Richard S. Ostfeld

Impacts of biodiversity on the emergence and transmission of infectious diseases

Current unprecedented declines in biodiversity reduce the ability of ecological communities to provide many fundamental ecosystem services. Here we evaluate evidence that reduced biodiversity affects the transmission of infectious diseases of humans, other animals and plants. In principle, loss of biodiversity could either increase or decrease disease transmission. However, mounting evidence indicates that biodiversity loss frequently increases disease transmission. In contrast, areas of naturally high biodiversity may serve as a source pool for new pathogens. Overall, despite many remaining questions, current evidence indicates that preserving intact ecosystems and their endemic biodiversity should generally reduce the prevalence of infectious diseases.

Limiting Resources and Territoriality in Microtine Rodents

Theories concerning microtine population dynamics have relied increasingly on assumptions about social structure, but there has been no underlying theory for social biology itself. Among microtine species, patterns of sex-specific territoriality, the best-studied aspect of their social organization, are diverse, setting the scene for the fragmented nature of the contemporary approaches to this issue. Here I propose a set of hypotheses to predict under what conditions females and males should defend territories. The argument has three main components. 1. Microtines have a low-quality diet and should tend to be food-limited. Females invest a large portion of their energy in reproductive physiology, and their reproductive success should be limited by their ability to acquire food and convert it into weaned offspring. Males invest much less energy in reproductive effort and do not participate in parental care; thus, their reproductive success should be limited by access to females. Therefore, territoriality in females should be food-based, and in males it should be female-based. 2. There are three main dietary categories for microtines: fruit-seed-fungus, forbs, and grasses. Although more work is needed to describe the spatial and temporal patterns of availability for these foods, a first approximation is possible. In general, fruits and seeds (in forest habitat) and forbs (in meadows) should be patchily distributed, relatively sparse, and poorly renewable. Since patchy distribution of a resource increases its defensibility, and since sparseness and poor renewability increase the costs of allowing exploitation by intruders, females relying on these two diets should be territorial. On the other hand, grass (in meadows) is evenly distributed (relative to forbs), abundant, and highly renewable. Thus, females of those species that rely largely on grasses should be nonterritorial. 3. When females are territorial they tend to be hyperdispersed, and when females are nonterritorial they should be clumped in distribution. Since evenly spaced females are difficult to defend, male territoriality should not occur in species showing female territoriality. Conversely, when females are nonterritorial, males should be territorial. I assess this argument by using published information. The relation between diet and female territoriality holds up well, with the caution that diet and behavior are seldom analyzed in the same population at the same time. Both factors are variable and their concurrent study necessary. The relation between female territoriality and male territoriality also holds up well, with the exception of Microtus ochrogaster, in which male-female pairs are territorial. Finally, several correlative and experimental approaches are suggested as tests of my predictions. A better understanding of the factors affecting microtine territoriality, and spacing behavior in general, should allow us to evaluate the suppositions of the many theories of how these populations are regulated.

Climate Change and Infectious Diseases: From Evidence to a Predictive Framework

Scientists have long predicted large-scale responses of infectious diseases to climate change, giving rise to a polarizing debate, especially concerning human pathogens for which socioeconomic drivers and control measures can limit the detection of climate-mediated changes. Climate change has already increased the occurrence of diseases in some natural and agricultural systems, but in many cases, outcomes depend on the form of climate change and details of the host-pathogen system. In this review, we highlight research progress and gaps that have emerged during the past decade and develop a predictive framework that integrates knowledge from ecophysiology and community ecology with modeling approaches. Future work must continue to anticipate and monitor pathogen biodiversity and disease trends in natural ecosystems and identify opportunities to mitigate the impacts of climate-driven disease emergence.

Of Mice and Mast Ecological connections in eastern deciduous forests

popular characterization of ecological systems is that everything is connected to everything else. Although in some metaphysical sense it may be true that influences experienced by a particular species are transmitted to all other species in the ecosystem, such pervasive connections have not been demonstrated scientifically. Instead, the focus of community ecology has been on pairwise interactions between species. The paradigm has been that the determinants of community structure can be elucidated by studies of direct effects of populations on one or a few other populations (Kareiva 1994). To identify the role of predation or competition in structuring ecological communities, typically a predator or competitor is removed, and the responses of prey or other competitors are monitored (Connell 1983, Menge and Sutherland 1976, Schoener 1983, Sih et al. 1985). These studies reveal the importance of direct effects in ecological communities. However, such experiments often produce unexpected results, In oak forests, both

BIODIVERSITY AND THE DILUTION EFFECT IN DISEASE ECOLOGY

Many infectious diseases of humans are caused by pathogens that reside in nonhuman animal reservoirs and are transmitted to humans via the bite of an arthropod vector. Most vectors feed from a variety of host species that differ dramatically in their reservoir competence; that is, their probability of transmitting the infection from host to vector. We explore a conceptual model of what we termed the “dilution effect,” whereby the presence of vertebrate hosts with a low capacity to infect feeding vectors (incompetent reservoirs) dilute the effect of highly competent reservoirs, thus reducing disease risk. Using Lyme disease as an example, we demonstrate the presence and estimate the magnitude of the dilution effect for local sites in eastern New York State. We found that the prevalence of Lyme disease spirochetes, Borrelia burgdorferi, in field-collected Ixodes ticks (37.6% and 70.5% for nymphal and adult stages, respectively) was dramatically lower than expected (∼90% and >95% for nymphal and adult stages, respectively) if ticks fed predominantly on highly competent reservoirs, white-footed mice (Peromyscus leucopus) and eastern chipmunks (Tamias striatus). We inferred the role of additional host species using an empirically based model that incorporated data on tick burdens per host, relative population densities of hosts, and reservoir competence of each host. Assuming an empirically realistic reservoir competence of 5% for non-mouse and non-chipmunk hosts, we determined that alternative hosts must provide 61% and 72% of larval and nymphal meals, respectively. Using computer simulations, we assembled simulated host communities that differed in species richness, evenness, and net interactions between alternative hosts and mice. We found that increasing species richness (but not evenness) reduced disease risk. Effects were most pronounced when the most competent disease reservoirs were community dominants and when alternative hosts had a net negative influence on the dominance of mice as a host for ticks. Our results highlight a critical role of biodiversity and host community ecology in the transmission of vector-borne zoonotic diseases that in turn has important consequences for human health.

EFFECTS OF RODENTS ON SURVIVAL OF TREE SEEDS AND SEEDLINGS INVADING OLD FIELDS

Tree invasion of old fields is an important process affecting landscape het- erogeneity and species diversity, as well as the quality of wildlife habitat, in eastern North America. We examined the effects of tree seed and seedling predation by small mammals on the rate, spatial pattern, and species composition of tree invasion in old fields. We performed field experiments inside U-shaped enclosures built at forest-field edges, within which we manipulated the density of meadow voles (Microtus pennsylvanicus), which are major seedling predators. Although we did not directly manipulate density of white-footed mice (Peromyscus leucopus), which are major seed predators, mouse density was high wherever vole density was low. We introduced cohorts of seeds and seedlings of red maple (Acer rubrum) or sugar maple (Acer saccharum) (as specified in the Methods for each trial), white ash (Fraxinus americana), white pine (Pinus strobus), and tree-of-heaven (Ailanthus altissima), all common early invaders of old fields in our study area. Rates of seedling predation were higher in enclosures with higher density of voles, and voles showed distinct preferences for red maple, white ash, and Ailanthus over white pine. Predation rates on small seedlings were higher than on larger seedlings. Seedlings near the forest edge were killed at a lower rate than those >5 m into the field. Predation rates on seeds were higher in low-vole-density treatments, where mice were more abundant. Mice showed distinct preferences for white pine, avoided Ailanthus, and consumed sugar maple and white ash at intermediate rates. Predation rates on seeds were higher in shrub-dominated than in herbaceous old fields. Overall density of mice increased dramatically between 1994 and 1995, and seed predation rates increased concomitantly. In 1994, seed predation was most intense 5 m and 10 m into the field, and less intense at the forest-field edge and 20 m into the field; although a similar pattern was observed in 1995, the variation was not statistically significant. We conclude that both of these common small mammal species can have pro- found effects on survival of tree propagules near forest-field edges, but that their effects are strongly dependent on density. Voles had a strong, negative direct effect on seedling survival, but a positive indirect effect on seed survival by inhibiting seed predation by mice. Voles and mice: (1) showed distinctly different food preferences; (2) had their strong- est effects at different positions with respect to the forest-field edge; and (3) had their strongest effects in different old-field types (herbaceous fields for voles, shrub-dominated fields for mice). These two species are not functionally redundant in their effects on old- field succession.

Climate, Deer, Rodents, and Acorns as Determinants of Variation in Lyme-Disease Risk

Risk of human exposure to vector-borne zoonotic pathogens is a function of the abundance and infection prevalence of vectors. We assessed the determinants of Lyme-disease risk (density and Borrelia burgdorferi-infection prevalence of nymphal Ixodes scapularis ticks) over 13 y on several field plots within eastern deciduous forests in the epicenter of US Lyme disease (Dutchess County, New York). We used a model comparison approach to simultaneously test the importance of ambient growing-season temperature, precipitation, two indices of deer (Odocoileus virginianus) abundance, and densities of white-footed mice (Peromyscus leucopus), eastern chipmunks (Tamias striatus), and acorns ( Quercus spp.), in both simple and multiple regression models, in predicting entomological risk. Indices of deer abundance had no predictive power, and precipitation in the current year and temperature in the prior year had only weak effects on entomological risk. The strongest predictors of a current years risk were the prior years abundance of mice and chipmunks and abundance of acorns 2 y previously. In no case did inclusion of deer or climate variables improve the predictive power of models based on rodents, acorns, or both. We conclude that interannual variation in entomological risk of exposure to Lyme disease is correlated positively with prior abundance of key hosts for the immature stages of the tick vector and with critical food resources for those hosts.

A call to ecologists: measuring, analyzing, and managing ecosystem services

Humans depend on ecosystem services, yet our ecological understanding of them is quite limited. In the classic example, when New York City decided to protect the Catskill Watershed rather than build an expensive water filtration plant, planners reasoned that the protection plan would be the cheaper option, even if they underestimated the area required by half. Such reasoning reflects our inability to predict how to manage lands to provide ecosystem services of sufficient quantity and quality. Human domination of the biosphere is rapidly altering the capacity of ecosystems to provide a variety of essential services; we therefore need to develop a better understanding of their ecological underpinnings, and to integrate this knowledge into a socioeconomic context to develop better policies and plans to manage them. We present a three-part research agenda to create the knowledge base necessary to accomplish this goal.

Are predators good for your health? Evaluating evidence for top‐down regulation of zoonotic disease reservoirs

Zoonotic diseases, caused by pathogens transmitted to people from vertebrate reservoirs, take an enormous toll on human health worldwide. Many of these disease agents are harbored in rodent populations, and humans are victims of “accidental” transmission. Here we explore the idea that predatory vertebrates indirectly protect human health by reducing population size of rodent reservoirs of human disease. Research frontiers include the importance of rodent population density to the incidence of human disease, as opposed to behavior or age structure effects; the roles of different types of 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. A better understanding of these basic ecological issues will inform both environmental and health policy.

Territoriality and Mating System of California Voles

(1) In this study I used radiotelemetry to examine patterns of space use by free-ranging California voles (Microtus californicus) both before and after the provision of supplemental food (fresh carrots). In each of the studys 2 years, carrots were provided over an area (100 m2) about the size of a California vole home range. The first run was conducted at peak population density, and the second at low density. (2) Home range core areas were 30-50% larger for males than for females, but peripheral areas were nearly 100% larger for males. Home ranges of those females having access to supplemental food shrank after provisioning, whereas those of males did not. Home ranges of males were nearly 100% larger at low than at high density, whereas those of females were 30-50% larger at low than at high density (the latter difference being non-significant). (3) Home ranges of females often overlapped extensively with those of other females, and nest-sharing was not uncommon. Some females shifted their home ranges after food addition to encompass more of the provisioned area. The addition of food induced overlap between females that had not previously overlapped. (4) Males showed very little overlap with other males, and this was not affected by food addition. Males rapidly occupied home ranges abandoned by adjacent males. (5) Males and females overlapped with each other extensively, but access to females was unequal. I conclude that male M. californicus are strongly territorial, but that females are non-territorial or selectively territorial. Mating is probably polygynous, and the most likely mode is female defence.