Dampening of population cycles in voles affects small mammal community structure, decreases diversity, and increases prevalence of a zoonotic disease.

Frauke Ecke,David G Angeler,Magnus Magnusson,Hussein Khalil,Birger Hörnfeldt

doi:10.1002/ece3.3074

Abstract

Long‐term decline and depression of density in cyclic small rodents is a recent widespread phenomenon. These observed changes at the population level might have cascading effects at the ecosystem level. Here, we assessed relationships between changing boreal landscapes and biodiversity changes of small mammal communities. We also inferred potential effects of observed community changes for increased transmission risk of Puumala virus (PUUV) spread, causing the zoonotic disease nephropatica epidemica in humans. Analyses were based on long‐term (1971–2013) monitoring data of shrews and voles representing 58 time series in northern Sweden. We calculated richness, diversity, and evenness at alpha, beta, and gamma level, partitioned beta diversity into turnover (species replacement) and nestedness (species addition/removal), used similarity percentages (SIMPER) analysis to assess community structure, and calculated the cumulated number of PUUV‐infected bank voles and average PUUV prevalence (percentage of infected bank voles) per vole cycle. Alpha, beta, and gamma richness and diversity of voles, but not shrews, showed long‐term trends that varied spatially. The observed patterns were associated with an increase in community contribution of bank vole (Myodes glareolus), a decrease of gray‐sided vole (M. rufocanus) and field vole (Microtus agrestis) and a hump‐shaped variation in contribution of common shrew (Sorex araneus). Long‐term biodiversity changes were largely related to changes in forest landscape structure. Number of PUUV‐infected bank voles in spring was negatively related to beta and gamma diversity, and positively related to turnover of shrews (replaced by voles) and to community contribution of bank voles. The latter was also positively related to average PUUV prevalence in spring. We showed that long‐term changes in the boreal landscape contributed to explain the decrease in biodiversity and the change in structure of small mammal communities. In addition, our results suggest decrease in small mammal diversity to have knock‐on effects on dynamics of infectious diseases among small mammals with potential implications for disease transmission to humans.

Highlights

The global loss of biodiversity has become a major concern as it negatively affects ecosystem functioning and potentially alters the emergence and transmission of infectious diseases (Balvanera et al, 2006; Hooper et al, 2012; Keesing et al, 2010; Loreau et al, 2001)
Pathogens hosted by small mammals and transmitted to humans include the Puumala virus (PUUV) hosted by the bank vole (Myodes glareolus Schreber) (Brummer-Korvenkontio et al, 1980) and causing nephropatia epidemica (NE), a hemorrhagic fever in humans, sometimes leading to kidney failure, and in rare cases to death (Vapalahti et al, 2003)
Average PUUV prevalence in spring per cycle was negatively correlated with beta diversity (τ = −0.949, FIGURE 6 Temporal changes (n = 11 and not 12 due to analysis of temporal changes between consecutive cycles) in (a) similarity between consecutive cycles based on trapping indices and (b–e) contribution (%) of the respective small mammal species to the observed changes in similarity in 12 cycles 1972–2012

Summary

| INTRODUCTION

The global loss of biodiversity has become a major concern as it negatively affects ecosystem functioning and potentially alters the emergence and transmission of infectious diseases (Balvanera et al, 2006; Hooper et al, 2012; Keesing et al, 2010; Loreau et al, 2001). Long-term decline and depression of density in cyclic voles has become a widespread phenomenon (Cornulier et al, 2013; Hörnfeldt, 2004; Ims, Henden, & Killengreen, 2008) The causes of these declines are largely unknown, but probably involve multiple elements including climatic factors (Cornulier et al, 2013; Kausrud et al, 2008; Korpela et al, 2013, 2014) and, at least in Sweden, landscape changes (Magnusson, Hörnfeldt, & Ecke, 2015). Despite observed changes in the small mammal population dynamics potentially affecting structural and functional patterns at the ecosystem level (Hörnfeldt, Hipkiss, & Eklund, 2005; Ims et al, 2008; FIGURE 1 Vole in a stone hole (Photo credit: Rolf Segerstedt). We assess these changes for taxon richness and diversity (exponential Shannon entropy) that cover distinct ecological phenomena, with richness focusing only on species presence–absence patterns and diversity covering both species abundances and ECKE et al (a)

| MATERIAL AND METHODS

Findings

| DISCUSSION