6. ECOLOGICAL DISRUPTIONS
Next, some examples of emerging infectious diseases are considered in relation to six main ecological disruption situations. Each configuration of changes includes an aspect of land use (Patz & Confalonieri 2004). There is some overlap between these six categories, listed below, since they refer to changes in complex dynamic ecosystems:
- (i) altered habitat, with proliferation of reservoir or vector populations;
- (ii) biodiversity change and habitat fragmentation;
(iii) ecosystem changes and loss of predators;
- (iv) intensified farming and animal husbandry;
- (v) niche invasion;
- (vi) host transfer.
- (a) Altered habitat, with proliferation of reservoir or vector populations
Rodent-borne hantavirus occurs widely in agricultural systems, as in South America and east Asia, and in arid grasslands in North America and elsewhere. In mid-1993, an unexpected outbreak in humans occurred in the Four Corners region of southwest USA. The infection entailed acute respiratory distress, with high fatality. This ‘hantavirus pulmonary syndrome’ was traced to infection with a previously unrecognized virus, maintained primarily within the common native deermouse. Human infection occurs via contact in dried, wind-blown excretions of infected mice.
Apparently, the El Nin˜o event of 1991–1992, with its unseasonally heavy summer rains, hugely boosted the local rodent populations, and potentiated the 1993 outbreak (Glass et al. 1995; Engelthaler et al. 1999). Populations of deermice were 10–15-fold higher than during the previous 20-year seasonal average (Parmenter et al. 1993).
(b) Biodiversity change and habitat fragmentation
Deforestation, with fragmentation of habitat, increases the ‘edge effect’, which then promotes pathogen–vector– host interaction. This process has contributed, in recent decades, to the emergence of the various viral haemorrhagic fevers in South America. These viral infections are caused by arenaviruses that have wild rodents as their natural hosts. They have been described especially in Argentina ( Junin virus), Bolivia (Machupo virus) and Venezuela (Guanarito virus) (Maiztegui 1975; Simpson 1978; Salas et al. 1991).
These haemorrhagic fever infections typically occur in outbreaks ranging from a few dozen to thousands of cases. Outbreaks have mostly occurred in rural populations, when individuals become infected by contact with contaminated rodent excretions. Consider the example of the Machupo virus. The clearing of forested land in Bolivia in the early 1960s, which was accompanied by blanket spraying of DDT to control malaria mosquitoes, led, respectively, to infestation of cropland by Calomys mice and to the poisoning of the rodents’ usual predators (village cats). The consequent proliferation of mice and their viruses resulted in the appearance of a new viral fever, the Bolivian (Machupo) haemorrhagic fever, which killed around one-seventh of the local population.
The impact of forest clearance, with road building, ditch construction, and subsequent damming and irrigation, is known to have diverse impacts on anopheline mosquito species. Cleared land and the creation of ditches may enhance breeding opportunities for the preexisting local malaria-transmitting anopheline mosquitoes. By contrast, habitat destruction may eliminate some local mosquito species, perhaps thereby opening a niche for an invasive anopheline species (Povoa et al. 2001).
(c) Ecosystem changes, loss of predators and host species imbalance
Lyme disease illustrates this category of factor. This bacterial disease was first identified in the northeast USA in 1976 in the town of Old Lyme. The disease is spread by ixodic ticks that transmit the spirochaete Borrelia burgdorferi. The ticks normally feed on deer and white-footed mice, with the latter being the more competent viral host species.
Forest fragmentation has led to changes in biodiversity. This includes the loss of various predator species—wolves, foxes, raptors and others—and a resultant shift of ticks from the less to the more competent host species (as white-footed mice have become relatively more numerous, because of the reduced ‘dilution’ effect of biodiversity). These changes, along with middle-class suburban sprawl into woodlands, have all been interconnected in the occurrence of this disease (Glass et al. 1995; Schmidt & Ostfeld 2001).
(d ) Intensified farming and animal husbandry
This category is well illustrated by the apparent interactions between avian viruses and humans in rural south China and environs. This interaction has been widely posited to underlie the emergence of new strains of influenza virus (perhaps with intervening passage through domesticated pigs). The influenza viruses are very unstable genetically, and are thus well adapted to evading host defences. Influenza viruses, when replicating in infected humans or animals, can undergo genetic rearrangement. For example, different subtypes of influenza A virus can swap genes, thereby producing a novel subtype with an altered antigenic profile, and this new subtype may on occasion be particularly virulent. This scrambling of genetic material, albeit usually minor, serves to ensure that animals and humans remain susceptible to the virus during each subsequent season. This enhances continuing survival prospects for the viruses.
(e) Niche invasion
The emergence of some infectious diseases results from a pathogen invading a new or recently vacated niche. A good example is the Nipah virus, which emerged as a human disease in Malaysia in 1999, causing over 100 deaths (Chua et al. 2000).
This highly pathogenic virus emerged from its natural reservoir host species (fruit bats) via domestic animal (pig) amplifier hosts. The ecological trigger appears to have been a complex series of human alterations to fruit bat habitat and agriculture in combination with a period of drought (Daszak et al. 2001; Chua et al. 2002). Three considerations are particularly relevant.
- (i) The virus does not appear to pass directly from bats to humans.
- (ii) The fruit bat’s habitat has been largely replaced in peninsular Malaysia by oil palm plantations.
(iii) Deforestation in adjacent Sumatra, coupled with a major El Nin˜o-driven drought, led to significant seasonal air-pollution haze events that cover Malaysia. This reduced the flowering and fruiting of forest trees that are the natural food of fruit bats, thus impairing their food supply.
Thus, the Nipah virus outbreak in 1999 was associated with a marked decline in forest fruit production. This caused the encroachment of fruit bats (the key Nipah virus reservoir) into pig farms, where fruit plantations were also maintained. Infected pigs then passed on the viral infection to pig farmers (Chua et al. 2002).
(f ) Host transfer
This, of course, is the old story of pathogens ‘jumping ship’. The HIV/AIDS pandemic has reminded us of this ongoing risk, since it is clear that SIV mutants passed into humans some time during the twentieth century. Bush-meat hunting in Africa has led to other local emergence episodes (Patz & Wolfe 2002): for example, forest workers cutting up chimpanzee meat have become infected with Ebola virus (WHO 1996).
Cross-species transmission is, of course, bidirectional: it can also entail non-human primate species and other valuable wildlife coming into contact with human pathogens. For example, the parasitic disease, Giardia, was introduced to the Ugandan mountain gorilla by humans through ecotourism and conservation activities (Nizeyi et al. 1999). Non-human primates have acquired measles from ecotourists (Wallis & Lee 1999).
(g) Human-induced climate change
Many pathogens and their vectors are very sensitive to climatic conditions, particularly temperature, surface water and humidity. It has become increasingly certain not only that humans face anthropogenic climate change, because of the continuing excessive emission of greenhouse gases, but that the process has begun (see figure 2). In the words of a recent authoritative review: ‘Modern climate change is dominated by human influences, which change in temperature (˚C)
The frequency and geographical range of certain plant and animal infectious diseases has reportedly changed, at least partly in response to climate change, over recent years (Harvell et al. 2002). For human infectious diseases, the causal configuration is intrinsically more complex (entailing many more demographic, social and technological influences), and therefore it has proven difficult to attribute clear-cut impacts due to recent climate change. Nevertheless, some suggestive evidence exists for an influence of recent climate change upon cholera in Bangladesh, tick-borne encephalitis in Sweden, and malaria in parts of eastern Africa (Lindgren & Gustafson 2001; Patz et al. 2002; Rodo et al. 2002).
There has been considerable attention paid to how human diseases such as malaria and dengue fever will respond to the plausible range of global climate changes over the coming century. Various statistical and biologically based (‘process’) models have been brought to bear. However, much of the topic has not yet been broached. How will patterns of domestic and urban water use change in a warmer world? How will a change in climatic conditions, and associated changes in ecosystems, affect the probabilities of microbial mutation and successful speciation? What would be the infectious disease consequences of an increase in the tempo of extreme weather events and natural disasters?
With global climate change, we are beginning to change the conditions of life on Earth at the planetary scale. This is unprecedented. It will have diverse, mostly negative, consequences for biological systems everywhere and for dependent human societies.
(h) Dengue fever: a labile disease affected by urbanization, travel, trade and climate
Dengue is the most important vector-borne viral disease of humans. This disease has attained additional prominence recently, as one that is very likely to be affected by global climate change. Dengue is numerically the most important vector-borne viral disease of humans. Approximately 80 million cases are reported every year, of which ca. 20 000 die. Although dengue is primarily a tropical disease, it has extended in recent decades to countries with temperate climates. This reflects the increase in the number of imported cases, resulting from increased air travel, and the introduction of an exotic vector, Aedes aegypti, adapted to a cold climate (Kuno 1995).
This vector species, which breeds in water-containing sites typically found in the urban environment, has made extraordinary evolutionary adjustments to coexist with humans, having originated in forest Africa. The vector has followed humankind on its travels and migrations around the world (Monath 1994). It has attained further recent prominence as one of the main infectious diseases likely to be affected by global climate change throughout this century and beyond.