whereby the maximum number of people—including future generations (as well as a number of species)—can benefit from policies geared toward sustaining both health and the environment.
http://www.ecohealth.net. The International Association for Ecology and Health (and its flagship journal Eco-Health). The association and journal now provide a gathering place for research and reviews that integrate the diverse knowledge of ecology, health, and sustainability, whether scientific, medical, local, or traditional.
http://sage.wisc.edu/pages/health.html. Information on global climate and land-use change impacts on ecosystems and human health at the University of Wisconsin.
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