Declining ecosystem health and the dilution effect

Abstract

The “dilution effect” implies that where species vary in susceptibility to infection by a pathogen, higher diversity often leads to lower infection prevalence in hosts. For directly transmitted pathogens, non-host species may “dilute” infection directly (1) and indirectly (2). Competitors and predators may (1) alter host behavior to reduce pathogen transmission or (2) reduce host density. In a well-studied system, we tested the dilution of the zoonotic Puumala hantavirus (PUUV) in bank voles (Myodes glareolus) by two competitors and a predator. Our study was based on long-term PUUV infection data (2003–2013) in northern Sweden. The field vole (Microtus agrestis) and the common shrew (Sorex araneus) are bank vole competitors and Tengmalm’s owl (Aegolius funereus) is a main predator of bank voles. Infection probability in bank voles decreased when common shrew density increased, suggesting that common shrews reduced PUUV transmission. Field voles suppressed bank vole density in meadows and clear-cuts and indirectly diluted PUUV infection. Further, Tengmalm’s owl decline in 1980–2013 may have contributed to higher PUUV infection rates in bank voles in 2003–2013 compared to 1979–1986. Our study provides further evidence for dilution effect and suggests that owls may have an important role in reducing disease risk.

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

“…This is not surprising as pathogen prevalence can be independent of host density via diversity‐driven reduction in encounter rate (e.g., Clay, Lehmer, St Jeor, et al., 2009b; Keesing, Holt, & Ostfeld, 2006), even though pathogen prevalence and number of infected hosts are generally related to overall host abundance (reviewed by Khalil, Hornfeldt, et al., 2014). Our results suggest that a more simplified small mammal community dominated by M. glareolus increases risk for humans (see also Khalil et al., 2016). Vole cycle XI (starting in spring 2006 and ending in spring 2009) was overall characterized by the highest density (except for cycle I; Figure 2) and high community contribution of M. glareolus (Figure 6), the highest number of PUUV‐infected M. glareolus and the highest PUUV prevalence (Figure 9).…”

“…In our study, both the number of PUUV‐infected M. glareolus and PUUV prevalence appeared to increase when the replacement (turnover) of shrew species (replaced by voles) among sites increased. This latter result supports the most recently suggested regulatory role of shrews for disease risk by “encounter reduction” (see Keesing et al., 2006 for reduction concepts), that is, potential shrew‐induced reduced contact rates among M. glareolus (Khalil et al., 2016). Our results indicate the presence of a dilution effect in the study system and pose a rare opportunity to test in detail the concept and related mechanisms of the dilution effect on PUUV to be analyzed in biobanked M. glareolus specimens (Odsjö, 2006; Hörnfeldt, 2015) for the entire period 1979 to present, that is, the time period covering the here presented study.…”

“…Data on PUUV‐antibody positive bank voles in spring and autumn were available for the vole cycles III‐IV (Niklasson, Hörnfeldt, Lundkvist, Björsten, & Leduc, 1995) and X‐XII and as Khalil et al. (2016) we excluded bank voles with maternal antibodies in any cycle from the analyses. We calculated the cumulated number of infected bank voles and average PUUV prevalence per cycle, for spring data, by first aggregating data per cycle from spring of the increase phase/year up to and throughout the year before the next cycle's increase phase/year.…”

“…Fourth, we discuss the implications of our results for ecosystem functioning of the boreal forest system in terms of PUUV dynamics and transmission risk. To achieve this, we analyze if altered disease dynamics (as shown by the cumulated number of PUUV‐infected bank voles and average PUUV‐prevalence per cycle) are related to not only changes in population dynamics of small mammals (as shown in Khalil et al., 2016) but also to changes in their diversity. Considering the increasing evidence for the importance of diversity for pathogen prevalence in, for example, hantavirus systems (Clay, Lehmer, St Jeor, & Dearing, 2009a,b; Dizney & Dearing, 2016; Dizney & Ruedas, 2009; Suzán et al., 2009), we expect that any long‐term changes in small mammal diversity would also be reflected in altered pathogen dynamics.…”

The wild life of tick-borne pathogens

“…There is some empirical evidence that this might be the case. For example, Khalil et al 293 showed that the presence of competitors and predators reduced Puumala hantavirus prevalence in Bank voles (Myodes glareolus), and I showed that the presence of predators and competitors can reduce the tick burden on rodents, resulting in a reduction of tick-borne disease risk (Chapter 5-6). Although these studies did not investigate how predators and competitors changed vector and pathogen prevalence, both speculated that the behaviour of hosts might play a large role.…”