Cheryl A. Parmenter

The Ecology and Evolutionary History of an Emergent Disease: Hantavirus Pulmonary Syndrome

I the spring of 1993, a previously undescribed disease emerged in the Southwest, killing 10 people during an 8-week period in May and June. Early during an infection, victims experienced flu-like symptoms for several days, but their condition suddenly and rapidly deteriorated as their lungs filled with fluids; death usually occurred within hours of the onset of this crisis period. There was no cure, no successful medication or treatment, and the disease agent (virus, bacterium, or toxin) was completely unknown. For the first few weeks, the mortality rate was 70%. Researchers from many disciplines immediately focused on the outbreak, attempting to identify the agent and understand the causes and dynamics of the disease. Within weeks, scientists at the Centers for Disease Control and Prevention (CDC) identified the agent as a previously unknown hantavirus (Bunyaviridae), subsequently named Sin Nombre virus, or SNV (Nichol et al. 1993). Because hantaviruses were known to be transmitted by rodents, investigators undertook an intensive small mammal field sampling campaign in the Four Corners region of New Mexico and Arizona. Shortly thereafter, CDC identified the viral reservoir host as a common and widely distributed rodent, the deer mouse, Peromyscus maniculatus (figure 1; Childs et al. 1994). During the identification period, on the medical side, physicians and medical staff made rapid progress in developing treatment methods to stabilize and sustain patients through the crisis period, thereby substantially improving patient survivorship; nonetheless, the mortality rate fell only to about 40%, where it remains today. The emergence of this new disease prompted many questions about its history, causes, and dynamics. Was this a newly Terry L. Yates (e-mail: tyates@unm.edu) is a professor in the Departments of Biology and Pathology at the University of New Mexico, Albuquerque, NM 87131. Cheryl A. Parmenter, Robert R. Parmenter, John R. Vande Castle, Jorge Salazar-Bravo, and Jonathan L. Dunnum are with the Department of Biology and the Museum of Southwestern Biology, University of New Mexico. James N. Mills, Thomas G. Ksiazek, Stuart T. Nichol, and Joni C. Young are with the Centers for Disease Control and Prevention, Atlanta, GA 30333. Charles H. Calisher and Barry J. Beaty are with the Arthropod-borne and Infectious Diseases Laboratory, Foothills Campus, Colorado State University, Fort Collins, CO 80523. Kenneth D. Abbott is with the Department of Biology, Yavapai College, Prescott, AZ 86301. Michael L. Morrison is with the Department of Wildlife and Fisheries Sciences, University of Arizona, Tuscon, AZ 85721. Robert J. Baker is with the Department of Biology and The Museum, Texas Tech University, Lubbock, TX 79409. Clarence J. Peters is with the Department of Pathology, University of Texas Medical Branch, Galveston, TX 77555.

SMALL‐MAMMAL DENSITY ESTIMATION: A FIELD COMPARISON OF GRID‐BASED VS. WEB‐BASED DENSITY ESTIMATORS

Statistical models for estimating absolute densities of field populations of animals have been widely used over the last century in both scientific studies and wildlife management programs. To date, two general classes of density estimation models have been developed: models that use data sets from capture–recapture or removal sampling techniques (often derived from trapping grids) from which separate estimates of population size (N) and effective sampling area (Â) are used to calculate density (D = N/Â); and models applicable to sampling regimes using distance-sampling theory (typically transect lines or trapping webs) to estimate detection functions and densities directly from the distance data. However, few studies have evaluated these respective models for accuracy, precision, and bias on known field populations, and no studies have been conducted that compare the two approaches under controlled field conditions. In this study, we evaluated both classes of density estimators on known densities of e...

Satellite imagery characterizes local animal reservoir populations of Sin Nombre virus in the southwestern United States

The relationship between the risk of hantaviral pulmonary syndrome (HPS), as estimated from satellite imagery, and local rodent populations was examined. HPS risk, predicted before rodent sampling, was highly associated with the abundance of Peromyscus maniculatus, the reservoir of Sin Nombre virus (SNV). P. maniculatus were common in high-risk sites, and populations in high-risk areas were skewed toward adult males, the subclass most frequently infected with SNV. In the year after an El Niño Southern Oscillation (ENSO), captures of P. maniculatus increased only in high-risk areas. During 1998, few sites had infected mice, but by 1999, 18/20 of the high-risk sites contained infected mice and the crude prevalence was 30.8%. Only 1/18 of the low-risk sites contained infected rodents, and the prevalence of infection was lower (8.3%). Satellite imagery identified environmental features associated with SNV transmission within its reservoir population, but at least 2 years of high-risk conditions were needed for SNV to reach high prevalence. Areas with persistently high-risk environmental conditions may serve as refugia for the survival of SNV in local mouse populations.

Hantavirus in Northern Short-tailed Shrew, United States

Phylogenetic analyses, based on partial medium- and large-segment sequences, support an ancient evolutionary origin of a genetically distinct hantavirus detected by reverse transcription–PCR in tissues of northern short-tailed shrews (Blarina brevicauda) captured in Minnesota in August 1998. To our knowledge, this is the first evidence of hantaviruses harbored by shrews in the Americas.

DEMOGRAPHIC FACTORS ASSOCIATED WITH PREVALENCE OF ANTIBODY TO SIN NOMBRE VIRUS IN DEER MICE IN THE WESTERN UNITED STATES

We used long-term data collected for up to 10 yr (1994–2004) at 23 trapping arrays (i.e., webs and grids) in Arizona, Colorado, Montana, and New Mexico to examine demographic factors known or suspected to be associated with risk of infection with Sin Nombre virus (SNV) in its natural host, the deer mouse (Peromyscus maniculatus). Gender, age (mass), wounds or scars, season, and local relative population densities were statistically associated with the period prevalence of antibody (used as a marker of infection) to SNV in host populations. Nevertheless, antibody prevalence and some of the risk factors associated with antibody prevalence, such as relative population density, gender bias, and prevalence of wounding, varied significantly among sites and even between nearby trapping arrays at a single site. This suggests that local microsite-specific differences play an important role in determining relative risk of infection by SNV in rodents and, consequently, in humans. Deer mouse relative population density varied among sites and was positively and statistically associated with infection prevalence, an association that researchers conducting shorter-term studies failed to demonstrate. Both wounding and antibody prevalence increased with mass class in both males and females; this increase was much more pronounced in males than in females and wounding was more frequent in adult males than in adult females. Prevalence of wounding was greatest among seropositive deer mice, regardless of mass class, but many deer mice without detectable wounds or scars eventually became infected. Many of these patterns, which will be useful in the development of predictive models of disease risk to humans, were only detected through the application of data collected over a long (10-yr) period and with abundant replication.

SMALL MAMMAL SURVIVAL AND TRAPABILITY IN MARK-RECAPTURE MONITORING PROGRAMS FOR HANTAVIRUS

Following the 1993 hantavirus pulmonary syndrome (HPS) epidemic in the southwestern United States, mammalogists and epidemiologists instituted long-term studies to monitor population density and prevalence of infection in rodents which constitute the reservoir for Sin Nombre virus (SNV). In this study, field techniques used in sampling small mammals for SNV infection were evaluated to determine if trapping and handling protocols were having significant effects on future trapability or mortality of animals. We compared rodent mark-recapture control plots, on which all rodents were simply measured, marked, and released on site, with experimental plots on which all animals were anesthetized with methoxyflurane, sampled for blood and saliva, measured, marked, and released. Blood samples were obtained from anesthetized animals on the experimental plots via a retro-orbital sinus puncture using a heparinized capillary tube. Dacron tipped oral swabs were used to collect buccal cells and saliva from the rodents oral cavity. Field data were collected monthly from August 1994 to August 1996 at two sites in New Mexico (USA). Analyses were based on 3,661 captures of 1,513 individuals representing 21 species from three rodent families (Rodentia: Muridae, Heteromyidae, Sciuridae) and two species of rabbits (Lagomorpha: Leporidae). Overall, for most murid rodents (including five Peromyscus spp., Neotoma albigula, and Onychomys leucogaster) and one rabbit species (Sylvilagus floridanus), the handling/bleeding procedures had no significant effects on recapture rates or mortality. In contrast, several species of heteromyids (Dipodomys ordii and Perognathus flavus), one murid (Reithrodontomys megalotis) and one leporid (S. auduboni) suffered higher mortality rates, and heteromyid kangaroo rats (D. ordii and D. merriami) exhibited lower trapability as a result of the anesthesia and sampling procedures. In view of the overall non-significant influence of the sampling procedures on murid rodents, the anesthesia and blood/saliva sampling protocols described herein appear to be appropriate for hantavirus research, and may serve as a model for environmental monitoring of other zoonotic agents and their reservoirs.

Statistical Sensitivity for Detection of Spatial and Temporal Patterns in Rodent Population Densities

A long-term monitoring program begun 1 year after the epidemic of hantavirus pulmonary syndrome in the U.S. Southwest tracked rodent density changes through time and among sites and related these changes to hanta–virus infection rates in various small-mammal reservoir species and human disease outbreaks. We assessed the statistical sensitivity of the programs field design and tested for potential biases in population estimates due to unintended deaths of rodents. Analyzing data from two sites in New Mexico from 1994 to 1998, we found that for many species of Peromyscus, Reithrodontomys, Neotoma, Dipodomys, and Perognathus, the monitoring program detected species-specific spatial and temporal differences in rodent densities; trap-related deaths did not significantly affect long-term population estimates. The program also detected a short-term increase in rodent densities in the winter of 1997-98, demonstrating its usefulness in identifying conditions conducive to increased risk for human disease.

Toward a Mechanistic Understanding of Environmentally Forced Zoonotic Disease Emergence: Sin Nombre Hantavirus

Abstract Understanding the environmental drivers of zoonotic reservoir and human interactions is crucial to understanding disease risk, but these drivers are poorly predicted. We propose a mechanistic understanding of human–reservoir interactions, using hantavirus pulmonary syndrome as a case study. Crucial processes underpinning the diseases incidence remain poorly studied, including the connectivity among natural and peridomestic deer mouse host activity, virus transmission, and human exposure. We found that disease cases were greatest in arid states and declined exponentially with increasing precipitation. Within arid environments, relatively rare climatic conditions (e.g., El Niño) are associated with increased rainfall and reservoir abundance, producing more frequent virus transmission and host dispersal. We suggest that deer mice increase their occupancy of peridomestic structures during spring–summer, amplifying intraspecific transmission and human infection risk. Disease incidence in arid states may increase with predicted climatic changes. Mechanistic approaches incorporating reservoir behavior, reservoir–human interactions, and pathogen spillover could enhance our understanding of global hantavirus ecology, with applications to other directly transmitted zoonoses.

Primary Succession on the Mount St. Helens Volcano: Ground Beetle (Coleoptera: Carabidae) Community Assembly and Species Turnover, 1980–2010

We documented the recruitment, loss, and turnover of 51 species of ground beetles during 30 years of post-eruption primary succession on the Pumice Plain near Spirit Lake at Mount St. Helens. We observed high species turnover, with many species colonizing, expanding their populations, and then declining to local extinction over periods of 10–15 years. Species patterns were related to soil and vegetation development, accrual of prey species, and natural-history characteristics of the resident species (e.g., trophic role, dispersal traits (flight/ambulatory), microhabitat preferences, seasonal/daily activity times). Overall, species successional turnover rates were substantially higher than plants and vertebrate wildlife species.