Lead Scientist(s)Dr Richard S Ostfeld
A major effort in the Ostfeld lab is the theoretical development and empirical testing of the Dilution Effect, which describes the mechanisms by which vertebrate diversity protects people against exposure to zoonotic diseases. Intensive study of the ecology of Lyme disease has been instrumental in developing this theory
In forested landscapes of the eastern and central United States, the white-footed mouse is typically one of the most abundant vertebrates. Imagine a recently hatched larval tick waiting on the forest floor, nearly immobile, waiting for a potential vertebrate host to approach. If the tick is born in a habitat that favors white-footed mice, and/or in a year of high mouse density, the tick has a high probability of obtaining its first blood meal from a mouse. Because a high percentage (#) of white-footed mice carry the spirochete bacterium that causes Lyme, it is very likely the tick will be infected. When it molts from a larvae into an infected nymph during the spring or summer, it will be dangerous to humans.
Two situations should reduce a questing larval tick's probability of encountering a white-footed mouse. One is a reduction in the population density of mice, the other an increase in the number of non-mouse hosts in the forest. When host diversity is high, there is a lower probability that ticks will feed on a white-footed mouse host. Larval ticks are less likely to become infected with B. burgdorferi when they feed on other vertebrate animals, such as chipmunks, lizards, or ground-dwelling birds. When tick's obtain their larval blood meal without becoming infected, they are not dangerous to humans when they feed as nymphs the following year.
The second situation, termed the Dilution Effect by Ostfeld and Keesing (2000 a, b), occurs when high host diversity dilutes the impact of white-footed mice, reducing mouse-tick interactions and subsequent disease risk. Empirical and theoretical support for the dilution effect is growing. An assessment of major tick host species at our New York study sites revealed that Lyme disease risk is lower when diverse host communities are present. Conversely, disease risk escalates in species-poor communities (LoGiudice et al. 2003). Computer simulation models (Van Buskirk and Ostfeld 1995, 1998, Schmidt and Ostfeld 2001) suggest mechanisms behind the dilution effect. Human-induced environmental changes, such as landscape fragmentation and predator suppression, can inadvertently increase disease risk by reducing biodiversity.
The dilution effect appears to be a general phenomenon, not restricted to the Lyme disease system. For the dilution effect to apply to a vector-borne zoonosis, the following conditions must hold:
The vector must be a generalist that parasitizes at least several host species, including humans
Hosts parasitized by the vector must vary strongly in their reservoir competence, such that some are highly infective and others are dilution hosts
Vectors must acquire the pathogen via blood meals rather than relying predominantly on transovarial transmission
The most competent reservoir host(s) must be dominant members of the host community, feeding a high proportion of the tick population. A corollary of condition (4) is that host species with lower reservoir competence will tend to occur only in more diverse communities.
The extent to which these conditions are met is the subject of ongoing assessments.
The conversion of forest into suburban developments and agricultural fields has resulted in the fragmentation of forested landscapes in eastern and central North America. The result is a series of landscapes in which a gradient of forest patches exists, from small woodlots (<1 hectare) to expanses of continuous forest. Recent field studies in Indiana and Illinois indicate that population densities of white-footed mice are considerably higher in forest patches than in continuous forest, and that mouse density tends to be inversely correlated with patch size. The ecological mechanisms behind this pattern are not entirely clear, but a possible mechanism is that natural enemies of mice, such as carnivores, raptors, and competing small mammals decline or disappear when forest habitat is highly fragmented.
Studies by Nupp and Swihart (1996, 1998) and Rosenblatt et al. (1999) reveal that rodents that compete with mice for food, such as chipmunks, gray squirrels (Sciurus carolinensis), and fox squirrels (S. niger), decline or disappear in small forest patches. Similarly, mammals that prey on mice, such as long-tailed weasels (Mustela frenata), red foxes (Vulpes vulpes), gray foxes (Urocyon cinereoargenteus), and coyotes (Canis latrans), require large expanses of forest and are absent from small woodlots (Rosenblatt et al. 1999). Other studies suggest that avian predators on mice, such as barred owls (Strix varia), are less abundant in highly fragmented landscapes than in more continuous old-growth forest. [Citations in Allan et al. 2003, Ostfeld and LoGiudice 2003].
Reduced vertebrate diversity in highly fragmented landscapes can affect Lyme disease dynamics through two different pathways. First, the loss of vertebrate diversity results in a high proportion of tick meals being taken from mice. As a result, habitat alteration reduces host diversity and weakens the dilution effect. Second, reductions in predators on and competitors with mice may be responsible for increased absolute mouse density, which should increase disease risk.Although the mechanisms are still under intensive study, recent research in Dutchess County, NY, shows that the abundance and infection prevalence of nymphal ticks is considerably higher in small woodlots than in larger forested areas. In patches less than 5 acres, risk of human exposure to Lyme disease was almost 5 times greater than in larger forested areas (Allan et al. 2003). Computer modeling suggests that the patterns of species loss with habitat fragmentation will determine how rapidly disease risk will increase (Ostfeld and LoGiudice 2003).
Monkeypox, hantavirus pulmonary syndrome (HPS), Lassa fever, Argentine and Bolivian hemorrhagic fevers, Lyme disease, granulocytic ehrlichiosis, leishmaniasis, Bubonic plague, scrub typhus, tick-borne encephalitis, Crimean-Congo hemorrhagic fever - for these diseases and many more, we are the unwitting victims of pathogens that cycle, often cryptically, within rodent populations.
It seems likely that disease transmission will be reduced when rodent populations occur both at chronically low densities and away from human habitation. Conversely, disease risk will increase with increasing rodent density, magnitude of fluctuations, and tendency to invade human dwellings.
In a literature review combined with new theory, we (Ostfeld and Holt 2004) recently found that rodent predators have a strong potential to protect human health. Generalist or highly mobile predators seem likely to be most effective at regulating rodent numbers at low levels, whereas specialist predators of limited mobility appear responsible for dramatically fluctuating rodent populations. Medium-sized mammalian predators and raptors illustrate the type of predators most likely to play a strong role in regulating rodents.
Habitat destruction and degradation generally affect predatory vertebrates more strongly than more herbivorous ones. As a consequence of predator loss, which we term "missing weapons of mouse destruction," we expect many rodent populations, and the pathogens they transmit, to perform well in fragmented landscapes. Although some studies support his expectation, further research is needed. Research frontiers include: correlations between rodent population density and human disease incidence (as opposed to behavior or age structure effects); the roles of different predators in determining both population dynamics and rodent density per se; and the effects of human-caused environmental change on predators and their rodent prey.