Robert R. 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.

Guidelines for Working with Rodents Potentially Infected with Hantavirus

Because of the high morbidity and mortality associated with hantavirus pulmonary syndrome and the possibility of aerosol transmission of hantaviruses, persons handling known reservoir species in the field, laboratory, or classroom should take special precautions to minimize the risk of infection. We provide specific guidelines for personal safety while trapping, handling and releasing, transporting, sampling, and performing necropsy on potentially infected rodents or teaching field classes in areas occupied by reservoir species. Special consideration should be given to respiratory protection, choice and use of disinfectants, decontamination of instruments and traps, proper disposal of infectious wastes, and preservation and shipment of samples intended for hantavirus testing. Precautionary testing of wild rodents used to start laboratory colonies is recommended. Although we specifically address hantaviruses, the procedures described are applicable for any study of populations of small mammals when an infectious zoonotic agent transmissible by aerosol and capable of causing high morbidity and mortality is involved.

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...

Traveling waves of infection in the hantavirus epidemics.

Traveling waves are analyzed in a model of the hantavirus infection in deer mice. The existence of two kinds of wave phenomena is predicted. An environmental parameter governs a transition between two regimes of propagation. In one of them the front of infection lags behind at a constant rate. In the other, fronts of susceptible and infected mice travel at the same speed, separated by a constant delay. The dependence of the delay on system parameters is analyzed numerically and through a piecewise linearization.

Integrating Patch and Boundary Dynamics to Understand and Predict Biotic Transitions at Multiple Scales

Human modification of landscapes overlying natural environmental heterogeneity is resulting in an increase in the numbers and types of ecological patches and their intervening boundaries. In this paper, we describe an operational framework for understanding and predicting dynamics of these biotic transitions for a range of environmental conditions across multiple spatial scales. We define biotic transitions as the boundary and the neighboring states, a more general definition than typically denoted by the terms boundary, ecotone, edge or gradient. We use concepts of patch dynamics to understand the structural properties of biotic transitions and to predict changes in boundaries through time and across space. We develop testable hypotheses, and illustrate the utility of our approach with examples from arid and semiarid ecosystems. Our framework provides new insights and predictions as to how landscapes may respond to future changes in climate and other environmental drivers.

PERSISTENTLY HIGHEST RISK AREAS FOR HANTAVIRUS PULMONARY SYNDROME: POTENTIAL SITES FOR REFUGIA

Interannual variation in the number of cases of human disease caused by hantaviruses in North America has been hypothesized to reflect environmental changes that influence rodent reservoir populations. This hypothesis postulates that when cases are rare reservoir populations are geographically restricted in patches of suitable habitat. Identifying these sites, which is needed to test the hypothesis, has proven to be a challenge. Satellite imagery of the U.S. Southwest has shown associations among the likelihood of human hantaviral disease and increases in the rodent populations, as well as increased prevalence of Sin Nombre virus (SNV) in rodent populations. In this study we characterize local areas that had environmental signatures that persisted as predicted highest risk sites for human disease through much of the 1990s. These areas represent a small percentage (0.3%) of the region. Exploratory analyses indicate that these areas were not randomly distributed, but were associated with certain landscape characteristics. Characteristics of elevation, slope, aspect, and land cover were associated with persistent high risk. Using multivariate Poisson regression to control for confounding effects, sites with deciduous- or mixed-forest land cover on moderate to steep slopes (>5 degrees) above 2130 m elevation were associated with increasing numbers of years at highest risk. These are candidate locations for refugia. Sites associated with cleared ground or shrubland were less often associated with high risk compared to reference conditions. The seasonal patterns of vegetation growth in persistently high-risk areas were compared to matched locations using MODIS (moderate resolution imaging spectroradiometer) NDVI (normalized difference vegetation index) during a time of a severe drought in the region from 2002 to 2004. Despite the drought and regardless of land cover, the NDVI in persistently highest risk areas had an early onset, with significantly higher levels of green vegetation that lasted longer than at comparable sites. These observations identify locations that can be monitored for the abundance of P. maniculatus and presence of SNV. If these sites are refugia, we predict they will be occupied by infected deer mice when other monitored sites are unoccupied.

The Effect of Habitat Fragmentation and Species Diversity Loss on Hantavirus Prevalence in Panama

Habitat fragmentation and diversity loss due to increased conversion of natural habitats to agricultural uses influence the distribution and abundance of wildlife species and thus may change the ecology of pathogen transmission. We used hantaviruses in Panama as a research model to determine whether anthropogenic environmental change is associated with changes in the dynamics of viral transmission. Specifically, we wanted to determine whether hantavirus infection was correlated with spatial attributes of the landscape at both large and small scales or whether these changes are mediated by changes in community composition. When analyzed at coarse spatial scales, hantavirus reservoirs were more commonly found in disturbed habitats and edge habitats than in forested areas. At local scales, reservoir species dominance was significantly correlated with the slope of the terrain. To evaluate the effect of small‐mammal diversity loss on infection dynamics, we implemented an experiment with selective species removal at experimental sites. Seroprevalence of hantavirus was higher in the community of small mammals and increased through time in the experimental sites. The higher seroprevalence in experimental plots suggests that greater diversity likely reduces encounter rates between infected and susceptible hosts. Our studies suggest that habitat loss and fragmentation and species diversity loss are altering hantavirus infection dynamics in Panama. Our work represents a multidisciplinary approach toward disease research that includes biodiversity concerns such as environmental change and degradation, human settlement patterns, and the ecology of host and nonhost species, work that may be especially important in tropical countries.

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.

Responses of a Riparian Forest-Floor Arthropod Community to Wildfire in the Middle Rio Grande Valley, New Mexico

Abstract We documented patterns of species extirpation, shifts in species dominance, and rates of recolonization of litter-layer arthropod species following a catastrophic forest fire. The study site was located along the Rio Grande within the Bosque del Apache National Wildlife Refuge, Socorro County, NM, in a riparian forest dominated by cottonwood [Populus deltoides ssp. wislizenii (S. Watson) Eckenwalder] and salt cedar (Tamarix chinensis Loureiro). The forest-floor arthropod community was sampled with 18 pitfall traps during 1994–1997. The study site burned in June 1996, and the intense fire reduced the litter layer to mineral ash and killed all the above-ground portions of trees; salt cedar and some cottonwood trees began to stump-sprout shortly after the fire, and achieved heights of two m by October 1996. The prefire forest-floor arthropod community consisted of 80 species, dominated by spiders (Lycosidae, Gnaphosidae, Salticidae), beetles (Carabidae, Staphylinidae, Cryptophagidae, Tenebrionidae), isopods (Armadillidae, Porcellionidae) and crickets (Gryllidae). The surviving postfire arthropod community was dominated by generalist ants (Formicidae). The dominant cricket, Gryllus alogus Rehn (Orthoptera: Gryllidae), exhibited a rapid recovery in abundance following the fire, and the number of certain species that preferred open, bare-ground habitat [e.g., the tiger beetle Cicindela punctulata Olivier (Coleoptera: Carabidae)] increased on the burned site. During the 9 mo following the fire, 79 arthropod species were recorded from the fire site, 29 (37%) of which had not been recorded before the fire. Of the original prefire 80 arthropod species, 30 species (37%) were not recorded after the fire, and overall arthropod abundance was substantially reduced. The extirpated species were generally uncommon before the fire, while the more abundant species displayed more successful recolonization. These results suggest that wildfire in the Rio Grande riparian forest of New Mexico can have a substantial, short-term impact on abundance and species composition of the forest-floor arthropod community, and that both survivor activity and recolonization processes by dominant species can be rapid. Given the capacity for rapid recolonization by these arthropod species, the long-term recovery of the forest-floor arthropod assemblage will likely be driven by the postfire recovery rate of the plant community and eventual structure and composition of the forest floor litter layer.

Responses of Small Mammals and Vegetation to a Reintroduction of Gunnison's Prairie Dogs

This study addressed the initial effects of a reintroduction of Gunnisons prairie dogs ( Cynomys gunnisoni ) on resident small mammal and plant communities on the Sevilleta National Wildlife Refuge (SNWR), New Mexico. In spring 1997, 60 prairie dogs (36.8 kg live mass) were introduced onto a former prairie dog colony in a desert grassland site. Small mammals and vegetation were sampled on both a treatment (reintroduction site) and a control site (without prairie dogs) before and after the prairie dogs were reintroduced. We tested for differences in small mammal and plant community change during the 1st year of the colonys existence using repeated measures analysis of variance. Although prairie dog biomass was ca. 32 times greater than that of the resident rodent community (1.2 kg), reintroduction of prairie dogs had no significant effect on the resident small mammal and plant communities. Total biomass and abundance of rodents, and percent cover and species richness of plants did not change during the 1st year following reintroduction of prairie dogs. However, two rodent species showed significant differences in abundance between the prairie dog colony and the control site. The banner-tailed kangaroo rat ( Dipodomys spectabilis ) was significantly more abundant on the treatment site before and after reintroduction of prairie dogs. In contrast, the white-footed mouse ( Peromyscus leucopus ) was significantly more abundant on the control site following reintroduction of prairie dogs. Habitat modifications made by the former prairie dog colony may be responsible for the habitat preferences observed by D. spectabilis and P. leucopus . Although reintroduction of prairie dogs had no observable influence on the resident small mammal and plant communities in the short-term, their influences may be more evident on a long-term time scale.