Population Density and Seasonality Effects on Sin Nombre Virus Transmission in North American Deermice (Peromyscus maniculatus) in Outdoor Enclosures

Karoun H Bagamian,Richard J Douglass,James N Mills,Brian R Amman,Amy J Kuenzi,Lance A Waller,Arlene Alvarado,Frederick R Adler

doi:10.1371/journal.pone.0037254

Karoun H Bagamian, Richard J Douglass + Show 6 more

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https://doi.org/10.1371/journal.pone.0037254

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Abstract

Surveys of wildlife host-pathogen systems often document clear seasonal variation in transmission; conclusions concerning the relationship between host population density and transmission vary. In the field, effects of seasonality and population density on natural disease cycles are challenging to measure independently, but laboratory experiments may poorly reflect what happens in nature. Outdoor manipulative experiments are an alternative that controls for some variables in a relatively natural environment. Using outdoor enclosures, we tested effects of North American deermouse (Peromyscus maniculatus) population density and season on transmission dynamics of Sin Nombre hantavirus. In early summer, mid-summer, late summer, and fall 2007–2008, predetermined numbers of infected and uninfected adult wild deermice were released into enclosures and trapped weekly or bi-weekly. We documented 18 transmission events and observed significant seasonal effects on transmission, wounding frequency, and host breeding condition. Apparent differences in transmission incidence or wounding frequency between high- and low-density treatments were not statistically significant. However, high host density was associated with a lower proportion of males with scrotal testes. Seasonality may have a stronger influence on disease transmission dynamics than host population density, and density effects cannot be considered independent of seasonality.

Highlights

In the past 30 years, numerous theoretical models have been proposed to explain how pathogens become established and spread in host populations
Infection prevalence in wild rodent populations is often associated with host population densities and dynamics in a prior season, an effect known as delayed densitydependent prevalence [11,12,13,14]
Regional wild North American deermouse (Peromyscus maniculatus; hereafter deermouse) populations in Montana show maximum Sin Nombre hantavirus (SNV) infection in the spring, and this peak is often positively associated with the size of the deermouse population the preceding fall [13,15]

Summary

Introduction

In the past 30 years, numerous theoretical models have been proposed to explain how pathogens become established and spread in host populations. For a horizontally transmitted pathogen, higher host population density may lead to higher prevalence of infection, because there is an increased number of potential hosts and because more susceptible hosts provide more opportunities for direct transmission through contact [3]. Higher densities of infective donors and susceptible hosts may amplify indirect transmission by increasing the amount of infectious pathogen in the environment [4]. While some mark-recapture studies of hantaviruses and arenaviruses in rodent populations in the United States and Europe have indicated a positive concurrent relationship between host population density and infection prevalence [6,7], others showed an inverse relationship or no direct association [8,9,10]. Some directly transmitted wildlife pathogens display characteristics of frequency-dependent dynamics (where transmission likelihood is independent of population density) [16,17], or transmission dynamics that vary between density and frequency dependence according to season [18]

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